Skip to main content

Advertisement

Log in

Tree species identity has little impact on the structure of soil bacterial communities in a 10-year-old tropical tree plantation

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

We investigated whether tree species identity has a significant impact on the structure of soil bacterial communities in a tropical tree plantation (Sardinilla, Panama). The experimental site contains tree species native to Panama, planted in both monoculture and mixed-species plots. Using a DNA fingerprinting approach (automated ribosomal intergenic spacer analysis [ARISA]), we identified significant differences in the community structure of abundant bacterial taxa in the bulk soil among all monoculture plots. We similarly found differences among plots containing five, three, one or no tree species. While distance-based gradients in bacterial community structure were detected across the plantation, further investigation revealed that the observed heterogeneity was, in fact, poorly related to the tree species in a given plot. We provide evidence that site related features (e.g., variability in soil pH) play a more important role in regulating the structure of bacterial communities within the bulk soil than tree species identity or richness.

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

Similar content being viewed by others

References

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E Ltd., Plymouth

    Google Scholar 

  • Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful measure of constrained ordination for ecology. Ecology 84:511–525

    Article  Google Scholar 

  • Astorga A, Oksanen J, Luoto M, Soinen J, Virtanen R, Muotka T (2012) Distance decay of similarity in freshwater communities: do macro- and microorganisms follow the same rules? Global Ecol Biogeogr 21:365–375

    Article  Google Scholar 

  • Ayres E, Steltzer H, Berg S, Wallenstein MD, Simmons BL, Wall DH (2009) Tree species traits influence soil physical, chemical, and biological properties in high elevation forests. PLoS One 4:e5964

    Article  PubMed  Google Scholar 

  • Baker KL, Langenheder S, Nicol GW, Ricketts D, Killham K, Campbell CD, Prosser JI (2009) Environmental and spatial characterisation of bacterial composition in soil to inform sampling strategies. Soil Biol Biochem 41:2292–2298

    Article  CAS  Google Scholar 

  • Barnes RJ, Baxter SJ, Lark RM (2007) Spatial covariation of Azotobacter abundance and soil properties: a case study using the wavelet transform. Soil Biol Biochem 39:295–310

    Article  CAS  Google Scholar 

  • Broz AK, Manter DK, Vivanco JM (2007) Soil fungal abundance and diversity: another victim of the invasive plant Centaurea maculosa. ISME J 1:763–765

    Article  PubMed  CAS  Google Scholar 

  • Ceccherini MT, Ascher J, Agnelli A, Certini G, Pietramellara G, Piovanelli C, Nannipieri P (2008) Tree bark and soil ammonia oxidizers: a molecular study on a historic forest of central Italy. Fresenius Environmenal Bulletin 17:882–889

    CAS  Google Scholar 

  • Cesco S, Mimmo T, Tonon G, Tomasi N, Pinton R, Terzano R, Neumann G, Weisskopf L, Renella G, Landi L, Nannipieri P (2012) Plant-borne flavenoids released in the rhizosphere: impact on soil bio-activities related to plant nutrition. A review. Biol Fert Soil 48:123–149

    Article  CAS  Google Scholar 

  • Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fert Soil 48:489–499

    Article  Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER v.6: User manual/tutorial. PRIMER-E, Plymouth

    Google Scholar 

  • Davidson J, Opik M, Zobel M, Vasar M, Metsis M, Moora M (2012) Communities of arbuscular mycorrhizal fungi detected in forest soil are spatially heterogeneous but do not vary throughout the growing season. PLoS One 7:e41938

    Article  Google Scholar 

  • De Ridder-Duine AS, Kowalchuk GA, Klein Gunnewiek PJA, Smant W, Van Veen JA, de Boer W (2005) Rhizosphere bacterial community composition in natural stands of Carex arenaria (sand sedge) is determined by bulk soil community composition. Soil Biol Biochem 37:349–357

    Article  Google Scholar 

  • Delagrange S, Potvin C, Messier C, Coll L (2008) Linking multiple-level tree traits with biomass accumulation in native tree species used for reforestation in Panama. Trees Struct Funct 22:585–596

    Article  Google Scholar 

  • Di HJ, Cameron KC, Shen JP, Winefield CS, O’Callaghan M, Bowatte S, He JZ (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621–624

    Article  CAS  Google Scholar 

  • Fenchel T, Finlay BJ (2004) The ubiquity of small species: patterns of local and global diversity. Bioscience 54:777–784

    Article  Google Scholar 

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. P Natl Acad Sci USA 103:626–631

    Article  CAS  Google Scholar 

  • Finlay BJ, Clarke KJ (1999) Ubiquitous dispersal of microbial species. Nature 400:828

    Article  CAS  Google Scholar 

  • Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. P Natl Acad Sci USA 102:14683–14688

    Article  CAS  Google Scholar 

  • Franklin RB, Mills AL (2009) Importance of spatially structured environmental heterogeneity in controlling microbial community composition at small spatial scales in an agricultural field. Soil Biol Biochem 41:1833–1840

    Article  CAS  Google Scholar 

  • Geets J, de Cooman M, Wittebolle L, Heylen K, Vanparys B, De Vos P, Verstraete W, Boon N (2007) Real-time PCR assay for the simultaneous quantification of nitrifying and denitrifying bacteria in activated sludge. Appl Microbiol Biotechnol 75:211–221

    Article  PubMed  CAS  Google Scholar 

  • Gomes NM, Heuer H, Schonfeld J, Costa R, Mendonca-Hagler L, Smalla K (2001) Bacterial diversity of the rhizosphere of maize (Zea mays) grown in tropical soil studied by temperature gradient gel electrophoresis. Plant Soil 232:167–180

    Article  CAS  Google Scholar 

  • Griffiths RI, Thomson BC, James P, Bell T, Bailey MJ, Whiteley AS (2011) The bacterial biogeography of British soils. Environ Microbiol 13:1642–1654

    Article  PubMed  Google Scholar 

  • Hackl E, Zechmeister-Boltenstern S, Bodrossy L, Sessitsch A (2004) Comparison of diversities and compositions of bacterial populations inhabiting natural forest soils. Appl Environ Microbiol 70:5057–5065

    Article  PubMed  CAS  Google Scholar 

  • Healy C, Gotelli NJ, Potvin C (2008) Partioning the effects of biodiversity and environmental heterogeneity for productivity and mortality in a tropical tree plantation. J Ecol 96:903–913

    Article  Google Scholar 

  • Houlden A, Timms-Wilson TM, Day MJ, Bailey MJ (2008) Influence of plant developmental stage on microbial community structure and activity in the rhizosphere of three field crops. FEMS Microbiol Ecol 65:193–201

    Article  PubMed  CAS  Google Scholar 

  • Inceoglu O, Falcao Salles J, van Overbeek L, Van Elsas JD (2010) Effects of plant genotype and growth stage on the Betaproteobacterial communties associated with differnte potato cultivars in two fields. Appl Environ Microbiol 76:3675–3684

    Article  PubMed  CAS  Google Scholar 

  • Innes L, Hobbs PJ, Bardgett RD (2004) The impacts of individual plant species on rhizosphere microbial communities in soils of different fertility. Biol Fert Soil 40:7–13

    Article  Google Scholar 

  • Jacob M, Viedenz K, Polle A, Thomas FM (2010) Leaf litter decomposition in temperate deciduous forest stands with a decreasing fraction of beech (Fagus sylvatica). Oecologia 164:1083–1094

    Article  PubMed  Google Scholar 

  • Kaiser C, Koranda M, Kitzler B, Fuchsleuger L, Schnecker J, Schweiger P, Rasche F, Zechmeister-Boltenstern S, Sessitsch A, Richter A (2010) Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil. New Phytol 187:843–858

    Article  PubMed  CAS  Google Scholar 

  • Kandeler E, Marschner P, Tscherko D, Gahoonia TS, Nielsen NE (2001) Microbial community composition and functional diversity in the rhizosphere of maize. Plant Soil 238:301–312

    Article  Google Scholar 

  • Kowalchuk GA, Buma DS, de Boer W, Klinkhamer PGL, Van Veen JA (2002) Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Anton Leeuw Int J G 81:509–520

    Article  Google Scholar 

  • Lakshmanan V, Kumar AS, Bais HP (2012) The ecological significance of plant-associated biofilms. In: Lear G, Lewis GD (eds) Microbial biofilms: Current research and applications. Caister Academic Press, Norfolk, pp 43–60

    Google Scholar 

  • Lear G, Anderson MJ, Smith JP, Boxen K, Lewis GD (2008) Spatial and temporal heterogeneity of the bacterial communities in stream epilithic biofilms. FEMS Microbiol Ecol 65:463–473

    Article  PubMed  CAS  Google Scholar 

  • Lear G, Boothroyd IKG, Turner SJ, Roberts K, Lewis GD (2009) A comparison of bacteria and benthic invertebrates as indicators of ecological health within streams. Freshwat Biol 54:1532–1543

    Article  CAS  Google Scholar 

  • Lear G, Lewis GD (2009) Nested automated ribosomal intergenic spacer analysis: a rapid and accurate method for comparison of bacterial community composition. J Rapid Meth Aut Microbiol 17:257–270

    Article  CAS  Google Scholar 

  • Lejon D, Chaussod R, Ranger J, Ranjard L (2005) Microbial community structure and density under different tree species in an acid forest soil (Morvan, France). Microbiol Ecol 50:614–625

    Article  Google Scholar 

  • Llinares F, Munoz-Mingarro D, Pozuelo JM, Ramos B, Bermudez de Castro F (1994) Microbial inhibition and nitrification potential in soils incibated with Elaeagnus angustifolia L. leaf litter. Geomicrobiol J 11:149–156

    Article  Google Scholar 

  • Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10

    Article  CAS  Google Scholar 

  • Marschner P, Marhan S, Kandeler E (2012) Microscale distribution and function of soil microorgniams in the interface between rhizosphere and detritusphere. Soil Biol Biochem 49:174–184

    Article  CAS  Google Scholar 

  • Martiny JBH, Eisen JA, Penn K, Allison SD, Horner-Devine MC (2011) Drivers of bacterial beta-diversity depend on spatial scale. P Natl Acad Sci USA 108:7850–7854

    Article  CAS  Google Scholar 

  • McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297

    Article  Google Scholar 

  • Mummey DL, Rillag MC (2008) Spatial characterization of arbuscular mycorrhizal fungal molecular diversity at the submetre scale in a temperate grassland. FEMS Microbiol Ecol 64:260–270

    Article  PubMed  CAS  Google Scholar 

  • Nacke H, Thurmer A, Wollher A, Will C, Hodac L, Herold N, Schoning I, Schrumpf M, Daniel R (2011) Pyrosequencing-based assessment of bacterial community structure along different management types in German forest and grassland soils. PLoS One 6:e17000

    Article  PubMed  CAS  Google Scholar 

  • Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G, Valori F (2008) Effects of root exudates on microbial diversity and activity in rhizosphere soils. In: Nautiyal CS, Dion P (eds) Molecular mechanisms of plant and microbe coexistence. Springer, Heideleberg, pp 339–365

    Chapter  Google Scholar 

  • Nekola JC, White PS (1999) The distance decay of similarity in biogeography and ecology. J Biogeog 26:867–878

    Article  Google Scholar 

  • Oelmann Y, Potvin C, Mark T, Werther L, Tapernon S, Wilcke W (2010) Tree mixture effects on aboveground nutrient pools of trees in an experimental plantation in Panama. Plant Soil 326:199–212

    Article  CAS  Google Scholar 

  • Philippot L, Hallin S, Borjesson G, Baggs EM (2008) Biogeochemical cycling in the rhizosphere having an impact on global change. Plant Soil 321:61–81

    Article  Google Scholar 

  • Plath M, Mody K, Potvin C, Dorn S (2011) Establishment of native tropical trees in monoculture and mixed-species plantations: small-scale effects on tree performance and insect herbivory. Forest Ecol Manag 261:741–750

    Article  Google Scholar 

  • Potvin C, Mancilla L, Buchmann N, Monteza J, Moore T, Murphy M, Oelmann Y, Schere-Lorenzen M, Turner BL, Wilcke W, Zeugin F, Wolf S (2010) An ecosystem approach to biodiversity effects: Carbon pools in a tropical tree plantation. Forest Ecol Manag 260:1614–1624

    Google Scholar 

  • Ranjard L, Poly F, Lata JC, Mougal C, Thioulouse J, Nazaret S (2001) Characterization of bacterial and fungal soil communities by automated ribosomal intergenic spacer analysis fingerprints: Biological and methodological variability. Appl Environ Microbiol 67:4479–4487

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Loinaz G, Onaindia M, Amezaga I, Mijangos I, Garbisu C (2008) Relationship between vegetation diversity and soil functional diversity in native mixed-oak forests. Soil Biol Biochem 40:49–60

    Article  CAS  Google Scholar 

  • Rotthauwe J, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoa as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712

    PubMed  CAS  Google Scholar 

  • Rousk J, Baath E, Brookes PC, Lauber CL, Luzopone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351

    Article  PubMed  Google Scholar 

  • Scherer-Lorenzen M, Bonilla JL, Potvin C (2007) Tree species richness affects litter production and decomposition rates in a tropical biodiversity experiment. Oikos 116:2108–2124

    Article  Google Scholar 

  • Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751

    Article  PubMed  CAS  Google Scholar 

  • Uren NC (2007) Types, amounts and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere biochemistry and organic substances at the soil–plant interface. CRC Press, Boca Raton, pp 1–21

    Chapter  Google Scholar 

  • Vesterdal L, Schmidt IK, Callsen I, Nilsson LO, Gundersen P (2008) Carbon and nitrogen in forest floor and mineral soil under six common European tree species. Forest Ecol Manag 255:35–48

    Article  Google Scholar 

  • Warembourg FR, Paul EA (1973) The use of 14CO2 canopy techniques for measuring carbon transfer through the plant–soil system. Plant Soil 38:31–345

    Article  Google Scholar 

  • Wolf S, Eugster W, Potvin C, Turner BL, Buchmann N (2011) Carbon sequestration potential of tropical pasture compared with afforestation in Panama. Glob Chang Biol 17:2763–2780

    Article  Google Scholar 

  • Zeugin F, Potvin C, Jansa J, Schere-Lorenzen M (2010) Is tree diversity an important driver for phosphorus and nitrogen aquistion of a young tropical plantation? Forest Ecol Manag 260:1424–1433

    Article  Google Scholar 

Download references

Acknowledgements

This work was funded by the Lincoln University Research Fund (Lear) and The University of Auckland Faculty Research Development Fund (Schwendenmann) with additional support from the Royal Society of New Zealand Marsden fund (Grant No. LU10901). Support for Taiga Yamamura was provided by the Lincoln University summer scholarship program. This study benefitted greatly from the logistical support provided by the Smithsonian Tropical Research Institute, Panama. We are particularly grateful to Catherine Potvin (McGill University, Canada) for her kind permission to conduct this study at the Sardinilla biodiversity experiment, Norbert Kunert (Max Planck Institute for Biogeochemistry, Germany) for his kind assistance with sample collection and the Centre for Soil and Environmental Research, Lincoln University, for assistance in qPCR analysis. The research was conducted under permits (SEX/P-60-10, SE/P-16-11) issued by ANAM (Autoridad Nacional del Ambiente, Panama).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gavin Lear.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

PERMANOVA of bacterial community ARISA profiles obtained from soil surrounding each tree in each monoculture plot sampled in December 2010, completed on the basis of the Bray Curtis similarity measure, and showing partitioning of multivariate variation and tests for the factors of Species, Tree and their interactions (DOC 29 kb)

Table S2

Diversity measures obtained for plots planted with 5, 3, 1 or no tree species (5 sp, 3 sp, 1 sp and 0 sp, respectively) sampled in July 2011. Data for 5 sp and 3 sp relate to samples taken from plots A3 and T4, respectively. Data for 0 sp relate to samples taken from plots Ca1 and Ca2. Data for 1 sp relate to samples taken from all monoculture plots. The average taxa diversity of monoculture plots planted with different tree species (Ae, Cm, Hc, Ls and Tr) is also shown (DOC 54 kb)

Table S3

Relationship between ARISA profiles on the basis of the Bray Curtis similarity measure and recorded environmental variables, analysed with a forward selection procedure using a DISTLM (DOC 30 kb)

Figure S4

Canonical analysis of the relationship between soil pH and bacterial community structure. Canonical distance is the relative position of datasets in the first dimension, generated from multi-dimensional scaling using the Bray-Curtis similarity measure (PPTX 82 kb)

Table S5

Key soil characteristics obtained for plots comprised of 5, 3, 1 or 0 tree species. Data for 5 sp and 3 sp relate to samples taken from plots A3 and T4, respectively. Data for 0 sp relate to samples taken from plots Ca1 and Ca2. Data for 1 sp relate to samples taken from all monoculture plots. The average taxa diversity of monoculture plots planted with different tree species (Ae, Cm, Hc, Ls and Tr) is also shown (DOC 60 kb)

Table S6

Abundance of bacterial amoA and archaeal amoA genes in plots with 5, 3, 1 or no tree species (5 sp, 3 sp, 1 sp and 0 sp, respectively). Data for 5 sp and 3 sp relate to samples taken from plots A3 and T4. Data for 0 sp relate to samples taken from plots Ca1 and Ca2. Data for 1 sp relate to samples taken from all monoculture plots. The average taxa diversity of monoculture plots planted with different tree species (Ae, Cm, Hc, Ls and Tr) is also shown. Data for nosZ genes were below detection. (DOC 47 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yamamura, T., Schwendenmann, L. & Lear, G. Tree species identity has little impact on the structure of soil bacterial communities in a 10-year-old tropical tree plantation. Biol Fertil Soils 49, 819–828 (2013). https://doi.org/10.1007/s00374-013-0774-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-013-0774-x

Keywords

Navigation