Thinning affects microbial biomass without changing enzyme activity in the soil of Pinus densiflora Sieb. et Zucc. forests after 7 years

  • Seongjun Kim
  • Guanlin Li
  • Seung Hyun Han
  • Hyun-Jun Kim
  • Choonsig Kim
  • Sang-Tae Lee
  • Yowhan Son
Original Paper


Key message

Thinning increased microbial biomass but did not alter enzyme activities in the soil of Pinus densiflora Sieb. et Zucc. forests in South Korea. This effect of thinning was larger under a relatively heavy thinning intensity, but there was divergence in the magnitude between sites.


The balance between microbial biomass accumulation and enzymatic C and N assimilation determines the level of bio-available C and N. However, the effects of thinning on these parameters remain contradictory and unconfirmed.


The effects of thinning intensity on microbial biomass and enzyme activity were assessed in the soil of Pinus densiflora Sieb. et Zucc. forests in South Korea.


Un-thinned control and 15 and 30% basal area thinning treatments were applied to two 51- to 60-year-old P. densiflora forests with different management histories, topographies, rainfall amounts, and soils. Seven years after thinning, microbial biomass and activities of N-acetyl-glucosaminidase, β-glucosidase, cellobiohydrolase, β-xylosidase, phenol oxidase, and peroxidase were measured before and after seasonally concentrated rains and at 0–10 cm depth.


Microbial biomass was generally highest under the 30% basal area thinning and lowest under the control, and was positively correlated to total soil C and N. The increase in microbial biomass was lower at the site displaying sandier, drier, and more acidic soils and retaining smaller amounts of thinning residue. Conversely, thinning had no significant effect on activities of all enzymes at both sites in both periods.


Thinning can promote accumulation of microbial biomass without significant change in enzyme activities participating in the assimilation of C and N. This effect of thinning tended to increase with thinning intensity but differed in magnitude between sites.


Enzyme assay Forest management Korean red pine Soil microbes 



We thank Jongyeol LEE, Sohye LEE, Hanna CHANG, Hyeon Min YUN, Min Ji PARK, Suwon CHOI, Jiae AN, and Yujin ROH for their assistance in both field and laboratory.

Supplementary material

13595_2018_690_MOESM1_ESM.docx (93 kb)
Table S1 (DOCX 92 kb)
13595_2018_690_MOESM2_ESM.docx (94 kb)
Table S2 (DOCX 93 kb)


  1. Adamczyk F, Adamczyk S, Kukkola M, Tamminen P, Smolander A (2015) Logging residue harvest may decrease enzymatic activity of boreal forest soils. Soil Biol Biochem 82:74–80. CrossRefGoogle Scholar
  2. Baena CW, Andrés-Abellán M, Lucas-Borja ME, Martínez-García E, García-Morote FA, Rubio E, López-Serrano FR (2013) Thinning and recovery effects on soil properties in two sites of a Mediterranean forest, in Cuenca Mountain (south-eastern of Spain). For Ecol Manag 308:223–230. CrossRefGoogle Scholar
  3. Benesch M, Glaser B, Dippold M, Zech W (2015) Soil microbial C and N turnover under Cupressus lusitanica and natural forests in southern Ethiopia assessed by decomposition of 13C- and 15N-labelled litter under field conditions. Plant Soil 388:133–146. CrossRefGoogle Scholar
  4. Boerner REJ, Giai C, Huang J, Miesel JR (2008) Initial effects of fire and mechanical thinning on soil enzyme activity and nitrogen transformations in eight North American forest ecosystems. Soil Biol Biochem 40:3076–3085. CrossRefGoogle Scholar
  5. Bolat Í (2014) The effect of thinning on microbial biomass C, N and basal respiration in black pine forest soils in Mudurnu, Turkey. Eur J For Res 133:131–139. CrossRefGoogle Scholar
  6. Bonde TA, Schnürer J, Rosswall T (1988) Microbial biomass as a fraction of potentially mineralizable nitrogen in soils from long-term field experiments. Soil Biol Biochem 20:447–452. CrossRefGoogle Scholar
  7. Boyle SI, Hart SC, Kaye JP, Waldrop MP (2005) Restoration and canopy type influence soil microflora in a ponderosa pine forest. Soil Sci Soc Am J 69:1627–1638. CrossRefGoogle Scholar
  8. Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842. CrossRefGoogle Scholar
  9. Brown IC (1943) A rapid method of determining exchangeable hydrogen and total exchangeable bases of soils. Soil Sci 56:353–357CrossRefGoogle Scholar
  10. Chen X-L, Wang D, Chen X, Wang J, Diao J-J, Zhang J-Y, Guan Q-W (2015) Soil microbial functional diversity and biomass as affected by different thinning intensities in a Chinese fir plantation. Appl Soil Ecol 92:35–44. CrossRefGoogle Scholar
  11. Chen X, Chen HYH, Chen X, Wang J, Chen B, Wang D, Guan Q (2016) Soil labile organic carbon and carbon-cycle enzyme activities under different thinning intensities in Chinese fir plantations. Appl Soil Ecol 107:162–169. CrossRefGoogle Scholar
  12. Dannenmann M, Gasche R, Ledebuhr A, Papen H (2006) Effects of forest management on soil N cycling in beech forests stocking on calcareous soils. Plant Soil 287:279–300. CrossRefGoogle Scholar
  13. 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 41:1180–1186. CrossRefGoogle Scholar
  14. Domínguez MT, Holthol E, Smith AR, Koller E, Emmett BA (2017) Contrasting response of summer soil respiration and enzyme activities to long-term warming and drought in a wet shrubland (WD Wales, UK). Appl Soil Ecol 110:151–155. CrossRefGoogle Scholar
  15. Flint LE, Flint AL (2002) Porosity. In: Campbell GS, Horton R, Jury WA, Nielsen DR, van Es HM, Wierenga PJ, Dane JH, Topp GC (eds) Methods of soil analysis. Part 4-physical methods. SSSA, Wisconsin, pp 255–293Google Scholar
  16. Gee GW, Or D (2002) Particle-size analysis. In: Campbell GS, Horton R, Jury WA, Nielsen DR, van Es HM, Wierenga PJ, Dane JH, Topp GC (eds) Methods of soil analysis. Part 4-physical methods. SSSA, Wisconsin, pp 255–293Google Scholar
  17. Geng Y, Dighton J, Gray D (2012) The effects of thinning and soil disturbance on enzyme activities under pitch pine soil in New Jersey Pinelands. Appl Soil Ecol 62:1–7. CrossRefGoogle Scholar
  18. Hodge A, Robinson D, Fitter A (2000) Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci 5:304–308. CrossRefPubMedGoogle Scholar
  19. Huang J, Wu P, Zhao X (2013) Effects of rainfall intensity, underlying surface and slope gradient on soil infiltration under simulated rainfall experiments. Catena 104:93–102. CrossRefGoogle Scholar
  20. Joergensen RG, Mueller T (1996) The fumigation-extraction method to estimate soil microbial biomass: calibration of the KEN value. Soil Biol Biochem 28:33–37. CrossRefGoogle Scholar
  21. Kim C, Son Y, Lee W-K, Jeong J, Noh N-J, Kim S-R, Yang A-R (2012) Litter decomposition and nutrient dynamics following forest tending (Soopkakkugi) works in a Pinus densiflora stand. For Sci Technol 8:99–104. Google Scholar
  22. Kim D-H, Kim J-H, Park J-H, Ewane EB, Lee D-H (2016a) Correlation between above-ground and below-ground biomass of 13-year-old Pinus densiflora S. et Z. planted in a post-fire area in Samcheok. For Sci Technol 12:115–124. Google Scholar
  23. Kim M, Lee W-K, Kim Y-S, Lim C-H, Song C, Park T, Son Y, Son Y-M (2016b) Impact of thinning intensity on the diameter and height growth of Larix kaempferi stands in central Korea. For Sci Technol 12:77–87. Google Scholar
  24. Kim S, Han SH, Li G, Yoon TK, Lee S-T, Kim C, Son Y (2016c) Effects of thinning intensity on nutrient concentration and enzyme activity in Larix kaempferi forest soils. J Ecol Environ 40:2. CrossRefGoogle Scholar
  25. Kim S, Li G, Han SH, Chang H, Kim H-J, Son Y (2017) Differential effects of coarse woody debris on microbial and soil properties in Pinus densiflora Sieb. Zucc forests Forests 8:292. Google Scholar
  26. Ko S, Yoon TK, Kim S, Kim C, Lee S-T, Seo KW, Son Y (2014) Thinning intensity effects on carbon storage of soil, forest floor and coarse woody debris in Pinus densiflora stands. J Korean For Soc 103:30–36. (in Korean) CrossRefGoogle Scholar
  27. Korea Forest Research Institute (2012) Forestry handbook. Korea Forest Research Institute, Seoul (in Korean) Google Scholar
  28. Korea Forest Service (2015) Statistical yearbook of forestry. Korea Forest Service, Daejeon (in Korean) Google Scholar
  29. Korea Meteorological Administration (2011) Climatological normals of Korea. Korea Meteorological Administration, Seoul (in Korean) Google Scholar
  30. Korea Meteorological Administration (2015) Annual climatological report. Korea Meteorological Administration, Seoul (in Korean) Google Scholar
  31. Lee CS, Kim JH (1987) Relationships between soil factors and growth of annual ring in Pinus densiflora on stony mountain. Korea J Ecol 10:151–159Google Scholar
  32. Maassen S, Fritze H, Wirth S (2006) Response of soil microbial biomass, activities, and community structure at a pine stand in northeastern Germany 5 years after thinning. Can J For Res 36:1427–1434. CrossRefGoogle Scholar
  33. Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5:785–803. CrossRefGoogle Scholar
  34. Moorhead DL, Rinkes ZL, Sinsabaugh RL, Weintraub MN (2013) Dynamic relationships between microbial biomass, respiration, inorganic nutrients and enzyme activities: informing enzyme-based decomposition models. Front Microbiol 4:1–12. CrossRefGoogle Scholar
  35. Mulvaney RL (1996) Nitrogen-inorganic forms. In: Sparks DL, Page AL, Helmke PA, Loeppert RH, Soltanpour PN, Tabatabai MA, Johnston CT, Sumner ME (eds) Methods of soil analysis. Part 3-chemical methods. SSSA and ASA, Wisconsin, pp 1146–1155Google Scholar
  36. Nannipieri PN, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670. CrossRefGoogle Scholar
  37. Nelson DW, Sommers LE (1996) Total carbon, organic carbon, and organic matter. In: Sparks DL, Page AL, Helmke PA, Loeppert RH, Soltanpour PN, Tabatabai MA, Johnston CT, Sumner ME (eds) Methods of soil analysis. Part 3-chemical methods. SSSA and ASA, Wisconsin, pp 961–1010Google Scholar
  38. Page-Dumroese DS, Jurgensen MF, Brown RE, Mroz GD (1999) Comparison of methods for determining bulk densities of rocky forest soils. Soil Sci Soc Am J 63:379–383. CrossRefGoogle Scholar
  39. Park J, Matzner E (2003) Controls on the release of dissolved organic carbon and nitrogen from a deciduous forest floor investigated by manipulations of aboveground litter inputs and water flux. Biogeochemistry 66:265–286. CrossRefGoogle Scholar
  40. Perakis SS, Hedin LO (2001) Fluxes and fates of nitrogen in soil of an unpolluted old-growth temperate forest, southern Chile. Ecology 82(8):2245–2260.[2245:FAFONI]2.0.CO;2Google Scholar
  41. Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315. CrossRefGoogle Scholar
  42. Saxton KE, Rawls WJ (2006) Soil water characteristic estimates by texture and organic matter for hydrologic solutions. Soil Sci Soc Am J 70:1569–1578. CrossRefGoogle Scholar
  43. Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602. CrossRefGoogle Scholar
  44. Smolander A, Saarsalmi A, Tamminen P (2015) Response of soil nutrient content, organic matter characteristics and growth of pine and spruce seedlings to logging residues. For Ecol Manag 357:117–125. CrossRefGoogle Scholar
  45. Son Y, Jun YC, Lee YY, Kim RH, Yang SY (2004) Soil carbon dioxide evolution, litter decomposition, and nitrogen availability four years after thinning in a Japanese larch plantation. Commun Soil Sci Plant Anal 35:1111–1122. CrossRefGoogle Scholar
  46. Tan X, Chang SX, Comeau PG, Wang Y (2008) Thinning effects on microbial biomass, N mineralization, and tree growth in a mid-rotation fire-origin lodgepole pine stand in the lower foothills of Alberta, Canada. For Sci 54:465–474Google Scholar
  47. Thibodeau L, Raymond P, Camiré C, Munson AD (2000) Impact of precommercial thinning in balsam fir stands on soil nitrogen dynamics, microbial biomass, decomposition, and foliar nutrition. Can J For Res 30:229–238. CrossRefGoogle Scholar
  48. Van Der Heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11(3):296–310. CrossRefPubMedGoogle Scholar
  49. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707. CrossRefGoogle Scholar
  50. Wang W, Page-Dumroese D, Lv R, Xiao C, Li G, Liu Y (2016) Soil enzyme activities in Pinus tabuliformis (Carriére) plantations in northern China. Forests 7:112. CrossRefGoogle Scholar
  51. Wardle DA (1998) Controls of temporal variability of the soil microbial biomass: a global-scale synthesis. Soil Biol Biochem 30(13):1627–1637. CrossRefGoogle Scholar
  52. Weil RR, Islam KR, Stine MA, Gruver JB, Samson-Liebig SE (2003) Estimating active carbon for soil quality assessment: a simplified method for laboratory and field use. Am J Altern Agric 18:3–17. CrossRefGoogle Scholar
  53. Witt C, Gaunt JL, Galicia CC, Ottow JCG, Neue H-U (2000) A rapid chloroform-fumigation extraction method for measuring soil microbial biomass carbon and nitrogen in flooded rice soils. Biol Fertil Soils 30:510–519. CrossRefGoogle Scholar
  54. Yoon TK, Noh NJ, Chung H, Yang A-R, Son Y (2015) Soil nitrogen transformation and availability in upland pine and bottomland alter forests. Forests 6:2941–2958. CrossRefGoogle Scholar

Copyright information

© INRA and Springer-Verlag France SAS, part of Springer Nature 2018

Authors and Affiliations

  • Seongjun Kim
    • 1
  • Guanlin Li
    • 1
  • Seung Hyun Han
    • 1
  • Hyun-Jun Kim
    • 1
  • Choonsig Kim
    • 2
  • Sang-Tae Lee
    • 3
  • Yowhan Son
    • 1
  1. 1.Department of Environmental Science and Ecological Engineering, Graduate SchoolKorea UniversitySeoulSouth Korea
  2. 2.Department of Forest ResourcesGyeongnam National University of Science and TechnologyJinjuSouth Korea
  3. 3.Forest Practice Research CenterNational Institute of Forest SciencePocheonSouth Korea

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