Skip to main content
SpringerLink
Log in

Effects of condensed tannins in conifer leaves on the composition and activity of the soil microbial community in a tropical montane forest

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

Abstract

Background and aims

Condensed tannins, a dominant class of plant secondary metabolites, play potentially important roles in plant-soil feedbacks by influencing the soil microbial community. Effects of condensed tannins on the soil microbial community and activity were examined by a short-term tannin-addition experiment under field and laboratory conditions.

Methods

Condensed tannins were extracted from the leaves of a dominant conifer (Dacrydium gracilis) in a tropical montane forest on Mt. Kinabalu, Borneo. The extracted tannins were added to soils beneath the conifer and a dominant broadleaf (Lithocarpus clementianus) to evaluate the dependence of the response to tannin addition on the initial composition of the soil microbial community.

Results

Enzyme activities in the field tannin-addition treatment were lower than in the deionized-water treatment. Carbon and nitrogen mineralization were also inhibited by tannin-addition. The fungi-to-bacteria ratio after tannin-addition was higher compared with the distilled-water treatment in the laboratory experiment.

Conclusions

Based on our results, we suggest that the higher concentration of condensed tannins in the leaf tissues of Dacrydium than in those of Lithocarpus is a factor influencing the microbial community and activity. This may have influences on subsequent plant performance, which induces plant-soil feedback processes that can control dynamics of the tropical montane forest ecosystem.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Aiba S, Kitayama K (1999) Structure, composition and species diversity in an altitude-substrate matrix of rain forest tree communities on Mount Kinabalu, Borneo. Plant Ecol 140:139–157

    Article  Google Scholar 

  • Aiba S, Kitayama K, Rebin R (2002) Species composition and species-area relationships of trees in nine permanent plots in altitudinal sequences on different geological substrates of Mount Kinabalu. Sabah Parks Nat J 5:7–69

    Google Scholar 

  • Balser TC, Firestone MK (2005) Linking microbial community composition and soil processes in a California annual grassland and mixed-conifer forest. Biogeochemistry 73:395–415

    Article  CAS  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  PubMed  CAS  Google Scholar 

  • Bowman WD, Steltzer H, Rosenstiel TN, Cleveland CC, Meier CL (2004) Litter effects of two co-occurring alpine species on plant growth, microbial activity and immobilization of nitrogen. Oikos 104:336–344

    Article  Google Scholar 

  • Fierer N, Schimel JP, Cates RG, Zou J (2001) Influence of balsam poplar tannin fractions on carbon and nitrogen dynamics in Alaskan taiga floodplain soils. Soil Biol Biochem 33:1827–1839

    Article  CAS  Google Scholar 

  • Frelich LE, Calcote RR, Davis MB, Pastor J (1993) Patch formation and maintenance in an old-growth hemlock-hardwood forest. Ecology 74:513–527

    Article  Google Scholar 

  • Frostegård A, Tunlid A, Bååth E (1991) Microbial biomass measured as total lipid phosphate in soils of different organic content. J Microbiol Methods 14:151–163

    Article  Google Scholar 

  • Frostegård A, Bååth E, Tunlid A (1993) Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty acid analysis. Soil Biol Biochem 25:723–730

    Article  Google Scholar 

  • Frostegârd A, Tunlid A, Bââth E (2011) Use and misuse of PLFA measurements in soils. Soil Biol Biochem 43:1621–1625

    Article  Google Scholar 

  • Hall SJ, Asner GP, Kitayama K (2004) Substrate, climate, and land use controls over soil N dynamics and N-oxide emissions in Borneo. Biogeochemistry 70:27–58

    Article  CAS  Google Scholar 

  • Hartley SE, Jones CG (1997) Plant chemistry and herbivory: or why the world is green. Plant ecology, 2nd edition edn. Blackwell Science, Cambridge, Mass

  • Hobbie SE (1992) Effects of plant species on nutrient cycling. TREE 7:336–339

    PubMed  CAS  Google Scholar 

  • Kanerva S, Smolander A (2008) How do coniferous needle tannins influence C and N transformations in birch humus layer? Eur J Soil Biol 44:1–9

    Article  CAS  Google Scholar 

  • Kanerva S, Kitunen V, Kiikkilä O, Loponen J, Smolander A (2006) Response of soil C and N transformations to tannin fractions originating from Scots pine and Norway spruce needles. Soil Biol Biochem 38:1364–1374

    Article  CAS  Google Scholar 

  • Kardol P, Cornips NJ, van Kempen MML, Bakx-Schotman JMT, van der Putten WH (2007) Microbe-mediated plant-soil feedback causes historical contingency effects in plant community assembly. Ecol Monogr 77:147–162

    Article  Google Scholar 

  • Kitayama K, Aiba SI, Majalap-Lee N, Ohsawa M (1998) Soil nitrogen mineralization rates of rainforests in a matrix of elevations and geological substrates on Mount Kinabalu, Borneo. Ecol Res 13:301–312

    Article  Google Scholar 

  • Kitayama K, Aiba S, Takyu M, Majalap N, Wagai R (2004a) Soil phosphorus fractionation and phosphorus-use efficiency of a Bornean tropical montane rain forest during soil aging with podozolization. Ecosystems 7:259–274

    Article  CAS  Google Scholar 

  • Kitayama K, Suzuki S, Hori M, Takyu M, Aiba SI, Majalap-Lee N, Kikuzawa K (2004b) On the relationships between leaf-litter lignin and net primary productivity in tropical rain forests. Oecologia 140:335–339

    Article  PubMed  Google Scholar 

  • Kitayama K, Aiba S, Ushio M, Seino T, Fujiki Y (2011) The ecology of porocarps in tropical montane forests of Borneo: distribution, population dynamics, and soil nutrient acquisition. In: Turner BL, Cernusak LA (eds) Ecology of the Podocarpaceae in Tropical Forests, vol 95. Smithsonian contributions to botany. Smithsonian Institution Scholarly Press, Washington DC, pp 101–117

    Google Scholar 

  • Kraal P, Nierop KGJ, Kaal J, Tietema A (2009) Carbon respiration and nitrogen dynamics in Corsican pine litter amended with aluminium and tannins. Soil Biol Biochem 41:2318–2327

    Article  CAS  Google Scholar 

  • Kraus TEC, Dahlgren RA, Zasoski RJ (2003) Tannins in nutrient dynamics of forest ecosystems—A review. Plant Soil 256:41–66

    Article  CAS  Google Scholar 

  • Kuiters AT (1990) Role of phenolic substances from decomposing forest litter in plant-soil interactions. Acta Bot Neerl 39:329–348

    CAS  Google Scholar 

  • Majuakim L (2005) Influence of foliar polyphenols on dissolved organic nitrogen in the soil water of the tropical montane forests on Mount Kinabalu, Borneo. Master Thesis, Kyoto University, Japan

  • Meier CL, Bowman WD (2008) Phenolic-rich leaf carbon fractions differentially influence microbial respiration and plant growth. Oecologia 158:95–107

    Article  PubMed  Google Scholar 

  • Mentzer JL, Goodman RM, Balser TC (2006) Microbial response over time to hydrologic and fertilization treatments in a simulated wet prairie. Plant Soil 284:85–100

    Article  CAS  Google Scholar 

  • Miki T, Ushio M, Fukui S, Kondoh M (2010) Functional diversity of microbial decomposers facilitates plant coexistence in a model of plant-microbe-soil feedback. Proc Natl Acad Sci U S A 107:14251–14256

    Article  PubMed  CAS  Google Scholar 

  • Neill C, Piccolo MC, Cerri CC, Steudler PA, Melillo JM, Brito M (1997) Net nitrogen mineralization and net nitrification rates in soils following deforestation for pasture across the southwestern Brazilian Amazon Basin landscape. Oecologia 110:243–252

    Article  Google Scholar 

  • Nierop KGJ, Verstraten JM, Tietema A, Westerveld JW, Wartenbergh PE (2006) Short- and long-term tannin induced carbon, nitrogen and phosphorus dynamics in Corsican pine litter. Biogeochemistry 79:275–296

    Article  CAS  Google Scholar 

  • Northup RR, Yu Z, Dahlren RA, Vogt KA (1995) Polyphenol control of nitrogen release from pine litter. Nature 377:227–229

    Article  CAS  Google Scholar 

  • Piccolo MC, Neill C, Cerri CC (1994) Net nitrogen mineralization and net nitrification along a tropical forest-to-pasture chronosequence. Plant Soil 162:61–70

    Article  CAS  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Development Core Team (2009) nlme: Linear and Nonlinear Mixed Effects of Models. R package version 3.1

  • Porter LJ, Hrstich LN, Chan BG (1986) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230

    Article  CAS  Google Scholar 

  • R Development Core Team (2011) R: A language and environment for statistical computing. Vienna, Austria

  • Ratledge C, Wilkinson SG (1988) Microbial lipids. Academic, London

    Google Scholar 

  • Scalbert A (1991) Antimicrobial properties of tannins. Phytochemistry 30:3875–3883

    Article  CAS  Google Scholar 

  • Schimel JP, Cates RG, Ruess R (1998) The role of balsam poplar secondary chemicals in controlling soil nutrient dynamics through succession in the Alaskan taiga. Biogeochemistry 42:221–234

    Article  CAS  Google Scholar 

  • Smolander A, Kanerva S, Adamczyk B, Kitunen V (2012) Nitrogen transformations in boreal forest soils-does composition of plant secondary compounds give any explanations? Plant Soil 350:1–26

    Article  CAS  Google Scholar 

  • Strickland MS, Lauber C, Fierer N, Bradford MA (2009) Testing the functional significance of microbial community composition. Ecology 90:441–451. doi:doi:10.1890/08-0296.1

    Article  PubMed  Google Scholar 

  • Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307

    Article  CAS  Google Scholar 

  • Ushio M, Adams JM (2011) A meta-analysis of the global distribution pattern of condensed tannins in woody tree leaves. Open Ecol J 4:18–23

    Article  CAS  Google Scholar 

  • Ushio M, Wagai R, Balser TC, Kitayama K (2008) Variations in the soil microbial community composition of a tropical montane forest ecosystem: does tree species matter? Soil Biol Biochem 40:2699–2702

    Article  CAS  Google Scholar 

  • Ushio M, Miki T, Kitayama K (2009) Phenolic control of plant nitrogen acquisition through the inhibition of soil microbial decomposition processes: a plant-microbe competition model. Microbes Environ 24:180–187

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ushio M, Kitayama K, Balser TC (2010b) Tree species-mediated spatial patchiness of the composition of microbial community and physicochemical properties in the topsoils of a tropical montane forest. Soil Biol Biochem 42:1588–1595

    Article  CAS  Google Scholar 

  • van der Putten WH, Bardgett RD, de Ruiter PC, Hol WHG, Meyer KM, Bezemer TM, Bradford MA, Christensen S, Eppinga MB, Fukami T, Hemerik L, Molofsky J, Schädler M, Scherber C, Strauss SY, Vos M, Wardle DA (2009) Empirical and theoretical challenges in aboveground-belowground ecology. Oecologia 161:1–14

    Article  PubMed  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    Article  PubMed  CAS  Google Scholar 

  • White DC, Ringelberg DB (1998) Signature lipid biomarker analysis. Techniques in microbial ecology. Oxford University Press, New York

    Google Scholar 

  • White DC, Davis WM, Nickels JS, King JD, Bobbie RJ (1979) Determination of the sedimentary microbial biomass by extractible lipid phosphate. Oecologia 40:51–62

    Article  Google Scholar 

  • Wood SN (2004) Stable and efficient multiple smoothing parameter estimation for generalized additive models. J Am Stat Assoc 99:673–686

    Article  Google Scholar 

  • Wurzburger N, Hendrick RL (2009) Plant litter chemistry and mycorrhizal roots promote a nitrogen feedback in a temperate forest. J Ecol 97:528–536

    Article  CAS  Google Scholar 

  • Yao H, He Z, Wilson MJ, Campbell CD (2000) Microbial biomass and community structure in a sequence of soils with increasing fertility and changing land use. Microb Ecol 40:223–237

    PubMed  CAS  Google Scholar 

  • Zelles L, Rackwitz R, Bai QY, Beck T, Beese F (1995) Discrimination of microbial diversity by fatty acid profiles of phospholipids and lipopolysaccharides in differently cultivated soils. Plant Soil 170:115–122

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Prof. Tohru Mitsunaga and Dr. Hiroyuki Takemoto for their support with the tannin extraction procedure. We also thank staffs of the Sabah Parks for their support and permission throughout the course of our research and Dr. Sizuo Suzuki for providing us with the data on leaf phenolics. We also thank Dr. Harry Read, Mr. Kevin Budsberg, Dr. Chao Liang and members of the Balser Lab at the University of Wisconsin-Madison for their support with lipid analysis. This research was supported by a grant-in-aid (MESSC 19380010) to K.K. and in part by Global COE program A06 to Kyoto University. M.U. is supported by JSPS Research Fellowship for Young Scientists (21–1526 and 23–586).

Author information

Author notes

  1. Kanehiro Kitayama

    Present address: Graduate School of Agriculture, Kyoto University, Kitashirakawa, Oiwake, Sakyo-ku, Kyoto, 606-8502, Japan

  2. Teri C. Balser

    Present address: Department of Soil and Water Science, The University of Florida IFAS, Gainesville, USA

Authors and Affiliations

  1. Center for Ecological Research, Kyoto University, 2-509-3 Hirano, Otsu, Shiga, 520-2113, Japan

    Masayuki Ushio & Kanehiro Kitayama

  2. Department of Soil Science, University of Wisconsin-Madison, Madison, WI, 53706, USA

    Teri C. Balser

Authors
  1. Masayuki Ushio
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Teri C. Balser
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kanehiro Kitayama
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Masayuki Ushio.

Additional information

Responsible Editor: Hans Lambers.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 80 kb)

Fig. S1

Cumulative carbon dioxide respired from soil samples in the laboratory experiment. The white and gray bars indicate the control and tannin-addition treatments. The bars indicate the SEM. The results of the statistical analyses are shown in Table 2. (PDF 13 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ushio, M., Balser, T.C. & Kitayama, K. Effects of condensed tannins in conifer leaves on the composition and activity of the soil microbial community in a tropical montane forest. Plant Soil 365, 157–170 (2013). https://doi.org/10.1007/s11104-012-1365-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-012-1365-6

Keywords

Search

Navigation