Arbuscular mycorrhizal fungi (AMF) are expected to be one of the key drivers determining the diversity of natural plant communities, especially in nutrient-poor and dry habitats. Several previous studies have explored the importance of AMF for the composition of plant communities in various types of habitats. Surprisingly, studies of the role of AMF in nutrient-poor dry grassland communities dominated by less mycotrophic plant species are still relatively rare. We present the results of a 3-year study in which a plant community in a species-rich dry grassland was subjected to the fungicide carbendazim to suppress AMF colonization. We tested the effect of the fungicide on the following parameters: the plant species composition; the number of plant species; the cover of the rare, highly mycorrhiza-dependent species Aster amellus; the cover of the dominant, less mycorrhiza-dependent species Brachypodium pinnatum; and the cover of graminoids and perennial forbs. In addition, we examined the mycorrhizal inoculation potential of the soil. We found that the suppression of AMF with fungicide resulted in substantial changes in plant species composition and significant decrease in species richness, the cover of A. amellus and the cover of perennial forbs. In contrast the species increasing their cover after fungicide application were graminoids--the C3 grasses B. pinnatum and Bromus erectus and the sedge Carex flacca. These species appear to be less mycorrhiza dependent. Moreover, due to their clonal growth and efficient nutrient usage, they are, most likely, better competitors than perennial forbs under fungicide application. Our results thus suggest that AMF are an essential part of the soil communities supporting a high diversity of plant species in species-rich dry grasslands in nutrient-poor habitats. The AMF are especially important for the maintenance of the populations of perennial forbs, many of which are rare and endangered in the area.

Institute of Botany Academy of Sciences of the Czech Republic Průhonice Czech Republic ; Department of Botany Faculty of Science Charles University Prague Czech Republic

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Gange AC, Brown VK, Sinclair GS (1993) Vesicular-Arbuscular Mycorrhizal Fungi: A Determinant of Plant Community Structure in Early Succession. Funct Ecol 7: 616-622. doi:10.2307/2390139. DOI

Francis R, Read D (1994) The contributions of mycorrhizal fungi to the determination of plant community structure. Plant Soil 159: 11-25.

Smith MD, Hartnett DC, Wilson GWT (1999) Interacting influence of mycorrhizal symbiosis and competition on plant diversity in tallgrass prairie. Oecologia 121: 574-582. doi:10.1007/s004420050964. PubMed DOI

Schweiger P, Spliid N, Jakobsen I (2001) Fungicide application and phosphorus uptake by hyphae of arbuscular mycorrhizal fungi into field-grown peas. Soil Biol Biochem 33: 1231-1237. doi:10.1016/S0038-0717(01)00028-1. DOI

Smith SE, Read DJ (2008) Mycorrhizal Symbiosis. Academic Press. 816 pp.

Allison V, Rajaniemi T, Goldberg D, Zak D (2007) Quantifying direct and indirect effects of fungicide on an old-field plant community: an experimental null-community approach. Plant Ecol 190: 53-69. doi:10.1007/s11258-006-9190-8. DOI

Šmilauer P, Šmilauerová M (2000) Effect of AM Symbiosis Exclusion on Grassland Community Composition. Folia Geobot 35: 13-25. doi:10.1007/BF02803084. DOI

Hartnett DC, Hetrick BAD, Wilson GWT, Gibson DJ (1993) Mycorrhizal Influence on Intra- and Interspecific Neighbour Interactions among Co-Occurring Prairie Grasses. J Ecol 81: 787-795. doi:10.2307/2261676. DOI

Hetrick B, Hartnett D, Wilson G, Gibson D (1994) Effects of Mycorrhizae, Phosphorus Availability, and Plant-Density on Yield Relationships Among Competing Tallgrass Prairie Grasses. Can J Bot 72: 168-176. doi:10.1139/b94-023. DOI

Van der Heijden MGA, Boller T, Wiemken A, Sanders IR (1998) Different Arbuscular Mycorrhizal Fungal Species Are Potential Determinants of Plant Community Structure. Ecology 79: 2082-2091. doi:10.1890/0012-9658(1998)079[2082:DAMFSA]2.0.CO;2. DOI

Van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R et al. (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69-72. doi:10.1038/23932. DOI

Hartnett DC, Wilson GWT (1999) Mycorrhizae Influence Plant Community Structure and Diversity in Tallgrass Prairie. Ecology 80: 1187-1195. doi:10.1890/0012-9658(1999)080[1187:MIPCSA]2.0.CO;2. DOI

O’Connor PJ, Smith SE, Smith FA (2002) Arbuscular mycorrhizas influence plant diversity and community structure in a semiarid herbland. New Phytol 154: 209-218. doi:10.1046/j.1469-8137.2002.00364.x. DOI

Grime J, Mackey J, Hillier S, Read D (1987) Floristic Diversity in a Model System Using Experimental Microcosms. Nature 328: 420-422. doi:10.1038/328420a0. DOI

Karanika E, Mamolos A, Alifragis D, Kalburtji K, Veresoglou D (2008) Arbuscular mycorrhizas contribution to nutrition, productivity, structure and diversity of plant community in mountainous herbaceous grassland of northern Greece. Plant Ecol 199: 225-234. doi:10.1007/s11258-008-9427-9. DOI

Fitter A (1986) Effect of Benomyl on Leaf Phosphorus Concentration in Alpine Grasslands - a Test of Mycorrhizal Benefit. New Phytol 103: 767-776. doi:10.1111/j.1469-8137.1986.tb00851.x. DOI

Fitter AH, Nichols R (1988) The use of benomyl to control infection by vesicular–arbuscular mycorrhizal fungi. New Phytol 110: 201-206. doi:10.1111/j.1469-8137.1988.tb00253.x. DOI

Wilson G, Hartnett D (1997) Effects of mycorrhizae on plant growth and dynamics in experimental tall grass prairie microcosms. Am J Bot 84: 478-478. doi:10.2307/2446024. PubMed: 21708601. PubMed DOI

Wilson GWT, Hartnett DC, Smith MD, Kobbeman K (2001) Effects of mycorrhizae on growth and demography of tallgrass prairie forbs. Am J Bot 88: 1452-1457. doi:10.2307/3558453. PubMed: 21669678. PubMed DOI

McCain K, Wilson G, Blair J (2011) Mycorrhizal suppression alters plant productivity and forb establishment in a grass-dominated prairie restoration. Plant Ecol 212: 1675-1685. doi:10.1007/s11258-011-9940-0. DOI

Helgason T, Merryweather JW, Young JPW, Fitter AH (2007) Specificity and resilience in the arbuscular mycorrhizal fungi of a natural woodland community. J Ecol 95: 623-630. doi:10.1111/j.1365-2745.2007.01239.x. DOI

Zobel M, Pilt I, Moora M, Pärtel M, Liira J (1999) Small-scale dynamics of plant communities in an experimentally polluted and fungicide-treated subarctic birch-pine forest. Acta Oecol 20: 29-37. doi:10.1016/S1146-609X(99)80013-7. DOI

Koorem K, Saks Ü, Sõber V, Uibopuu A, Öpik M et al. (2012) Effects of arbuscular mycorrhiza on community composition and seedling recruitment in temperate forest understory. Basic Appl Ecol 13: 663-672.

Newsham KK, Watkinson AR, West HM, Fitter AH (1995) Symbiotic Fungi Determine Plant Community Structure: Changes in a Lichen- Rich Community Induced by Fungicide Application. Funct Ecol 9: 442-447. doi:10.2307/2390007. DOI

Jordan N, Huerd S (2008) Effects of soil fungi on weed communities in a corn–soybean rotation. Renew Agr Foods Syst 23: 108-117.

Dhillion SS, Gardsjord TL (2004) Arbuscular mycorrhizas influence plant diversity, productivity, and nutrients in boreal grasslands. Can J Bot 82: 104-114. doi:10.1139/b03-139. DOI

Koide RT, Huenneke LF, Hamburg SP, Mooney HA (1988) Effects of Applications of Fungicide, Phosphorus and Nitrogen on the Structure and Productivity of an Annual Serpentine Plant Community. Funct Ecol 2: 335-344. doi:10.2307/2389406. DOI

Blanke V, Wagner M, Renker C, Lippert H, Michulitz M et al. (2011) Arbuscular mycorrhizas in phosphate-polluted soil: interrelations between root colonization and nitrogen. Plant Soil 343: 379-392. doi:10.1007/s11104-011-0727-9. DOI

Bolliger J, Edwards TC Jr., Eggenberg S, Ismail S, Seidl I et al. (2011) Balancing Forest-Regeneration Probabilities and Maintenance Costs in Dry Grasslands of High Conservation Priority. Conserv Biol 25: 567-576. doi:10.1111/j.1523-1739.2010.01630.x. PubMed: 21175843. PubMed DOI

O’Connor P, Manjarrez M, Smith SE (2009) The fate and efficacy of benomyl applied to field soils to suppress activity of arbuscular mycorrhizal fungi. Can J Microbiol 55: 901-904. doi:10.1139/W09-035. PubMed: 19767864. PubMed DOI

Wilson GWT, Hartnett DC (1998) Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. Am J Bot 85: 1732-1738. doi:10.2307/2446507. PubMed: 21680333. PubMed DOI

Gange A, Brown V, Farmer L (1990) A Test of Mycorrhizal Benefit in an Early Successional Plant Community. New Phytol 115: 85-91. doi:10.1111/j.1469-8137.1990.tb00925.x. DOI

Chýlová T, Münzbergová Z (2008) Past land use co-determines the present distribution of dry grassland plant species. Preslia 80: 183-198.

Studnička M (1972) Dry grasslands in České Středohoří : A study of ecology and fytocenology. M.S. thesis Prague: Charles University.

Ellenberg H (1988) Vegetation Ecology of Central Europe. UK: Cambridge University Press. 758 pp.

Raabová J, Münzbergová Z, Fischer M (2007) Ecological rather than geographic or genetic distance affects local adaptation of the rare perennial herb, Aster Amellus. Biol Conserv 139: 348-357. doi:10.1016/j.biocon.2007.07.007. DOI

Münzbergová Z (2004) Effect of spatial scale on factors limiting species distributions in dry grassland fragments. J Ecol 92: 854-867. doi:10.1111/j.0022-0477.2004.00919.x. DOI

Tremlová K, Münzbergová Z (2007) Importance of species traits for species distribution in fragmented landscapes. Ecology 88: 965-977. doi:10.1890/06-0924. PubMed: 17536712. PubMed DOI

Knappová J, Hemrová L, Münzbergová Z (2012) Colonization of central European abandoned fields by dry grassland species depends on the species richness of the source habitats: a new approach for measuring habitat isolation. Landsc Ecol 27: 97-108. doi:10.1007/s10980-011-9680-5. DOI

Knappová J, Knapp M, Münzbergová Z (2013) Spatio-Temporal Variation in Contrasting Effects of Resident Vegetation on Establishment, Growth and Reproduction of Dry Grassland Plants: Implications for Seed Addition Experiments. PLOS ONE 8: e65879. doi:10.1371/journal.pone.0065879. PubMed: 23755288. PubMed DOI PMC

Environmental Protection Agency (2001) Benomyl; Cancellation Order. Available: http://www.epa.gov/EPA-PEST/2001/August/Day-08/p19572.htm. Accessed 2013 October 17.

Helweg A (1973) Undersoegelser over fungicidet benomyl i jord. I. Stabilitet og biologisk nedbrydning. (Investigations on the fungicide benomyl in soil. I stabilim and biological decomposing.) Statens Forsogs Plant: 232-243..

Tang CS, Yanagihara K, Zhang Y (1992) 1-butyl isocyanate from aqueous Benlate® formulations. Arch Environ Contam Toxicol 23: 270-272. doi:10.1007/BF00212286. DOI

Kahiluoto H, Vestberg M (2000) Creation of a non-mycorrhizal control for a bioassay of AM effectiveness. Mycorrhiza 9: 259-270. doi:10.1007/PL00009990. DOI

Westhoff V, van der Maarel E (1978) The Braun-Blanquet approach. In: Whittaker RH. Classification of plant communities. Den Haag, NL: Dr. W Jung. pp. 287-399.

Castro S, Loureiro J, Procházka T, Münzbergová Z (2012) Cytotype distribution at a diploid–hexaploid contact zone in Aster Amellus (Asteraceae). Ann Bot 110: 1047-1055. doi:10.1093/aob/mcs177. PubMed: 22887024. PubMed DOI PMC

Pánková H, Münzbergová Z, Rydlová J, Vosátka M (2008) Differences in AM fungal root colonization between populations of perennial Aster species have genetic reasons. Oecologia 157: 211-220. doi:10.1007/s00442-008-1064-4. PubMed: 18523810. PubMed DOI

Pánková H, Münzbergová Z, Rydlová J, Vosátka M (2011) The response of Aster Amellus (Asteraceae) to mycorrhiza depends on the origins of both the soil and the fungi. Am J Bot 98: 850-858. doi:10.3732/ajb.0900350. PubMed: 21613062. PubMed DOI

Sudová R, Rydlová J, Münzbergová Z, Suda J (2010) Ploidy-specific interactions of three host plants with arbuscular mycorrhizal fungi: Does genome copy number matter? Am J Bot 97: 1798-1807. doi:10.3732/ajb.1000114. PubMed: 21616819. PubMed DOI

Wilson J, Trinick M (1983) Factors Affecting the Estimation of Numbers of Infective Propagules of Vesicular Arbuscular Mycorrhizal Fungi by the Most Probable Number Method. Aust J Crops Sci 21: 73-81.

Koske R, Gemma J (1989) A Modified Procedure for Staining Roots to Detect VA-Mycorrhizas. Mycol Res 92: 486-505. doi:10.1016/S0953-7562(89)80195-9. DOI

Giovannetti M, Mosse B (1980) An Evaluation of Techniques for Measuring Vesicular Arbuscular Mycorrhizal Infection in Roots. New Phytol 84: 489-500. doi:10.1111/j.1469-8137.1980.tb04556.x. DOI

Ehrenberger F, Gorbach S (1973) Methoden der organischen Elementar- und Spurenanalyse. Weinheim: Verlag Chemie.

Lepš J, Šmilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press. 292 pp.

Ter Braak CJF, Šmilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5). Microcomputer Power Ithaca, NY.

Pedersen CT, Sylvia DM (1997) Limitations to using benomyl in evaluating mycorrhizal functioning. Biol Fertil Soils 25: 163-168.

Van der Heijden MGA (2004) Arbuscular mycorrhizal fungi as support systems for seedling establishment in grassland. Ecol Lett 7: 293-303. doi:10.1111/j.1461-0248.2004.00577.x. DOI

Jones MD, Smith SE (2004) Exploring functional definitions of mycorrhizas: Are mycorrhizas always mutualisms? Can J Bot 82: 1089-1109. doi:10.1139/b04-110. DOI

Harley JL, Harley EL (1987) A Check-List of Mycorrhiza in the British Flora. New Phytol 105: 1-102. doi:10.1111/j.1469-8137.1987.tb00107.x. DOI

Muthukumar T, Udaiyan K, Shanmughavel P (2004) Mycorrhiza in sedges–an overview. Mycorrhiza 14: 65-77. doi:10.1007/s00572-004-0296-3. PubMed: 14999550. PubMed DOI

Bobbink R (1991) Effects of Nutrient Enrichment in Dutch Chalk Grassland. J Appl Ecol 28: 28-41. doi:10.2307/2404111. DOI

Turnau K (1998) Heavy metal content and localization in mycorrhizal Euphorbia cyparissias zinc wastes in southern Poland. Acta Soc Bot Pol Pol Tow Bot 67: 105-113.

Pendleton RL, Pendleton BK, Howard GL, Warren SD (2004) Response of Lewis flax seedlings to inoculation with arbuscular mycorrhizal fungi and cyanobacteria. In: Hild AL, Shaw NL, Meyer SE. Seed and soil dynamics in shrubland ecosystems. USDA Forest Service Proceedings. Available: http://www.fs.fed.us/rm/pubs/rmrs_p031/rmrs_p031_064_068.pdf. Accessed 2013 February 26.

Doubková P, Suda J, Sudová R (2011) Arbuscular mycorrhizal symbiosis on serpentine soils: the effect of native fungal communities on different Knautia arvensis ecotypes. Plant Soil 345: 325-338. doi:10.1007/s11104-011-0785-z. DOI

Grime JP, Hodgson JG, Hunt R (1988) Comparative plant ecology. A Funct Approach Common British Species: 742.

Crawley M (2009) Plant Ecology. John Wiley & Sons. 742 pp.

Newsham KK, Fitter AH, Watkinson AR (1994) Root Pathogenic and Arbuscular Mycorrhizal Fungi Determine Fecundity of Asymptomatic Plants in the Field. J Ecol 82: 805-814. doi:10.2307/2261445. DOI

Burrows LA, Edwards CA (2000) The effects of the fungicide carbendazim in an innovative integrated terrestrial microcosm system. British Crop Protection Council; pp. 365-370.

Chen S-K, Edwards CA (2001) A microcosm approach to assess the effects of fungicides on soil ecological processes and plant growth: comparisons of two soil types. Soil Biol Biochem 33: 1981-1991. doi:10.1016/S0038-0717(01)00132-8. DOI

Mazur AR (1977) Soil microorganisms and preventive fungicide programs - What are the interactions?. Available: http://gsr.lib.msu.edu/1970s/1977/770504.pdf. Accessed 2013 October 17.

The role of plant-soil feedback in long-term species coexistence cannot be predicted from its effects on plant performance

Arbuscular mycorrhizal fungi and associated microbial communities from dry grassland do not improve plant growth on abandoned field soil

Duration of the conditioning phase affects the results of plant-soil feedback experiments via soil chemical properties

Roles of Arbuscular Mycorrhizal Fungi and Soil Abiotic Conditions in the Establishment of a Dry Grassland Community