Hostname: page-component-7d684dbfc8-dh8xm Total loading time: 0 Render date: 2023-10-01T00:15:44.270Z Has data issue: false Feature Flags: { "corePageComponentGetUserInfoFromSharedSession": true, "coreDisableEcommerce": false, "coreDisableSocialShare": false, "coreDisableEcommerceForArticlePurchase": false, "coreDisableEcommerceForBookPurchase": false, "coreDisableEcommerceForElementPurchase": false, "coreUseNewShare": true, "useRatesEcommerce": true } hasContentIssue false

Soil–Occupancy Effects of Invasive and Native Grassland Plant Species on Composition and Diversity of Mycorrhizal Associations

Published online by Cambridge University Press:  20 January 2017

Nicholas R. Jordan*
Agronomy and Plant Genetics Department, University of Minnesota, 1991 Buford Circle, St. Paul MN 55108
Laura Aldrich-Wolfe
Biology Department, Concordia College, Moorhead, MN 56562
Sheri C. Huerd
Agronomy and Plant Genetics Department, University of Minnesota, 1991 Buford Circle, St. Paul MN 55108
Diane L. Larson
U.S. Geological Survey, Northern Prairie Wildlife Research Center, 1561 Lindig St., St. Paul, MN 55108
Gary Muehlbauer
Agronomy and Plant Genetics Department, University of Minnesota, 1991 Buford Circle, St. Paul MN 55108
Corresponding author's E-mail:


Diversified grasslands that contain native plant species can produce biofuels, support sustainable grazing systems, and produce other ecosystem services. However, ecosystem service production can be disrupted by invasion of exotic perennial plants, and these plants can have soil-microbial “legacies” that may interfere with establishment and maintenance of diversified grasslands even after effective management of the invasive species. The nature of such legacies is not well understood, but may involve suppression of mutualisms between native species and soil microbes. In this study, we tested the hypotheses that legacy effects of invasive species change colonization rates, diversity, and composition of arbuscular-mycorrhizal fungi (AMF) associated with seedlings of co-occurring invasive and native grassland species. In a glasshouse, experimental soils were conditioned by cultivating three invasive grassland perennials, three native grassland perennials, and a native perennial mixture. Each was grown separately through three cycles of growth, after which we used T-RFLP analysis to characterize AMF associations of seedlings of six native perennial and six invasive perennial species grown in these soils. Legacy effects of soil conditioning by invasive species did not affect AMF richness in seedling roots, but did affect AMF colonization rates and the taxonomic composition of mycorrhizal associations in seedling roots. Moreover, native species were more heavily colonized by AMF and roots of native species had greater AMF richness (number of AMF operational taxonomic units per seedling) than did invasive species. The invasive species used to condition soil in this experiment have been shown to have legacy effects on biomass of native seedlings, reducing their growth in this and a previous similar experiment. Therefore, our results suggest that successful plant invaders can have legacies that affect soil-microbial associations of native plants and that these effects can inhibit growth of native plant species in invaded communities.

Copyright © Weed Science Society of America 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)


Literature Cited

Aldrich-Wolfe, L. 2007. Distinct mycorrhizal communities on new and established hosts in a transitional tropical plant community. Ecology 88:559566.CrossRefGoogle Scholar
Allen, E., Allen, M., Egerton-Warburton, L., Corkidi, L., and Gómez-Pompa, A. 2003. Impacts of early-and late-seral mycorrhizae during restoration in seasonal tropical forest, Mexico. Ecol. Appl. 13:17011717.CrossRefGoogle Scholar
Batten, K., Scow, K., Davies, K., and Harrison, S. 2006. Two invasive plants alter soil microbial community composition in serpentine grasslands. Biol. Invasions 8:217230.CrossRefGoogle Scholar
Best, R. and Arcese, P. 2009. Exotic herbivores directly facilitate the exotic grasses they graze: mechanisms for an unexpected positive feedback between invaders. Oecologia 159:139150.CrossRefGoogle Scholar
Bray, S., Kitajima, K., and Sylvia, D. 2003. Mycorrhizae differentially alter growth, physiology, and competitive ability of an invasive shrub. Ecol. Appl. 13:565574.CrossRefGoogle Scholar
Callaway, R. M., Cipollini, D., Barto, K., Thelen, G. C., Hallett, S. G., Prati, D., Stinson, K., and Klironomos, J. 2008. Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89:10431055.CrossRefGoogle Scholar
Carey, E., Marler, M., and Callaway, R. 2004. Mycorrhizae transfer carbon from a native grass to an invasive weed: evidence from stable isotopes and physiology. Plant Ecol. 172:133141.CrossRefGoogle Scholar
Duda, J., Freeman, D., Emlen, J., Belnap, J., Kitchen, S., Zak, J., Sobek, E., Tracy, M., and Montante, J. 2003. Differences in native soil ecology associated with invasion of the exotic annual chenopod, Halogeton glomeratus. Biol. and Fert. Soils 38:7277.CrossRefGoogle Scholar
Goujon, M., McWilliam, H., Li, W., Valentin, F., Squizzato, S., Paern, J., and Lopez, R. 2010. A new bioinformatics analysis tools framework at EMBL–EBI. Nucleic Acids Res. 38:W695.CrossRefGoogle ScholarPubMed
Great Plains Flora Association. 1986. Flora of the Great Plains. R. L. McGregor and T. M. Barkley, eds. Lawrence, Kansas :. Univ. Pr. of Kansas. 1402 p.Google Scholar
Grman, E. and Suding, K. N. 2010. Within Year Soil Legacies Contribute to Strong Priority Effects of Exotics on Native California Grassland Communities. Restor. Ecol. 18:664670.CrossRefGoogle Scholar
Hallett, S. 2006. Dislocation from coevolved relationships: a unifying theory for plant invasion and naturalization? Weed Sci. 54:282290.CrossRefGoogle Scholar
Hart, M. M. and Reader, R. J. 2002. Host plant benefit from association with arbuscular mycorrhizal fungi: variation due to differences in size of mycelium. Biol. Fert. Soils 36:357366.CrossRefGoogle Scholar
Hartnett, D. and Wilson, G. 2002. The role of mycorrhizas in plant community structure and dynamics: lessons from grasslands. Plant Soil 244:319331.CrossRefGoogle Scholar
Hausmann, N. and Hawkes, C. 2009. Plant neighborhood control of arbuscular mycorrhizal community composition. New Phytol. 183:11881200.CrossRefGoogle Scholar
Hausmann, N. and Hawkes, C. 2010. Order of plant host establishment alters the composition of arbuscular mycorrhizal communities. Ecology 91:23332343.CrossRefGoogle Scholar
Hawkes, C., Belnap, J., D'Antonio, C., and Firestone, M. 2006. Arbuscular mycorrhizal assemblages in native plant roots change in the presence of invasive exotic grasses. Plant Soil 281:369–80.CrossRefGoogle Scholar
Inderjit, , and van der Putten, W. H. 2010. Impacts of soil microbial communities on exotic plant invasions. Trends Ecol. Evol. 25:512519.CrossRefGoogle ScholarPubMed
Jordan, N., Larson, D., and Huerd, S. 2008. Soil modification by invasive plants: effects on native and invasive species of mixed-grass prairies. Biol. Invasions 10:177190.CrossRefGoogle Scholar
Jordan, N. R., Larson, D. L., and Huerd, S. C. 2011. Evidence of Qualitative Differences between Soil-Occupancy Effe.cts of Invasive vs. Native Grassland Plant Species. Invas. Plant Sci. Manage. 4:1121.CrossRefGoogle Scholar
Kivlin, S. N. and Hawkes, C. V. 2011. Differentiating between effects of invasion and diversity: impacts of aboveground plant communities on belowground fungal communities. New Phytol. 189:526535.CrossRefGoogle ScholarPubMed
Kourtev, P., Ehrenfeld, J., and Häggblom, M. 2002. Exotic plant species alter the microbial community structure and function in the soil. Ecology 83:31523166.CrossRefGoogle Scholar
Krüger, M., Stockinger, H., Krüger, C., and Schüßler, A. 2009. DNA-based species level detection of Glomeromycota: one PCR primer set for all arbuscular mycorrhizal fungi. New Phytol. 183:212223.CrossRefGoogle Scholar
Kulmatiski, A. 2006. Exotic plants establish persistent communities. Plant Ecol. 187:261275.CrossRefGoogle Scholar
Larkin, M., Blackshields, G., Brown, N., Chenna, R., McGettigan, P., McWilliam, H., Valentin, F., Wallace, I., Wilm, A., and Lopez, R. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947.CrossRefGoogle Scholar
Lekberg, Y., Koide, R., Rohr, J., Aldrich-Wolfe, L., and Morton, J. 2007. Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. J. Ecol. 95:95105.CrossRefGoogle Scholar
Lockwood, J. and Samuels, C. 2004. Assembly models and restoration practice. Pages 5570 in Temperton, V. M., Hobbs, R. J., Nuttle, T., and Hale, S., eds. Assembly rules and restoration ecology. Island Press, Washington, USA.Google Scholar
Lombardo, K., Fehmi, J., Rice, K., and Laca, E. 2007. Nassella pulchra survival and water relations depend more on site productivity than on small scale disturbance. Restor. Ecol. 15:177178.CrossRefGoogle Scholar
McCune, B. and Mefford, M. J. 2006. PC-Ord for Windows v. 5.15. Multivariate analysis of ecological data. MjM Software, Gleneden Beach, Oregon, USA.Google Scholar
McGonigle, T., Miller, M., Evans, D., Fairchild, G., and Swan, J. 1990. A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. New Phytol. 115:495501.CrossRefGoogle Scholar
Mummey, D. and Rillig, M. 2006. The invasive plant species Centaurea maculosa alters arbuscular mycorrhizal fungal communities in the field. Plant Soil 288:8190.CrossRefGoogle Scholar
Mummey, D., Rillig, M., and Holben, W. 2005. Neighboring plant influences on arbuscular mycorrhizal fungal community composition as assessed by T-RFLP analysis. Plant Soil 271:8390.CrossRefGoogle Scholar
Noyd, R., Pfleger, F., and Russelle, M. 1995. Interactions between native prairie grasses and indigenous arbuscular mycorrhizal fungi: implications for reclamation of taconite iron ore tailing. New Phytol. 129:651660.CrossRefGoogle Scholar
Ortega, Y. and Pearson, D. 2005. Weak vs. strong invaders of natural plant communities: assessing invasibility and impact. Ecol. Appl. 15:651661.CrossRefGoogle Scholar
Peltzer, D., Bellingham, P., Kurokawa, H., Walker, L., Wardle, D., and Yeates, G. 2009. Punching above their weight: low biomass non native plant species alter soil properties during primary succession. Oikos 118:10011014.CrossRefGoogle Scholar
Perry, D. A. 1995. Self-Organizing Systems Across Scales. Trends in Ecology & Evolution 10:241244.CrossRefGoogle Scholar
Pringle, A., Bever, J., Gardes, M., Parrent, J., Rillig, M., and Klironomos, J. 2009. Mycorrhizal symbioses and plant invasions. Annu. Rev. Ecol. Evol. Syst. 40:699715.CrossRefGoogle Scholar
Raizada, P., Raghubanshi, A., and Singh, J. 2008. Impact of invasive alien plant species on soil processes: a review. P. Nat A. Sci. India B 78:288298.Google Scholar
Reinhart, K. and Callaway, R. 2006. Soil biota and invasive plants. New Phytol. 170:445457.CrossRefGoogle ScholarPubMed
Renker, C., Heinrichs, J., Kaldorf, M., and Buscot, F. 2003. Combining nested PCR and restriction digest of the internal transcribed spacer region to characterize arbuscular mycorrhizal fungi on roots from the field. Mycorrhiza 13:191198.Google ScholarPubMed
Richardson, D., Allsopp, N., D'Antonio, C., Milton, S., and Rejmanek, M. 2000. Plant invasions–the role of mutualisms. Biol. Rev. 75:6593.CrossRefGoogle ScholarPubMed
Rout, M. and Callaway, R. 2009. An invasive plant paradox. Science 324:734.CrossRefGoogle ScholarPubMed
SAS Institute. 2009. JMP release 8 : Statistics and graphics guide. 2nd edition. Cary, NC : SAS Institute. 146 p.Google Scholar
Seifert, E., Bever, J., and Maron, J. 2009. Evidence for the evolution of reduced mycorrhizal dependence during plant invasion. Ecology 90:10551062.CrossRefGoogle ScholarPubMed
Shah, M. A., Reshi, Z. A., and Rasool, N. 2010. Plant invasions induce a shift in Glomalean spore diversity. Trop. Ecol. 51:317323.Google Scholar
Standish, R., Cramer, V., and Hobbs, R. 2008. Land-use legacy and the persistence of invasive Avena barbata on abandoned farmland. J. Appl. Ecol. 45:15761583.CrossRefGoogle Scholar
Stinson, K., Campbell, S., Powell, J., Wolfe, B., Callaway, R., Thelen, G., Hallett, S., Prati, D., and Klironomos, J. 2006. Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. Plos Biol. 4:727.CrossRefGoogle Scholar
Suding, K., Gross, K., and Houseman, G. 2004. Alternative states and positive feedbacks in restoration ecology. Trends Ecol. Evol. 19:4653.CrossRefGoogle ScholarPubMed
van der Heijden, M. 2004. Arbuscular mycorrhizal fungi as support systems for seedling establishment in grassland. Ecol. Lett. 7:293303.CrossRefGoogle Scholar
van der Putten, W., Klironomos, J., and Wardle, D. 2007. Microbial ecology of biological invasions. ISME J. 1:2837.CrossRefGoogle Scholar
Vatovec, C., Jordan, N., and Huerd, S. 2005. Responsiveness of certain agronomic weed species to arbuscular mycorrhizal fungi. Renew. Agr. Food Sys. 20:181189.CrossRefGoogle Scholar
Verbruggen, E. and Kiers, T. 2010. Evolutionary ecology of mycorrhizal functional diversity in agricultural systems. Evol. Appl., 3 5:547560.CrossRefGoogle Scholar
Vogelsang, K. and Bever, J. 2009. Mycorrhizal densities decline in association with nonnative plants and contribute to plant invasion. Ecology 90:399407.CrossRefGoogle ScholarPubMed
Walling, S. Z. and Zabinski, C. A. 2004. Host plant differences in arbuscular mycorrhizae: Extra radical hyphae differences between an invasive forb and a native bunchgrass. Plant Soil 265:335344.CrossRefGoogle Scholar
White, T., Bruns, T., Lee, S., and Taylor, J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Pages 315322 in Innes, M. A., Gelfand, D. H., Sninsky, J. J., and White, T. J., eds. PCR protocols a guide to methods and applications.Google Scholar
Wilson, G. and Hartnett, D. 1998. Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. Amer. J. Bot. 85:1732.CrossRefGoogle ScholarPubMed
Wolfe, B. and Klironomos, J. 2005. Breaking new ground: soil communities and exotic plant invasion. BioScience 55:477487.CrossRefGoogle Scholar
Zhang, Q., Yang, R. Y., Tang, J. J., Yang, H. S., Hu, S. J., and Chen, X. 2010. Positive Feedback between Mycorrhizal Fungi and Plants Influences Plant Invasion Success and Resistance to Invasion. PLoS One 5.Google ScholarPubMed