Skip to main content

Advertisement

Log in

Changes of soil chemical properties, microbial biomass and enzymatic activities along a gradient of forest degradation in logged over tropical rain forests, Borneo

  • Research Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Purpose

The purpose of our study was to investigate soil chemical properties, soil microbial biomass and soil enzyme activities in a gradient of forest degradation in logged over tropical rain forests, Borneo. We hypothesized that the changes of above-ground vegetation could affect soil organic matter, which further influenced soil microbial biomass and enzyme activities.

Methods

A total of 35 forest plots with varying magnitude of logging influences were investigated for vegetation composition and soil parameters. The 35 plots were sorted based on tree genus compositions by a Principal Co-ordinates analysis (PCoA) and PCoA axis-1 values represented a gradient of forest degradation. Soil physicochemical properties, microbial biomass carbon and nitrogen, and four extracellular enzymes were measured.

Results

Linear regression analyses showed that soil organic carbon and total nitrogen concentrations decreased with decreasing PCoA axis-1 values (i.e., increasing magnitude of degradation), while soil pH values increased. Soil microbial biomass carbon and nitrogen, and the activities of four extracellular enzymes all decreased with decreasing PCoA axis-1 values. The activities of four enzymes were correlated with soil microbial biomass. Structural equation modeling showed that soil organic carbon explained the greatest variation of soil microbial biomass.

Conclusion

Above-ground forest degradation directly affects soil organic matter, which then affects soil microbial biomass. The combined actions of reduced microbial biomass and reduced soil organic matter as the substrate for the enzymes decrease microbial enzyme activities during the process of forest degradation. These changes may in turn feed back to the regrowth or succession of degraded forest ecosystems.

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

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are not publicly available due the datasets are still used in unpublished studies, but are available from the corresponding author on reasonable request.

References

  • Adamczyk B (2021) How do boreal forest soils store carbon? BioEssays 43:2100010

    Article  CAS  Google Scholar 

  • Adamczyk B, 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

    Article  CAS  Google Scholar 

  • Akinyemi DS, Zhu Y, Zhao M, Zhang P, Shen H, Fang J (2020) Response of soil extracellular enzyme activity to experimental precipitation in a shrub-encroached grassland in Inner Mongolia. Glob Ecol Conserv 23:e01175

    Article  Google Scholar 

  • Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944

    Article  CAS  Google Scholar 

  • Aoyagi R, Kitayama K (2016) Nutrient allocation among plant organs across 13 tree species in three Bornean rain forests with contrasting nutrient availabilities. J Plant Res 129:675–684

    Article  CAS  PubMed  Google Scholar 

  • Aoyagi R, Imai N, Fujiki S, Sugau JB, Pereira JT, Kitayama K (2017) The mixing ratio of tree functional groups as a new index for biodiversity monitoring in Bornean production forests. For Ecol Manag 403:27–43

    Article  Google Scholar 

  • Ashton PS, Hall P (1992) Comparisons of structure among mixed dipterocarp forests of North-Western Borneo. J Ecol 80:459

    Article  Google Scholar 

  • Asner GP, Hughes RF, Varga TA, Knapp DE, Kennedy-Bowdoin T (2009) Environmental and biotic controls over aboveground biomass throughout a tropical rain Forest. Ecosystems 12:261–278

    Article  Google Scholar 

  • Bai X, Dippold MA, An S, Wang B, Zhang H, Loeppmann S (2021) Extracellular enzyme activity and stoichiometry: the effect of soil microbial element limitation during leaf litter decomposition. Ecol Indic 121:107200

    Article  CAS  Google Scholar 

  • Bayranvand M, Akbarinia M, Salehi JG, Gharechahi J, Baldrian P (2021) Distribution of soil extracellular enzymatic, microbial, and biological functions in the C and N-cycle pathways along a Forest altitudinal gradient. Front Microbiol 12:660603

    Article  PubMed  PubMed Central  Google Scholar 

  • Bell CW, Fricks BE, Rocca JD, Steinweg JM, McMahon SK, Wallenstein MD (2013) High-throughput Fluorometric measurement of potential soil extracellular enzyme activities. J Vis Exp 50961

  • Blanc L, Echard M, Herault B, Bonal D, Marcon E, Chave J, Baraloto C (2009) Dynamics of aboveground carbon stocks in a selectively logged tropical Forest. Ecol Appl 19:1397–1404

    Article  PubMed  Google Scholar 

  • Carter MR, Gregorich EG (2008) Soil sampling and methods of analysis, 2nd edn. CRC press, Boca Raton

    Google Scholar 

  • Chave J, Réjou-Méchain M, Búrquez A, Chidumayo E, Colgan MS, Delitti WBC, Duque A, Eid T, Fearnside PM, Goodman RC, Henry M, Martínez-Yrízar A, Mugasha WA, Muller-Landau HC, Mencuccini M, Nelson BW, Ngomanda A, Nogueira EM, Ortiz-Malavassi E et al (2014) Improved allometric models to estimate the aboveground biomass of tropical trees. Glob Change Biol 20:3177–3190

    Article  Google Scholar 

  • de Andrade RB, Balch JK, Parsons AL, Armenteras D, Roman-Cuesta RM, Bulkan J (2017) Scenarios in tropical forest degradation: carbon stock trajectories for REDD+. Carbon Bal Manag 12:6

    Article  Google Scholar 

  • Dick WA (2011) Development of a soil enzyme reaction assay. Methods of soil enzymology. Madison, Wisconsin, USA: Soil Sci Soc Am 9:71–84

    CAS  Google Scholar 

  • Don A, Schumacher J, Freibauer A (2011) Impact of tropical land-use change on soil organic carbon stocks - a meta-analysis: SOIL ORGANIC CARBON AND LAND-USE CHANGE. Glob Chang Biol 17:1658–1670

    Article  Google Scholar 

  • Giweta M (2020) Role of litter production and its decomposition, and factors affecting the processes in a tropical forest ecosystem: a review. J Ecol Environ 44:11

    Article  Google Scholar 

  • Hasegawa M, Ito MT, Yoshida T, Seino T, Chung AYC, Kitayama K (2014) The effects of reduced-impact logging practices on soil animal communities in the Deramakot Forest Reserve in Borneo. Appl Soil Ecol 83:13–21

    Article  Google Scholar 

  • Houghton RA (2012) Carbon emissions and the drivers of deforestation and forest degradation in the tropics. Curr Opin Environ Sustain 4:597–603

    Article  Google Scholar 

  • Huth A, Ditzer T (2001) Long-term impacts of logging in a tropical rain forest—a simulation study. For Ecol Manag 19

  • Imai N, Samejima H, Langner A, Ong RC, Kita S, Titin J, Chung AYC, Lagan P, Lee YF, Kitayama K (2009) Co-benefits of sustainable Forest Management in Biodiversity Conservation and Carbon Sequestration. PLoS One 4:e8267

    Article  PubMed  PubMed Central  Google Scholar 

  • Imai N, Kitayama K, Titin J (2012a) Effects of logging on phosphorus pools in a tropical rainforest of Borneo. J Trop For Sci 13

  • Imai N, Seino T, Aiba S, Takyu M, Titin J, Kitayama K (2012b) Effects of selective logging on tree species diversity and composition of Bornean tropical rain forests at different spatial scales. Plant Ecol 213:1413–1424

    Article  Google Scholar 

  • Imai N, Tanaka A, Samejima H, Sugau JB, Pereira JT, Titin J, Kurniawan Y, Kitayama K (2014) Tree community composition as an indicator in biodiversity monitoring of REDD+. For Ecol Manag 313:169–179

    Article  Google Scholar 

  • Imai N, Sugau JB, Pereira JT, Titin J, Kitayama K (2019) Impacts of selective logging on spatial structure of tree species composition in Bornean tropical rain forests. J For Res 24:335–340

    Article  Google Scholar 

  • Jati AS, Samejima H, Fujiki S, Kurniawan Y, Aoyagi R, Kitayama K (2018) Effects of logging on wildlife communities in certified tropical rainforests in East Kalimantan, Indonesia. For Ecol Manag 427:124–134

    Article  Google Scholar 

  • Junaedi A, Hardiwinoto S, Supriyo H, Mindawati N (2020) Litter productivity and leaf litter nutrient return of three native tree species in drained tropical peatland, Riau-Indonesia. IOP Conf Ser: Earth Environ Sci 533:012007

    Article  Google Scholar 

  • Kieliszewska-Rokicka B (1999) Phosphate status and acid phosphatase activity in soil and ectomycorrhizas in two mature stands of scots pine (Pinus sylvestris L.) exposed to different levels of anthropogenic pollution. Acta Soc Bot Pol 68:311–317

    Article  CAS  Google Scholar 

  • Kissinger G, Herold M, De Sy V (2012) Drivers of deforestation and forest degradation. A synthesis report for REDD+ Policymakers 48(10.1016)

  • Kitayama K (2013) The activities of soil and root acid phosphatase in the nine tropical rain forests that differ in phosphorus availability on mount Kinabalu, Borneo. Plant Soil 367:215–224

    Article  CAS  Google Scholar 

  • Kitayama K, Fujiki S, Aoyagi R, Imai N, Sugau J, Titin J, Nilus R, Lagan P, Sawada Y, Ong R, Kugan F, Mannan S (2018) Biodiversity observation for land and ecosystem health (BOLEH): a robust method to evaluate the management impacts on the bundle of carbon and biodiversity ecosystem Services in Tropical Production Forests. Sustainability 10:4224

    Article  Google Scholar 

  • Knight TR, Dick RP (2004) Differentiating microbial and stabilized β-glucosidase activity relative to soil quality. Soil Biol Biochem 36:2089–2096

    Article  CAS  Google Scholar 

  • Langner A, Samejima H, Ong RC, Titin J, Kitayama K (2012) Integration of carbon conservation into sustainable forest management using high resolution satellite imagery: a case study in Sabah, Malaysian Borneo. Int J Appl Earth Obs Geoinf 18:305–312

    Google Scholar 

  • Liu M, Gan B, Li Q, Xiao W, Song X (2022) Effects of nitrogen and phosphorus addition on soil extracellular enzyme activity and stoichiometry in Chinese fir (Cunninghamia lanceolata) forests. Front Plant Sci 13:834184

    Article  PubMed  PubMed Central  Google Scholar 

  • Luo L, Meng H, Gu JD (2017) Microbial extracellular enzymes in biogeochemical cycling of ecosystems. J Environ Manag 197:539–549

    Article  CAS  Google Scholar 

  • Mertens B, Lambin EF (2000) Land-cover-change trajectories in southern Cameroon. Ann Assoc Am Geogr 90:467–494

    Article  Google Scholar 

  • Moorhead DL, Lashermes G, Sinsabaugh RL (2012) A theoretical model of C- and N-acquiring exoenzyme activities, which balances microbial demands during decomposition. Soil Biol Biochem 53:133–141

    Article  CAS  Google Scholar 

  • Moscatelli MC, Lagomarsino A, Garzillo AMV, Pignataro A, Grego S (2012) β-Glucosidase kinetic parameters as indicators of soil quality under conventional and organic cropping systems applying two analytical approaches. Ecol Indic 13:322–327

    Article  CAS  Google Scholar 

  • Ngaba MJY, Ma XQ, Hu YL (2020) Variability of soil carbon and nitrogen stocks after conversion of natural forest to plantations in eastern China. PeerJ 8:e8377

    Article  PubMed  PubMed Central  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2020) vegan: Community Ecology Package. R Package Version 2.5–7

  • Ong RC, Kleine M (1996) DIPSIM: dipterocarp forest growth simulation model–a tool for forest-level management planning. Dipterocarp forest ecosystem towards sustainable management, Singapore

  • Ong RC, Langner A, Imai N, Kitayama K (2013) Management history of the study sites: the Deramakot and Tangkulap Forest reserves. In: Kitayama K (ed) Co-benefits of sustainable forestry: ecological studies of a certified Bornean rain Forest, ecological research monographs. Springer Japan, Tokyo, pp 1–21

    Google Scholar 

  • Ouedraogo I, Savadogo P, Tigabu M, Cole R, Oden PC, Ouadba JM (2011) Trajectory analysis of Forest cover change in the tropical dry Forest of Burkina Faso, West Africa. Landsc Res 36:303–320

    Article  Google Scholar 

  • Pearson TRH, Brown S, Casarim FM (2014) Carbon emissions from tropical forest degradation caused by logging. Environ Res Lett 9:034017

    Article  CAS  Google Scholar 

  • Pfeifer M, Kor L, Nilus R, Turner E, Cusack J, Lysenko I, Khoo M, Chey VK, Chung AC, Ewers RM (2016) Mapping the structure of Borneo’s tropical forests across a degradation gradient. Remote Sens Environ 176:84–97

    Article  Google Scholar 

  • Sabah Forestry Department (2005) Forest management plant 2: Deramakot forest reserve, Forest management unit no.19. Sandakan

  • Samejima H, Ong R, Lagan P, Kitayama K (2012) Camera-trapping rates of mammals and birds in a Bornean tropical rainforest under sustainable forest management. For Ecol Manag 270:248–256

    Article  Google Scholar 

  • Saner P, Loh YY, Ong RC, Hector A (2012) Carbon stocks and fluxes in tropical lowland dipterocarp rainforests in Sabah, Malaysian Borneo. PLoS ONE 7:e29642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seino T, Takyu M, Aiba S, Kitayama K, Ong RC (2006) Floristic composition, stand structure, and above-ground biomass of the tropical rain forests of Deramakot and Tangkulap Forest Reserve in Malaysia under different forest managements. In Synergy between carbon management and biodiversity conservation in tropical rain forests. Proceedings of the 2nd workshop, Sandakan, Malaysia. Vol. 30

  • Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404

    Article  CAS  Google Scholar 

  • Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD et al (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264

    Article  PubMed  Google Scholar 

  • Sistla SA, Schimel JP (2013) Seasonal patterns of microbial extracellular enzyme activities in an arctic tundra soil: identifying direct and indirect effects of long-term summer warming. Soil Biol Biochem 66:119–129

    Article  CAS  Google Scholar 

  • Stone MM, DeForest JL, Plante AF (2014) Changes in extracellular enzyme activity and microbial community structure with soil depth at the Luquillo critical zone observatory. Soil Biol Biochem 75:237–247

    Article  CAS  Google Scholar 

  • Ushio M, Kitayama K, Balser TC (2010) Tree species effects on soil enzyme activities through effects on soil physicochemical and microbial properties in a tropical montane forest on Mt. Kinabalu, Borneo. Pedobiologia 53:227–233

    Article  CAS  Google Scholar 

  • Ushio M, Miki T, Balser TC (2013) A coexisting fungal-bacterial community stabilizes soil decomposition activity in a microcosm experiment. PLoS One 8:e80320

    Article  PubMed  PubMed Central  Google Scholar 

  • Ushio M, Aiba S, Takeuchi Y, Iida Y, Matsuoka S, Repin R, Kitayama K (2017) Plant-soil feedbacks and the dominance of conifers in a tropical montane forest in Borneo. Ecol Monogr 87:105–129

    Article  Google Scholar 

  • Wang J, Huang S, He Q, Bing H, Chen X, Zhang X, Tian X, Zhou J, Wilcke W, Wu Y (2020) Microplate fluorimetric assay of soil leucine aminopeptidase activity: alkalization is not needed before fluorescence reading. Biol Fertil Soils 56:281–285

    Article  CAS  Google Scholar 

  • Wang S, Mori T, Zou S, Zheng H, Heděnec P, Zhu Y, Wang W, Li A, Liu N, Jian S, Liu Z, Tan X, Mo J, Zhang W (2022) Changes in vegetation types affect soil microbial communities in tropical islands of southern China. Glob Ecol Conserv 37:e02162

    Article  Google Scholar 

  • Xu C, Xiang W, Gou M, Chen L, Lei P, Fang X, Deng X, Ouyang S (2018) Effects of Forest restoration on soil carbon, nitrogen, phosphorus, and their stoichiometry in Hunan, Southern China. Sustainability 10:1874

    Article  Google Scholar 

Download references

Acknowledgements

We acknowledge the kind assistance from Sabah Forestry Department and Forest Research Centre for conducting this study. Dr. Yoshimi Sawada assisted fieldworks. Ms. Mayu Sasaki assisted laboratory analyses. Research licenses was granted from Sabah Biodiversity Centre to KK (JKM/MBS.1000-2/2 JLD.7 (177)). This research was supported by the United Nations University GGS Project Fund to KK, and by the MEXT/JSPS KAKENHI Grant Number 18KK0206.

Funding

Author Kanehiro Kitayama has received financial support was provided by United Nations University GGS Project Fund. Author Kanehiro Kitayama has received financial support was provided by MEXT/JSPS KAKENHI (Grant numbers [18KK0206]).

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. Material preparation, collection and analysis were performed by Linzi Jiang. Some methodologies were performed by Masayuki Ushio. The funding acquisition, supervision and project administration were performed by Kanehiro Kitayama. The first draft of the manuscript was written by Linzi Jiang and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Linzi Jiang.

Ethics declarations

Competing interests

The authors have no relevant financial or non-financial interests to disclose.

Additional information

Responsible Editor: Feike A. Dijkstra.

Publisher’s note

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

Supplementary Information

ESM 1

(DOCX 359 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

Jiang, L., Ushio, M. & Kitayama, K. Changes of soil chemical properties, microbial biomass and enzymatic activities along a gradient of forest degradation in logged over tropical rain forests, Borneo. Plant Soil 485, 525–536 (2023). https://doi.org/10.1007/s11104-022-05848-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-022-05848-w

Keywords

Navigation