Skip to main content

Advertisement

Log in

Land use and host neighbor identity effects on arbuscular mycorrhizal fungal community composition in focal plant rhizosphere

Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

Arbuscular mycorrhizal fungi (AMF) provide a number of ecosystem services as important members of the soil microbial community. Increasing evidence suggests AMF diversity is at least partially controlled by the identities of plants in the host plant neighborhood. However, much of this evidence comes from greenhouse studies or work in invaded systems dominated by single plant species, and has not been tested in species-rich grasslands. We worked in 67 grasslands spread across the three German Biodiversity Exploratories that are managed primarily as pastures and meadows, and collected data on AMF colonization, AMF richness, AMF community composition, plant diversity, and land use around focal Plantago lanceolata plants. We analyzed the data collected within each Exploratory (ALB Schwäbische Alb, HAI Hainich-Dün, SCH Schorfheide-Chorin) separately, and used variance partitioning to quantify the contribution of land use, host plant neighborhood, and spatial arrangement to the effect on AMF community composition. We performed canonical correspondence analysis to quantify the effect of each factor independently by removing the variation explained by the other factors. AMF colonization declined with increasing land use intensity (LUI) along with concurrent increases in non-AMF, suggesting that the ability of AMF to provide protection from pathogens declined under high LUI. In ALB and HAI mowing frequency and percent cover of additional P. lanceolata in the host plant neighborhood were important for AMF community composition. The similar proportional contribution of land use and host neighborhood to AMF community composition in a focal plant rhizosphere suggests that the diversity of this important group of soil microbes is similarly sensitive to changes at large and small scales.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Antoninka A, Reich PB, Johnson NC (2011) Seven years of carbon dioxide enrichment, nitrogen fertilization and plant diversity influence arbuscular mycorrhizal fungi in a grassland ecosystem. New Phytol 192:200–214

    Article  PubMed  Google Scholar 

  • Barto EK, Rillig MC (2010) Does herbivory really suppress mycorrhiza? A meta-analysis. J Ecol 98:745–753

    Article  Google Scholar 

  • Bever JD (2002) Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proc R Soc Lond B 269:2595–2601

    Article  Google Scholar 

  • Bever JD (2003) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol 157:465–473

    Article  Google Scholar 

  • Bever JD, Morton JB, Antonovics J, Schultz PA (1996) Host-dependent sporulation and species diversity of arbuscular mycorrhizal fungi in a mown grassland. J Ecol 84:71–82

    Article  Google Scholar 

  • Blüthgen N, Dormann CF, Prati D, Klaus VH, Kleinebecker T, Hölzel N, Alt F, Boch S, Gockel S, Hemp A, Müller J, Nieschulze J, Renner SC, Schöning I, Schumacher U, Socher SA, Wells K, Birkhofer K, Buscot F, Oelmann Y, Rothenwöhrer C, Scherber C, Tscharntke T, Weiner CN, Fischer M, Kalko EKV, Linsenmair KE, Schulze E-D, Weisser WW (2012) A quantitative index of land-use intensity in grasslands: integrating mowing, grazing and fertilization. Basic Appl Ecol 13:207–220

    Article  Google Scholar 

  • Borcard D, Legendre P (2002) All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol Model 153:51–68

    Article  Google Scholar 

  • Borcard D, Legendre P, Drapeau P (1992) Partialling out the spatial component of ecological variation. Ecology 73:1045–1055

    Article  Google Scholar 

  • Borcard D, Legendre P, Avois-Jacquet C, Tuomisto H (2004) Dissecting the spatial structure of ecological data at multiple scales. Ecology 85:1826–1832

    Article  Google Scholar 

  • Corradi N, Croll D, Colard A, Kuhn G, Ehinger M, Sanders IR (2007) Gene copy number polymorphisms in an arbuscular mycorrhizal fungal population. Appl Environ Microbiol 73:366–369

    Article  PubMed  CAS  Google Scholar 

  • Culman SW, Bukowski R, Gauch HG, Cadillo-Quiroz H, Buckley DH (2009) T-REX: software for the processing and analysis of T-RFLP data. BMC Bioinformatics 10:171

    Article  PubMed  Google Scholar 

  • Dray S (2010) spacemakeR: spatial modelling. R package version 0.0-5/r83. http://R-Forge.R-project.org/projects/sedar/

  • Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

    Google Scholar 

  • Egerton-Warburton LM, Johnson NC, Allen EB (2007) Mycorrhizal community dynamics following nitrogen fertilization: a cross-site test in five grasslands. Ecol Monogr 77:527–544

    Article  Google Scholar 

  • Eom AH, Hartnett DC, Wilson GWT, Figge DAH (1999) The effect of fire, mowing and fertilizer amendment on arbuscular mycorrhizas in tallgrass prairie. Am Midl Nat 142:55–70

    Article  Google Scholar 

  • Eom AH, Wilson GWT, Hartnett DC (2001) Effects of ungulate grazers on arbuscular mycorrhizal symbiosis and fungal community structure in tallgrass prairie. Mycologia 93:233–242

    Article  Google Scholar 

  • Fischer M, Bossdorf O, Gockel S, Hänsel F, Hemp A, Hessenmöller D, Korte G, Nieschulye J, Pfeiffer S, Prati D, Renner S, Schöning I, Schumacher U, Wells K, Buscot F, Kalko EKV, Linsenmair KE, Schulze E-D, Weisser WW (2010) Implementing large-scale and long-term functional biodiversity research: the Biodiversity Exploratories. Basic Appl Ecol 11:473–485

    Article  Google Scholar 

  • Hausmann NT, Hawkes CV (2009) Plant neighborhood control of arbuscular mycorrhizal community composition. New Phytol 183:1188–1200

    Article  PubMed  Google Scholar 

  • Hawkes CV, Belnap J, D’Antonio C, Firestone MK (2006) Arbuscular mycorrhizal assemblages in native plant roots change in the presence of invasive exotic species. Plant Soil 281:369–380

    Article  CAS  Google Scholar 

  • Johnson D, IJdo M, Genney DR, Anderson IC, Alexander IJ (2005) How do plants regulate the function, community structure, and diversity of mycorrhizal fungi? J Exp Bot 56:1751–1760

    Article  PubMed  CAS  Google Scholar 

  • Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301

    Article  Google Scholar 

  • Lekberg Y, Schnoor T, Kjøller R, Gibbons SM, Hansen LH, Al-Soud WA, Sørensen SJ, Rosendahl S (2012) 454-Sequencing reveals stochastic local reassembly and high disturbance tolerance within arbuscular mycorrhizal fungal communities. J Ecol 100:151–160

    Article  Google Scholar 

  • Mummey DL, Rillig MC, Holben WE (2005) Neighboring plant influences on arbuscular mycorrhizal fungal community composition as assessed by T-RFLP analysis. Plant Soil 271:83–90

    Article  CAS  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H (2012) vegan: community ecology package. R package version 2.0-3. http://CRAN.R-project.org/package=vegan

  • R Development Core Team (2010) R: a language and environment for statistical computing. eds. R Foundation for Statistical Computing, Vienna

  • Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53

    Article  PubMed  CAS  Google Scholar 

  • Rillig MC, Allen MF, Klironomos JN, Chiariello NR, Field CB (1998) Plant species-specific changes in root-inhabiting fungi in a California annual grassland: responses to elevated CO2 and nutrients. Oecologia 113:252–259

    Article  Google Scholar 

  • Saito K, Suyama Y, Sato S, Sugawara K (2004) Defoliation effects on the community structure of arbuscular mycorrhizal fungi based on 18S rDNA sequences. Mycorrhiza 14:363–373

    Article  PubMed  CAS  Google Scholar 

  • Schnoor TK, Lekberg Y, Rosendahl S, Olsson PA (2011) Mechanical soil disturbance as a determinant of arbuscular mycorrhizal fungal communities in semi-natural grassland. Mycorrhiza 2:211–220

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Elsevier Science, London

    Google Scholar 

  • Su YY, Guo LD (2007) Arbuscular mycorrhizal fungi in non-grazed, restored and over-grazed grassland in the Inner Mongolia steppe. Mycorrhiza 17:689–693

    Article  PubMed  Google Scholar 

  • Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355

    Article  Google Scholar 

  • van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310

    Article  PubMed  Google Scholar 

  • van Diepen LTA, Lilleskov EA, Pregitzer KS (2011) Simulated nitrogen deposition affects community structure of arbuscular mycorrhizal fungi in northern hardwood forests. Mol Ecol 20:799–811

    Article  Google Scholar 

  • Verbruggen E, Kiers ET (2010) Evolutionary ecology of mycorrhizal functional diversity in agricultural systems. Evol Appl 3:547–560

    Article  Google Scholar 

  • Veresoglou SD, Rillig MC (2012) Suppression of fungal and nematode plant pathogens through arbuscular mycorrhizal fungi. Biol Lett 8:214–216

    Article  PubMed  Google Scholar 

  • Vierheilig H, Coughlan A, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007

    PubMed  CAS  Google Scholar 

  • Wubet T, Weiß M, Kottke I, Teketay D, Oberwinkler F (2006) Phylogenetic analysis of nuclear small subunit rDNA sequences suggests that the endangered African Pencil Cedar, Juniperus procera, is associated with distinct members of Glomeraceae. Mycol Res 110:1059–1069

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Ruth Lintermann for help in the lab at FU Berlin, and the local-implementation teams in each Exploratory for help in the field. We thank the managers of the three exploratories, Swen Renner, Sonja Gockel, Kerstin Wiesner, and Martin Gorke for their work in maintaining the plot and project infrastructure; Simone Pfeiffer and Christiane Fischer for giving support through the central office, Michael Owonibi for managing the central data base, and Markus Fischer, Eduard Linsenmair, Dominik Hessenmöller, Jens Nieschulze, Daniel Prati, Ingo Schöning, Ernst-Detlef Schulze, Wolfgang W. Weisser and the late Elisabeth Kalko for their role in setting up the Biodiversity Exploratories project. Two anonymous reviewers provided many suggestions for revision. The work has been funded by the DFG Priority Program 1374 “Infrastructure-Biodiversity-Exploratories” (DFG-Refno.). Field work permits were issued by the responsible state environmental offices of Baden-Württemberg, Thüringen, and Brandenburg (according to § 72 BbgNatSchG).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. Kathryn Morris.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 85 kb)

Appendix

Appendix

We collected data on 67 temperate grasslands in the German Biodiversity Exploratories (http://www.biodiversity-exploratories.de/1/home/). Plots were split among three exploratories with 32 in the Schwäbische Alb (AEG2, AEG3, AEG6, AEG7, AEG8, AEG9, AEG11, AEG12, AEG13, AEG15, AEG17, AEG18, AEG21, AEG22, AEG24, AEG25, AEG26, AEG27, AEG28, AEG30, AEG31, AEG32, AEG33, AEG34, AEG36, AEG38, AEG40, AEG41, AEG42, AEG43, AEG47, AEG49), 18 in Hainich Dün (HEG6, HEG8, HEG9, HEG11, HEG17, HEG18, HEG23, HEG24, HEG27, HEG28, HEG29, HEG30, HEG34, HEG36, HEG42, HEG44, HEG46, HEG48), and 17 in Schorfheide-Chorin (SEG31, SEG32, SEG33, SEG34, SEG35, SEG37, SEG38, SEG39, SEG40, SEG41, SEG42, SEG43, SEG44, SEG45, SEG46, SEG47, SEG48). Site details can be found in Fischer et al. (2010).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Morris, E.K., Buscot, F., Herbst, C. et al. Land use and host neighbor identity effects on arbuscular mycorrhizal fungal community composition in focal plant rhizosphere. Biodivers Conserv 22, 2193–2205 (2013). https://doi.org/10.1007/s10531-013-0527-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-013-0527-z

Keywords

Navigation