Plant and Soil

, Volume 414, Issue 1–2, pp 81–93 | Cite as

Asymmetric effects of litter removal and litter addition on the structure and function of soil microbial communities in a managed pine forest

  • Qiong Zhao
  • Aimée T. Classen
  • Wei-Wei Wang
  • Xin-Ran Zhao
  • Bing Mao
  • De-Hui Zeng
Regular Article

Abstract

Aims

Variation in tree litter inputs and understory vegetation caused by human disturbances and climate change in forest plantations can extend to alter forest stability and productivity over time. Here, we explore how tree litter inputs interact with understory plant management to influence belowground processes in a managed forest plantation.

Methods

We conducted a two-factor nested experimental manipulation of pine litter and understory vegetation in a nutrient-poor Pinus sylvestris var. mongolica plantation. Three levels of tree litter manipulation (ambient litter, litter removal and litter addition) were nested in two levels of understory manipulation (understory intact and understory removal). After two years of manipulation, mineral soils were analyzed for total and extractable C, N and P concentrations, N mineralization, enzyme activities, as well as the microbial community structure (as indicated by phospholipid fatty acids).

Results

Litter removal had little impact on C and nutrient cycling as well as microbial biomass and community structure in this low nutrient pine plantation; however, litter addition and the removal of the understory vegetation had large impacts on these processes. Litter addition elevated soil microbial biomass, acid phosphatase and β-1, 4-glucosidase activities, by a much greater degree when the understory vegetation was intact than when the understory was removed. Litter addition also reduced soil available P by 39% when the understory vegetation was intact, and reduced soil available P by 74% and NO3 –N by 45% when the understory was removed. Litter addition significantly reduced the ratio of Gram-positive to Gram-negative bacteria as well as the ratio between PLFA markers cy17:0 and 16:1ω7. Understory removal reduced the ratio of PLFA markers cy17:0 to 16:1ω7.

Conclusions

Our study results show that, in this managed pine plantation, soil microbial community structure and function were more sensitive to an increase rather than to a decrease in pine litter inputs. Further, we found that the presence of understory vegetation can increase soil microbial biomass and alleviate the reduction in available N and P concentrations induced by pine litter addition. Thus, preservation of the understory vegetation is an effective way to maintain the functional stability of managed forests on nutrient-poor soils.

Keywords

Pinus sylvestris var. mongolica Litter Understory vegetation Soil microbial community Nutrient availability 

Notes

Acknowledgements

We thank Guiyan Ai and Zhencheng Su for their help in lab analyses, and thank Yunzhi Yan for his help in statistical analyses. We are grateful to Gregory S. Newman and two referees for their valuable comments and suggestions. This work was supported by the National Natural Science Foundation of China (Nos. 41373087 and 31270668) and the State Key Laboratory of Forest and Soil Ecology of China (LFSE2013-11).

Data availability statement

The datasets generated and/or analyzed during the current study are available from corresponding author on reasonable request.

Supplementary material

11104_2016_3115_MOESM1_ESM.docx (18 kb)
Supplementary material 1 (DOCX 18 kb)

References

  1. Attiwill PM, Adams MA (1993) Tansley review no. 50. Nutrient cycling in forests. New Phyto 124:561–582CrossRefGoogle Scholar
  2. Bland JM, Altman DG (1995) Multiple significance tests: the Bonferroni method. BMJ-Brit Med J 310:170CrossRefGoogle Scholar
  3. Blazier MA, Hennessey TC, Deng SP (2005) Effects of fertilization and vegetation control on microbial biomass carbon and dehydrogenase activity in a juvenile loblolly pine plantation. For Sci 51:449–459Google Scholar
  4. Bossio DA, Scow KM, Gunapala N, Graham KJ (1998) Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microb Ecol 36:1–12CrossRefPubMedGoogle Scholar
  5. Brant JB, Myrold DD, Sulzman EW (2006) Root controls on soil microbial community structure in forest soils. Oecologia 148:650–659CrossRefPubMedGoogle Scholar
  6. Busse MD, Cochran PH, Barrett JW (1996) Changes in ponderosa pine site productivity following removal of understory vegetation. Soil Sci Soc Am J 60:1614–1621CrossRefGoogle Scholar
  7. Busse MD, Beattie SE, Powers RF, Sanchez FG, Tiarks AE (2006) Microbial community responses in forest mineral soil to compaction, organic matter removal, and vegetation control. Can J For Res 36:577–588CrossRefGoogle Scholar
  8. Chapin FS III (1983) Nitrogen and phosphorus nutrition and nutrient cycling by evergreen and deciduous understory shrubs in an Alaskan black spruce forest. Can J For Res 13:773–781CrossRefGoogle Scholar
  9. Chevasco ED, Minogue PJ, Mackowiak C, Comerford NB (2016) Fertilization and pine straw raking in slash pine plantations: P removals and effects on total and mobile soil, foliage and litter P pools. For Ecol Manag 376:310–320CrossRefGoogle Scholar
  10. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143CrossRefGoogle Scholar
  11. Elliott KJ, Vose JM, Knoepp JD, Clinton BD, Kloeppel BD (2015) Functional role of the herbaceous layer in eastern deciduous forest ecosystems. Ecosystems 18:221–236CrossRefGoogle Scholar
  12. FAO (2010) Global Forest resources assessment 2010. Main report. FAO forestry paper 163. FAO, Rome, p. 378Google Scholar
  13. Feng HM, He HB, Bai Z, Wu YY, Guo BD, Zhang M, Zhang XD (2008) Microbial degradation of acetochlor in mollisol and the effects of acetochlor on the characteristics of soil phospholipid fatty acids. Chinese J App Ecol 19:1585–1590 (in Chinese)Google Scholar
  14. Feng W, Schaefer DA, Zou X, Zhang M (2011) Shifting sources of soil labile organic carbon after termination of plant carbon inputs in a subtropical moist forest of Southwest China. Ecol Res 26:437–444CrossRefGoogle Scholar
  15. Fisk MC, Fahey TJ (2001) Microbial biomass and nitrogen cycling responses to fertilization and litter removal in young northern hardwood forests. Biogeochemistry 53:201–223CrossRefGoogle Scholar
  16. Fox TR (2000) Sustained productivity in intensively managed forest plantations. For Ecol Manag 138:187–202CrossRefGoogle Scholar
  17. Frostegård A, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Ferti Soils 22:59–65CrossRefGoogle Scholar
  18. Gartner TB, Cardon ZG (2004) Decomposition dynamics in mixed-species leaf litter. Oikos 104:230–246CrossRefGoogle Scholar
  19. Gilliam FS (2007) The ecological significance of the herbaceous layer in forest ecosystems. Bioscience 57:845–858CrossRefGoogle Scholar
  20. Gurlevik N, Kelting DL, Allen HL (2004) Nitrogen mineralization following vegetation control and fertilization in a 14-year-old loblolly pine plantation. Soil Sci Soc Am J 68:272–281CrossRefGoogle Scholar
  21. Hofmeister J, Oulehle F, Krám P, Hruška J (2008) Loss of nutrients due to litter raking compared to the effect of acidic deposition in two spruce stands, Czech Republic. Biogeochemistry 88:139–151CrossRefGoogle Scholar
  22. Holub SM, Lajtha K, Spears JDH, Tóth JA, Crow SE, Caldwell BA, Papp M, Nagy PT (2005) Organic matter manipulations have little effect on gross and net nitrogen transformations in two temperate forest mineral soils in the USA and Central Europe. For Ecol Manag 214:320–330CrossRefGoogle Scholar
  23. Huang W, Spohn M (2015) Effects of long-term litter manipulation on soil carbon, nitrogen, and phosphorus in a temperate deciduous forest. Soil Biol Biochem 83:12–18CrossRefGoogle Scholar
  24. Kotroczó Z, Veres Z, Fekete I, Krakomperger Z, Tóth JA, Lajtha K, Tóthmérész B (2014) Soil enzyme activity in response to long-term organic matter manipulation. Soil Biol Biochem 70:237–243CrossRefGoogle Scholar
  25. Leff JW, Wieder WR, Taylor PG, Townsend AR, Nemergut DR, Grandy AS, Cleveland CC (2012) Experimental litterfall manipulation drives large and rapid changes in soil carbon cycling in a wet tropical forest. Glob Chang Biol 18:2969–2979CrossRefPubMedGoogle Scholar
  26. Lin GG, Mao R, Zhao L, Zeng DH (2013) Litter decomposition of a pine plantation is affected by species evenness and soil nitrogen availability. Plant Soil 373:649–657CrossRefGoogle Scholar
  27. Liu LL, Greaver TL (2010) A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecol Lett 13:819–828CrossRefPubMedGoogle Scholar
  28. Lu RK (1999) Analytical methods of soil and agricultural chemistry. China Agricultural Science and Technology Publishing House, Beijing (in Chinese)Google Scholar
  29. Matsushima M, Chang SX (2007) Effects of understory removal, N fertilization, and litter layer removal on soil N cycling in a 13-year-old white spruce plantation infested with Canada bluejoint grass. Plant Soil 292:243–258CrossRefGoogle Scholar
  30. McFarlane KJ, Schoenholtz SH, Powers RF (2009) Plantation management intensity affects belowground carbon and nitrogen storage in northern California. Soil Sci Soc Am J73:1020–1032CrossRefGoogle Scholar
  31. Mitchell RJ, Keith AM, Potts JM, Ross J, Reid E, Dawson LA (2012) Overstory and understory vegetation interact to alter soil community composition and activity. Plant Soil 352:65–84CrossRefGoogle Scholar
  32. Moore-Kucera J, Dick RP (2008) PLFA profiling of microbial community structure and seasonal shifts in soils of a Douglas-fir chronosequence. Microb Ecol 55:500–511CrossRefPubMedGoogle Scholar
  33. Muller RN (2003) Nutrient relations of the herbaceous layer in deciduous forest ecosystem. In: Gilliam FS, Roberts MR (eds) The herbaceous layer in forests of eastern North America. Oxford University Press, New York, pp. 15–37Google Scholar
  34. Nelson DW, Sommers LE (1996) Total carbon, organic carbon and organic matter. In: Sparks DL, Page AL, Helmke PA, Leoppert RH, Soltanpour PN, Tabatabai MA, Johnston CT, Sumner ME (eds) Methods of soil analysis. Part 3: chemical methods. Soil Science Society of America, Wisconsin, pp. 961–1010Google Scholar
  35. Nilsson MC, Wardle DA (2005) Understory vegetation as a forest ecosystem driver: evidence from the northern Swedish boreal forest. Fron Ecol Environ 3:421–428CrossRefGoogle Scholar
  36. Norby RJ, Hanson PJ, O’Neill EG, Tschaplinski TJ, Weltzin JF, Hansen RA, Cheng W, Wullschleger SD, Gunderson CA, Edwards NT, Johnson DW (2002) Net primary productivity of a CO2-enriched deciduous forest and the implications for carbon storage. Ecol Appl 12:1261–1266Google Scholar
  37. Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium biocarbonate. US Department of Agriculture, p19 (Circular No. 939)Google Scholar
  38. Park JH, 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 66:265–286CrossRefGoogle Scholar
  39. Powers RF, Busse MD, McFarlane KJ, Zhang J, Young DH (2013) Long-term effects of silviculture on soil carbon storage: does vegetation control make a difference? Forestry 86:47–58CrossRefGoogle Scholar
  40. Prevost-Boure NC, Maron PA, Ranjard L, Nowak V, Dufrene E, Damesin C, Soudani K, Lata JC (2011) Seasonal dynamics of the bacterial community in forest soils under different quantities of leaf litter. Appl Soil Ecol 47:14–23CrossRefGoogle Scholar
  41. Qiao Y, Miao S, Silva LCR, Horwath WR (2014) Understory species regulate litter decomposition and accumulation of C and N in forest soils: a long-term dual-isotope experiment. For Ecol Manag 329:318–327CrossRefGoogle Scholar
  42. Rifai SW, Markewitz D, Borders B (2010) Twenty years of intensive fertilization and competing vegetation suppression in loblolly pine plantations: impacts on soil C, N, and microbial biomass. Soil Biol Biochem 42:713–723CrossRefGoogle Scholar
  43. Sayer EJ, Heard MS, Grant HK, Marthews TR, Tanner EVJ (2011) Soil carbon release enhanced by increased tropical forest litterfall. Nat Clim Chang 1:304–307CrossRefGoogle Scholar
  44. Sayer EJ, Wright SJ, Tanner EVJ, Yavitt JB, Harms KE, Powers JS, Kaspari M, Garcia MN, Turner BL (2012) Variable responses of lowland tropical forest nutrient status to fertilization and litter manipulation. Ecosystems 15:387–400CrossRefGoogle Scholar
  45. Sayer EJ (2006) Using experimental manipulation to assess the roles of leaf litter in the functioning of forest ecosystems. Biol Rev 81:1–31CrossRefPubMedGoogle Scholar
  46. Six J, Conant RT, Paul EA, Paustian K (2002) Stabilization mechanisms of soil organic matter: implications for C-saturation of soils. Plant Soil 241:155–176CrossRefGoogle Scholar
  47. Slesak RA, Schoenholtz SH, Harrington TB (2011) Soil carbon and nutrient pools in Douglas-fir plantations 5 years after manipulating biomass and competing vegetation in the Pacific northwest. For Ecol Manag 262:1722–1728CrossRefGoogle Scholar
  48. Sohi SP, Mahieu N, Arah JRM, Powlson DS, Madari B, Gaunt JL (2001) A procedure for isolating soil organic matter fractions suitable for modeling. Soil Sci Soc Am J 65:1121–1128CrossRefGoogle Scholar
  49. Streit K, Hagedorn F, Hiltbrunner D, Portmann M, Saurer M, Buchmann N, Wild B, Richter A, Wipf S, Siegwolf RTW (2014) Soil warming alters microbial substrate use in alpine soils. Glob Chang Biol 20:1327–1338CrossRefPubMedGoogle Scholar
  50. Sun XL, Zhao J, You YM, Sun OJ (2016) Soil microbial responses to forest floor litter manipulation and nitrogen addition in a mixed-wood forest of northern China. Sci Rep 6:19536CrossRefPubMedPubMedCentralGoogle Scholar
  51. Swallow M, Quideau SA, MacKenzie MD, Kishchuk BE (2009) Microbial community structure and function: the effect of silvicultural burning and topographic variability in northern Alberta. Soil Biol Biochem 41:770–777CrossRefGoogle Scholar
  52. Tabatabai MA (1994) Soil enzymes. In: Weaver RW, Angle JS, Bottobley PS (eds) Methods of soil analysis. Part 2: microbiological and biochemical methods, SSSA Book Series No, vol 5. Soil Science Society of America, Madison, WI, pp. 775–883Google Scholar
  53. Waldrop MP, Firestone MK (2004) Microbial community utilization of recalcitrant and simple carbon compounds: impact of oak-woodland plant communities. Oecologia 138:275–284CrossRefPubMedGoogle Scholar
  54. Wagner RG, Little KM, Richardson B, McNabb K (2006) The role of vegetation management for enhancing productivity of the world’s forests. Forestry 79:57–79CrossRefGoogle Scholar
  55. Wang Q, He T, Wang S, Liu L (2013) Carbon input manipulation affects soil respiration and microbial community composition in a subtropical coniferous forest. Agric For Meteorol 178-179:152–160CrossRefGoogle Scholar
  56. Wu J, Liu Z, Wang X, Sun Y, Zhou L, Lin Y, Fu S (2011) Effects of understory removal and tree girdling on soil microbial community composition and litter decomposition in two eucalyptus plantations in South China. Funct Ecol 25:921–931CrossRefGoogle Scholar
  57. Wu J, Liu Z, Huang G, Chen D, Zhang W, Shao Y, Wan S, Fu S (2014) Response of soil respiration and ecosystem carbon budget to vegetation removal in eucalyptus plantations with contrasting ages. Sci Rep 4:6262CrossRefPubMedPubMedCentralGoogle Scholar
  58. Xu S, Liu LL, Sayer EJ (2013) Variability of above-ground litter inputs alters soil physicochemical and biological processes: a meta-analysis of litterfall-manipulation experiments. Biogeosciences 10:7423–7433CrossRefGoogle Scholar
  59. Zelles L (1997) Phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere 35:275–294CrossRefPubMedGoogle Scholar
  60. Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol Fertil Soils 29:111–129CrossRefGoogle Scholar
  61. Zhao L, Hu YL, Lin GG, Gao YC, Fang YT, Zeng DH (2013) Mixing effects of understory plant litter on decomposition and nutrient release of tree litter in two plantations in Northeast China. PLoS One 8(10):e76334CrossRefPubMedPubMedCentralGoogle Scholar
  62. Zhao Q, Zeng DH, Fan ZP, Yu ZY, Hu YL, Zhang JW (2009) Seasonal variations in phosphorus fractions in semiarid sandy soils under different vegetation types. For Ecol Manag 258:1376–1382CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Qiong Zhao
    • 1
    • 2
    • 3
  • Aimée T. Classen
    • 2
  • Wei-Wei Wang
    • 1
    • 4
  • Xin-Ran Zhao
    • 1
    • 4
  • Bing Mao
    • 1
  • De-Hui Zeng
    • 1
    • 3
    • 5
  1. 1.Key Laboratory of Forest Ecology and ManagementInstitute of Applied Ecology, Chinese Academy of SciencesShenyangPeople’s Republic of China
  2. 2.Center for Macroecology, Evolution and Climate, The Museum of Natural HistoryUniversity of CopenhagenCopenhagenDenmark
  3. 3.Daqinggou Ecological StationInstitute of Applied Ecology, Chinese Academy of SciencesShenyangPeople’s Republic of China
  4. 4.University of Chinese Academy of SciencesBeijingPeople’s Republic of China
  5. 5.Institute of Applied Ecology, Chinese Academy of SciencesShenyangPeople’s Republic of China

Personalised recommendations