Skip to main content

Advertisement

Log in

Altered soil microbial properties and functions after afforestation increase soil carbon and nitrogen but not phosphorus accumulation

  • ORIGINAL PAPER
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

Afforestation can substantially influence terrestrial carbon (C), nitrogen (N), and phosphors (P) stocks by changing soil microbial properties and functions, but the direction and magnitude of the effects of afforestation on soil microbial properties and functions at global scales remain unknown. Here, we conducted a meta-analysis of 1292 paired observations from 217 studies to explore the effects of afforestation on soil microbial communities and their linkages with the dynamics of soil C, N, and P stocks. Afforestation increased total plant biomass and litterfall by 314% and 643%, respectively, and increased soil organic C (SOC) and N stocks by 37% and 29%, respectively, but did not significantly affect soil P stock. Afforestation increased soil bacterial and fungal biomass by 36% and 49%, respectively, and fungi: bacteria ratio by 20%, suggesting that microbial groups shifted; i.e., the biomass of r- strategists decreased and the biomass of K- strategists increased. Moreover, afforestation increased the activities of β-glucosidase (59%), cellulase (136%), β-1,4-N-acetylglucosamnidase (123%), urease (59%) and acid phosphatase (66%), and increased microbial biomass C (MBC, 85%), N (MBN, 109%), and the MBC:SOC ratio (27%), but decreased the microbial metabolic quotient (13%). The beneficial effects of afforestation on soil microbial properties and functions differed depending on the initial land cover type, stand age, stand type, plantation species, and climate change. The increases in soil C and N stocks following afforestation were indirectly associated with the increases in fungal biomass, MBC, MBN, and directly related to the increases in the activities of cellulase and β-1,4-N-acetylglucosaminidase and the decreases in the microbial metabolic quotient besides the increased plant biomass and litterfall. Overall, these results suggest that the preservation of soil functions following afforestation should be considered for C and N sequestration to mitigate climate change.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data Availability

All data included in this study are available upon request by contact with the corresponding author.

References

  • Anderson TH, Domsch KH (1993) The metabolic quotient for CO2 (qCO2) as a specific activity parameter to assess the effects of environmental conditions, such as pH, on the microbial biomass of forest soils. Soil Biol Biochem 25:393–395

    Article  Google Scholar 

  • Bárcena TG, Kiaer LP, Vesterdal L, Stefansdottir HM, Gundersen P, Sigurdsson BD (2014) Soil carbon stock change following afforestation in Northern Europe : a meta-analysis. Glob Chang Biol 20:2393–2405

    Article  PubMed  Google Scholar 

  • Berber ASK, Farasat S, Namli A (2014) Afforestation effects on soil biochemical properties. Eur J for Sci 1:25–34

    Google Scholar 

  • Berthrong ST, Jobbaagy EG, Jackson RB (2009) A global meta analysis of soil exchangeable cations, pH, carbon, and nitrogen with afforestation. Ecol Appl 19:2228–2241

    Article  PubMed  Google Scholar 

  • Borenstein M, Hedges LV, Higgins JP, Rothstein HR (2009) Introduction to meta-analysis. John Wiley & Sons, West Sussex, UK

    Book  Google Scholar 

  • Delgado-Baquerizo M, Maestre FT, Reich PB, Jeffries TC, Gaitan JJ, Encinar D, Berdugo M, Campbell CD, Singh BK (2016) Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun 7:10541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng Q, Cheng X, Hui D, Zhang Q, Li M, Zhang Q (2016) Soil microbial community and its interaction with soil carbon and nitrogen dynamics following afforestation in central China. Sci Total Environ 541:230–237

    Article  CAS  PubMed  Google Scholar 

  • Deng Q, McMahon DE, Xiang YZ, Yu CL, Jackson RB, Hui DF (2017) A global meta-analysis of soil phosphorus dynamics after afforestation. New Phytol 213:181–192

    Article  CAS  PubMed  Google Scholar 

  • Doelman JC, Stehfest E, van Vuuren DP, Tabeau A, Hof AF, Braakhekke MC, Gernaat DEHJ, van den Berg M, van Zeist WJ, Dailoglou V, van Meijl H, Luca PL (2020) Afforestation for climate change mitigation: Potentials, risks and trade-offs. Glob Chang Biol 26:1576–1591

    Article  PubMed  Google Scholar 

  • FAO (2020) Global Forest Resources Assessment 2020 - Key findings. FAO, Rome

    Google Scholar 

  • Fierer N, Strickland MS, Liptzin D, Bardford MA, Cleveland CC (2009) Global patterns in belowground communities. Ecol Lett 12:1238–1249

    Article  PubMed  Google Scholar 

  • Ghorbani M, Sohrabi H, Sadati SE, Babaei F (2018) Productivity and dynamics of pure and mixed –species plantation of Populous deltoids Bartr. Ex marsh and Alnus subcordata C.A. Mey. For Ecol Manag 409:890–898

    Article  Google Scholar 

  • Gunina A, Smith AR, Godbold DL, Jones DL, Kuzyakov Y (2017) Response of soil microbial community to afforestation with pure and mixed species. Plant Soil 412:357–368

    Article  CAS  Google Scholar 

  • Hartmann M, Widmer F (2006) Community structure analyses are more sensitive to differences in soil bacterial communities than anonymous diversity indices. Appl Environ Microb 72:7804–7812

    Article  CAS  Google Scholar 

  • Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Clim 25:1965–1978

    Article  Google Scholar 

  • Holden SR, Treseder K (2013) A meta-analysis of soil microbial biomass responses to forest disturbances. Front Microbiol 4:163

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang XZ, Cui C, Hou EQ, Li FB, Liu WJ, Jiang LF, Luo YQ, Xu XN (2022) Acidification of soil due to forestation at the global scale. For Ecol Manag 505:119951

    Article  Google Scholar 

  • Insam H, Haselwandter K (1989) Metabolic quotient of the soil microflora in relation to plant succession. Oecologia 79:174–178

    Article  CAS  PubMed  Google Scholar 

  • Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept & review. Soil Biol Biochem 83:184–199

    Article  CAS  Google Scholar 

  • Laganière J, Angers DA, Paré D (2010) Carbon accumulation in agricultural soils after afforestation: a meta-analysis. Glob Chang Biol 16:439–453

    Article  Google Scholar 

  • Li DJ, Niu SL, Luo YQ (2012) Global patterns of the dynamics of soil carbon and nitrogen stocks following afforestation : a meta-analysis. New Phytol 195:172–181

    Article  CAS  PubMed  Google Scholar 

  • Li QX, Feng J, Wu JJ, Jia W, Zhang Q, Chen Q, Zhang DD, Cheng XL (2019) Spatial variation in soil microbial community structure and its relation to plant distribution and local environments following afforestation in central China. Soil till Res 193:8–16

    Article  Google Scholar 

  • Liu D, Wang BR, Bhople P, Davlatbekov F, Yu FQ (2020) Land rehabilitation improves edaphic conditions and increases soil microbial biomass and abundance. Soil Ecol Lett 2:145–156

    Article  CAS  Google Scholar 

  • Lorenz M, Thiele-Bruhn S (2019) Tree species affect soil organic matter stocks and stoichiometry in interaction with soil microbiota. Geoderma 353:35–46

    Article  CAS  Google Scholar 

  • Luo XZ, Hou EQ, Zhang LL, Zang XW, Yi YF, Zhang GH, Wen DZ (2019) Effects of forest conversion on carbon-degrading enzyme activities in subtropical China. Sci Total Environ 696:133968

    Article  CAS  PubMed  Google Scholar 

  • Luo XZ, Hou EQ, Chen JQ, Li J, Zhang LL, Zang XW, Wen DZ (2020) Dynamics of carbon, nitrogen, and phosphorus stocks and stoichiometry resulting from conversion of primary broadleaf forest to plantation and secondary forest in subtropical China. CATENA 193:104606

    Article  CAS  Google Scholar 

  • Luo XZ, Wen DZ, Hou EQ, Zhang LL, Li Y, He XJ (2022) Changes in the composition of soil microbial communities and their carbon-cycle genes following the conversion of primary broadleaf forests to plantations and secondary forests. Land Degrad Dev 33:974–985

    Article  Google Scholar 

  • Macdonald CA, Thomas N, Robinson L, Tate KR, Ross DJ, Dando J, Singh BK (2009) Physiological, biochemical and molecular responses of the soil microbial community after afforestation of pastures with Pinus radiate. Soil Biol Biochem 41:1642–1651

    Article  CAS  Google Scholar 

  • Mueller KE, Hobbie SE, Oleksyn J, Reich PB, Eissenstat DM (2012) Do evergreen and deciduous trees have different effects on net N mineralization soil ? Ecology 93:1463–1472

    Article  PubMed  Google Scholar 

  • Mukhopadhyay S, Maiti SK (2014) Soil CO2 flux in grassland, afforested land and reclaimed coalmine overburden dumps: a case study. Land Degrad Dev 25:216–227

    Article  Google Scholar 

  • Nannipieri P, Trasar-Cepeda C, Dick RP (2018) Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol Fert Soils 54:11–19

    Article  CAS  Google Scholar 

  • Odum EP (1969) The strategy of ecosystem development. Science 164:262–270

    Article  CAS  PubMed  Google Scholar 

  • Pabst H, Gerschlauer F, Kiese R, Kuzyakov Y (2016) Land use and precipitation affect organic and microbial carbon stocks and the specific metabolic quotient in soils of eleven ecosystems of Mt. Kilimanjaro, Tanzania. Land Degrad Dev 27:592–602

    Article  Google Scholar 

  • Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon–nutrient couplings in temperate forests. New Phytol 199:41–51

    Article  CAS  PubMed  Google Scholar 

  • Ren CJ, Kang D, Wu JP, Zhao FZ, Yang GH, Han XH, Feng YZ, Ren GX (2016) Temporal variation in soil enzyme activities after afforestation in the Loess Plateau, China. Geoderma 282:103–111

    Article  CAS  Google Scholar 

  • Scheibe A, Steffens C, Seven J, Jacob A, Hertel D, Leuschner C, Gleixner G (2015) Effects of tree identity dominate over tree diversity on the soil microbial community structure. Soil Biol Biochem 81:219–227

    Article  CAS  Google Scholar 

  • Shahbaze M, Kuzyakov Y, Sanaullah M, Heitkamp F, Zelenev V, Kumar A, Blagodatskay E (2017) Microbial decomposition of soil organic matter is mediated by quality and quantity of crop residues: Mechanisms and thresholds. Biol Fert Soils 53:287–301

    Article  Google Scholar 

  • Shen CC, Xiong JB, Zhang HY, Feng YZ, Lin XG, Li XY, Liang WJ, Chu HY (2013) Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol Biochem 57:204–211

    Article  CAS  Google Scholar 

  • Shi SW, Peng CH, Wang M, Zhu QA, Yang G, Yang YZ, Xi TT, Zhang TL (2016) A global meta-analysis of changes in soil carbon, nitrogen, phosphorus and sulfur, and stoichiometric shifts after forestation. Plant Soil 407:323–340

    Article  CAS  Google Scholar 

  • Sinsabaugh RL, Follstad Shah JJ (2012) Ecoenzymatic stoichiometry and ecological theory. Annu Rev Ecol Evol S 43:313–343

    Article  Google Scholar 

  • Spohn M, Chodak M (2015) Microbial respiration per unit biomass increases with carbon-to-nutrient ratios in forest soils. Soil Biol Biochem 81:128–133

    Article  CAS  Google Scholar 

  • Viechtbauer W (2010) Conducting meta-analysis in R with the metafor package. J Stat Softw 36:1–48

    Article  Google Scholar 

  • Wang B, Xue S, Liu GB, Zhang GH, Li G, Ren ZP (2012) Changes in soil nutrient and enzyme activities under different vegetations in the Loess Plateau area, Northwest China. CATENA 92:186–195

    Article  CAS  Google Scholar 

  • Wang Y, Chen L, Xiang WH, Ouyang S, Zhang TD, Zhang XL, Zeng YL, Hu YT, Luo GW, Kuzyakov Y (2021) Forest conversion to plantations: A meta-analysis of consequences for soil and microbial properties and functions. Glob Chang Biol 27:5643–5656

    Article  CAS  PubMed  Google Scholar 

  • Wu JJ, Zhang FY, Lei Y, Zhang QF, Cheng XL (2016) Afforestation impacts microbial biomass and its natural 13C and 15N abundance in soil aggregates in central China. Sci Total Environ 568:52–56

    Article  CAS  PubMed  Google Scholar 

  • Xiang YZ, Liu Y, Yue XJ, Yao B, Zhang LY, He J, Luo Y, Xu XY, Zong JZ (2021) Factors controlling soil organic carbon and total nitrogen stocks following afforestation with Robinia pseudoacaica on cropland across China. For Ecol Manag 494:11927

    Article  Google Scholar 

  • Xu XF, Schimel JP, Thornton PF, Song X, Yuan FM, Goswami S (2014) Substrate and environmental controls on microbial assimilation of soil organic carbon: a framework for Earth system models. Ecol Lett 17:547–555

    Article  PubMed  Google Scholar 

  • Zechmeister-Boltenstern S, Keiblinger KM, Mooshammer M, Panuelas J, Richter A, Sardans J, Wanek W (2015) The application of ecological stoichiometry to plant-microbial-soil organic matter transformations. Ecol Monog 85:133–155

    Article  Google Scholar 

  • Zhao FZ, Ren CJ, Han XH, Yang GH, Wang J, Doughty R, Wang ZT (2019) Trends in soil microbial communities in afforestation ecosystem modulated by aggradation phase. Forest Ecol Manag 441:167–175

    Article  Google Scholar 

  • Zhou ZH, Wang CK, Luo YQ (2018) Effects of forest degradation on microbial communities and soil carbon cycling: A global meta-analysis. Global Ecol Biogeogr 27:110–124

    Article  Google Scholar 

  • Zhou S, Wang JY, Chen L, Wang J, Zhao FZ (2020) Microbial community structure and functional genes drive soil priming effect following afforestation. SciTotal Environ 825:153925

    Google Scholar 

Download references

Funding

This work was funded by the National Natural Science Foundation of China (31570401; 41973076; 32201406) and the Guangdong Basic and Applied Basic Research Foundation (2021A1515110837; 2023A1515010911), and South China Botanical Garden, Chinese Academy of Sciences (Granted No: QNXM-08).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dazhi Wen.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 26022 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Luo, X., Hou, E., Zhang, L. et al. Altered soil microbial properties and functions after afforestation increase soil carbon and nitrogen but not phosphorus accumulation. Biol Fertil Soils 59, 645–658 (2023). https://doi.org/10.1007/s00374-023-01726-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-023-01726-4

Keywords

Navigation