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Plant interspecific differences in arbuscular mycorrhizal colonization as a result of soil carbon addition

Mycorrhiza volume 23, pages 61–70 (2013)Cite this article

Abstract

Soil nutrient availability and colonization by arbuscular mycorrhizal fungi are important and potentially interacting factors shaping vegetation composition and succession. We investigated the effect of carbon (C) addition, aimed at reducing soil nutrient availability, on arbuscular mycorrhizal colonization. Seedlings of 27 plant species with different sets of life-history traits (functional group affiliation, life history strategy and nitrophilic status) were grown in pots filled with soil from a nutrient-rich set-aside field and amended with different amounts of C. Mycorrhizal colonization was progressively reduced along the gradient of increasing C addition in 17 out of 27 species, but not in the remaining species. Grasses had lower colonization levels than forbs and legumes and the decline in AM fungal colonization was more pronounced in legumes than in other forbs and grasses. Mycorrhizal colonization did not differ between annual and perennial species, but decreased more rapidly along the gradient of increasing C addition in plants with high Ellenberg N values than in plants with low Ellenberg N values. Soil C addition not only limits plant growth through a reduction in available nutrients, but also reduces mycorrhizal colonization of plant roots. The effect of C addition on mycorrhizal colonization varies among plant functional groups, with legumes experiencing an overproportional reduction in AM fungal colonization along the gradient of increasing C addition. We therefore propose that for a better understanding of vegetation succession on set-aside fields one may consider the interrelationship between plant growth, soil nutrient availability and mycorrhizal colonization of plant roots.

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References

  • Bago B, Pfeffer PE, Douds DD, Brouillette J, Bécard G, Shachar-Hill Y (1999) Carbon metabolism in spores of the arbuscular mycorrhizal fungus Glomus intraradices as revealed by nuclear magnetic resonance spectroscopy. Plant Physiol 121:263–271

    PubMed  Article  CAS  Google Scholar 

  • Bezemer TM, Lawson CS, Hedlund K, Edwards AR, Brook AJ, Igual JM, Mortimer SR, Van der Putten WH (2006) Plant species and functional group effects on abiotic and microbial soil properties and plant–soil feedback responses in two grasslands. J Ecol 94:893–904

    Article  CAS  Google Scholar 

  • Blanke V, Renker C, Wagner M, Füllner K, Held M, Kuhn A, Buscot F (2005) Nitrogen supply affects arbuscular mycorrhizal colonization of Artemisia vulgaris in a phosphate-polluted field site. New Phytol 166:981–992

    PubMed  Article  CAS  Google Scholar 

  • Blumenthal DM, Jordan NR, Russelle MP (2003) Soil carbon addition controls weeds and facilitates prairie restoration. Ecol Appl 13:605–615

    Article  Google Scholar 

  • Corbin JD, D'Antonio CM (2004) Can carbon addition increase competitiveness of native grasses? A case study from California. Rest Ecol 12:36–43

    Article  Google Scholar 

  • Cornwell WK, Bedford BL, Chapin CT (2001) Occurrence of arbuscular mycorrhizal fungi in a phosphorus-poor wetland and mycorrhizal response to phosphorus fertilization. Am J Bot 88:1824–1829

    PubMed  Article  CAS  Google Scholar 

  • Ellenberg H (1974) Zeigerwerte der Gefäßflanzen Mitteleuropas. Goltze, Göttingen

    Google Scholar 

  • Eschen R, Müller-Schärer H, Schaffner U (2006) Soil carbon addition affects plant growth in a species-specific way. J Appl Ecol 43:35–42

    Article  CAS  Google Scholar 

  • Eschen R, Mortimer SR, Lawson CS, Edwards AR, Brook AJ, Igual JM, Hedlund K, Schaffner U (2007) Carbon addition alters early succession on ex-arable fields. J Appl Ecol 44:95–104

    Article  CAS  Google Scholar 

  • Eschen R, Müller-Schärer H, Schaffner U (2009) Aboveground environment type, soil nutrient content and arbuscular mycorrhizal fungi explain establishment success of Centaurea jacea on ex-arable land and in late-successional grasslands. Plant Soil 322:115–123

    Article  CAS  Google Scholar 

  • Gange AC, Ayres RL (1999) On the relation between arbuscular mycorrhizal colonization and plant benefit? Oikos 87:615–621

    Article  Google Scholar 

  • Gange AC, Brown VK, Farmer L (1990) A test of mycorrhizal benefit in an early successional plant community. New Phytol 115:85–91

    Article  Google Scholar 

  • Grime JP, Mackey JML, Hillier SH, Read DJ (1987) Floristic diversity in a model system using experimental microcosms. Nature 328:420–422

    Article  Google Scholar 

  • Hansson M, Fogelfors H (1998) Management of permanent set-aside on arable land in Sweden. J Appl Ecol 35:758–771

    Article  Google Scholar 

  • Hodge A, Robinson D, Fitter A (2000) Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci 5:304–308

    PubMed  Article  CAS  Google Scholar 

  • Janos DP (1980) Mycorrhizae influence tropical succession. Biotropica 12:56–64

    Article  Google Scholar 

  • Johnson NC, Rowland DL, Corkidi L, Eggerton-Warburton LM, Allen EB (2003) Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands. Ecology 84:1895–1905

    Article  Google Scholar 

  • Kleijn D (2003) Can establishment characteristics explain the poor colonization success of late successional grassland species on ex-arable land? Rest Ecol 11:131–138

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Koide RT (1991) Nutrient supply, nutrient demand and plant response to mycorrhizal infection. New Phytol 117:365–386

    Article  CAS  Google Scholar 

  • Koide RP, Schreiner RP (1992) Regulation of the arbuscular–vesicular mycorrhizal symbiosis. Ann Rev Plant Phys Mol Biol 43:557–581

    Article  CAS  Google Scholar 

  • Marrs RH (1993) Soil fertility and nature conservation in Europe: theoretical considerations and practical management solutions. Adv Ecol Res 24:241–300

    Article  CAS  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular–arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  • Newman EI, Reddell P (1987) The distribution of mycorrhizas among families of vascular plants. New Phytol 106:745–751

    Article  Google Scholar 

  • Newsham KK, Fitter AH, Watkinson AR (1995) Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol Evol 10:407–411

    PubMed  Article  CAS  Google Scholar 

  • Perry LG, Galatowitsch SM, Rosen CJ (2004) Competitive control of invasive vegetation: a native wetland sedge suppresses Phalaris arundinacea in carbon-enriched soil. J Appl Ecol 41:151–162

    Article  CAS  Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org

  • Schaffers AP, Sýkora KV (2000) Reliability of Ellenberg indicator values for moisture, nitrogen and soil reaction: a comparison with field measurements. J Veg Sci 11:225–244

    Article  Google Scholar 

  • Scheublin TR, Ridgway KP, Young JPW, Van der Heijden MGA (2004) Nonlegumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. Appl Env Microb 70:6240–6246

    Article  CAS  Google Scholar 

  • Schmidt IK, Michelsen A, Jonasson S (1997) Effects of labile soil carbon on nutrient partitioning between an arctic graminoid and microbes. Oecologia 112:557–565

    Article  Google Scholar 

  • Siqueira JO, Carbone Carneiro MA, Curi N, da Silva Rosado SC, Davide AC (1998) Mycorrhizal colonization and mycotrophic growth of native woody species as related to successional groups in Southeastern Brazil. For Ecol Manag 107:241–252

    Article  Google Scholar 

  • Smith SE, Read DJ (1996) Mycorrhizal Symbiosis, 2nd edn. Academic Press, San Diego

    Google Scholar 

  • Tilman D (1993) Species richness of experimental productivity gradients: how important is colonization limitation? Ecology 74:2179–2191

    Article  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 (2002) Arbuscular mycorrhizal fungi as a determinant of plant diversity: in search for underlying mechanisms and general principles. In: Van der Heijden MGA (ed) Mycorrhizal ecology. Springer, Berlin, pp 243–266

    Google Scholar 

  • Van der Heijden MGA (2004) Arbuscular mycorrhizal fungi as support systems for seedling establishment in grassland. Ecol Lett 7:293–303

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Wilson G, Hartnett D (1998) Interspecific variation in plant response to mycorrhizal colonization in tallgrass prairie. Am J Bot 85:1732–1738

    PubMed  Article  CAS  Google Scholar 

  • Zangaro W, Nishidate FR, Spago Camargo FR, Romagnoli GG, Vandressen J (2005) Relationships among arbuscular mycorrhizas, root morphology and seedling growth of tropical native woody species in southern Brazil. J Trop Ecol 21:529–540

    Article  Google Scholar 

Download references

Acknowledgements

We thank Alan Gange for comments on a previous version of the manuscript. This research was supported by grant from the Swiss Federal Office for Education and Science (Project 01.0086) awarded to H.M.S. and U.S. to join the 'TLinks' project funded by the European Commission within the Framework V Energy, Environment and Sustainable Development Programme (EVK2-CT-2001-00123) and by a post-doctoral grant from the Swiss National Science Foundation (PBFRA-114618) awarded to R.E.

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Affiliations

  1. CABI, Rue des Grillons 1, 2800, Delémont, Switzerland

    René Eschen & Urs Schaffner

  2. Department of Biology, Unit Ecology and Evolution, University of Fribourg, 1700, Fribourg, Switzerland

    Heinz Müller-Schärer

Authors
  1. René Eschen
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  2. Heinz Müller-Schärer
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  3. Urs Schaffner
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Correspondence to René Eschen.

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Eschen, R., Müller-Schärer, H. & Schaffner, U. Plant interspecific differences in arbuscular mycorrhizal colonization as a result of soil carbon addition. Mycorrhiza 23, 61–70 (2013). https://doi.org/10.1007/s00572-012-0451-1

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  • DOI: https://doi.org/10.1007/s00572-012-0451-1

Keywords

  • Arbuscular-mycorrhizal fungi
  • C addition
  • Functional plant type
  • Legume species
  • Root colonization
  • Species-specific response