Hostname: page-component-594f858ff7-pr6g6 Total loading time: 0 Render date: 2023-06-07T00:37:49.131Z Has data issue: false Feature Flags: { "corePageComponentGetUserInfoFromSharedSession": false, "coreDisableEcommerce": false, "corePageComponentUseShareaholicInsteadOfAddThis": true, "coreDisableSocialShare": false, "useRatesEcommerce": true } hasContentIssue false

Evidence of Qualitative Differences between Soil-Occupancy Effects of Invasive vs. Native Grassland Plant Species

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
Diane L. Larson
U.S. Geological Survey, Northern Prairie Wildlife Research Center, 1561 Lindig St., St. Paul, MN 55108
Sheri C. Huerd
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 are being recognized as important elements of agricultural landscapes and for production of biofuel feedstocks as well as a variety of other ecosystem services. Unfortunately, establishment of such grasslands is often difficult, unpredictable, and highly vulnerable to interference and invasion by weeds. Evidence suggests that soil-microbial “legacies” of invasive perennial species can inhibit growth of native grassland species. However, previous assessments of legacy effects of soil occupancy by invasive species that invade grasslands have focused on single invasive species and on responses to invasive soil occupancy in only a few species. In this study, we tested the hypothesis that legacy effects of invasive species differ qualitatively from those of native grassland species. In a glasshouse, three invasive and three native grassland perennials and a native perennial mixture were grown separately through three cycles of growth and soil conditioning in soils with and without arbuscular mycorrhizal fungi (AMF), after which we assessed seedling growth in these soils. Native species differed categorically from invasives in their response to soil conditioning by native or invasive species, but these differences depended on the presence of AMF. When AMF were present, native species largely had facilitative effects on invasive species, relative to effects of invasives on other invasives. Invasive species did not facilitate native growth; neutral effects were predominant, but strong soil-mediated inhibitory effects on certain native species occurred. Our results support the hypothesis that successful plant invaders create biological legacies in soil that inhibit native growth, but suggest also this mechanism of invasion will have nuanced effects on community dynamics, as some natives may be unaffected by such legacies. Such native species may be valuable as nurse plants that provide cost-effective restoration of soil conditions needed for efficient establishment of diversified grasslands.

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. B., Allen, M. E., Egerton-Warburton, L., Corkidi, L., and Gomez-Pompa, A. 2003. Impacts of early- and late-seral mycorrhizae during restoration in seasonal tropical forest, Mexico. Ecol. Appl 13:17011717.CrossRefGoogle Scholar
Azcon-Aguilar, C., Palenzuela, J., Roldan, A., Bautista, S., Vallejo, R., and Barea, J. M. 2003. Analysis of the mycorrhizal potential in the rhizosphere of representative plant species from desertification-threatened mediterranean shrublands. Appl. Soil Ecol 22:2937.CrossRefGoogle Scholar
Barni, E. and Siniscalco, C. 2000. Vegetation dynamics and arbuscular mycorrhiza in old-field successions of the western Italian Alps. Mycorrhiza 10:6372.CrossRefGoogle Scholar
Batten, K. M., Scow, K. M., and Espeland, E. K. 2008. Soil microbial community associated with an invasive grass differentially impacts native plant performance. Microb. Ecol 55:220228.CrossRefGoogle ScholarPubMed
Belyea, L. 2004. Beyond ecological filters: feedback networks in the assembly and restoration of community structure. Pages 115132. In Temperton, V., Hobbs, R., Halle, S., and Nuttle, T. eds. Assembly Rules and Restoration Ecology: Bridging the Gap between Theory and Practice. Washington, DC Island Press.Google Scholar
Bertness, M. D. and Callaway, R. 1994. Positive interactions in communities. Trends Ecol. Evol 9:191193.CrossRefGoogle ScholarPubMed
Best, R. J. 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 ScholarPubMed
Bezemer, T. M., Graca, O., Rousseau, P., and van der Putten, W. H. 2004. Above- and belowground trophic interactions on creeping thistle (Cirsium arvense) in high- and low-diversity plant communities: potential for biotic resistance? Plant Biol 6:231238.CrossRefGoogle Scholar
Blumenthal, D. M., Jordan, N. R., and Svenson, E. L. 2005. Effects of prairie restoration on weed invasions. Agric. Ecosyst. Environ 107:221230.CrossRefGoogle Scholar
Bray, S. R., Kitajima, K., and Sylvia, D. M. 2003. Mycorrhizae differentially alter growth, physiology, and competitive ability of an invasive shrub. Ecol. Appl 13:565574.CrossRefGoogle Scholar
Burrows, R. L. and Pfleger, F. L. 2002. Arbuscular mycorrhizal fungi respond to increasing plant diversity. Can. J. Bot 80:120130.CrossRefGoogle Scholar
Callaway, R. 1997. Positive interactions in plant communities and the individualistic-continuum concept. Oecologia 112:143149.CrossRefGoogle ScholarPubMed
Callaway, R. M., Mahall, B. E., Wicks, C., Pankey, J., and Zabinski, C. 2003. Soil fungi and the effects of an invasive forb on grasses: neighbor identity matters. Ecology 84:129135.CrossRefGoogle Scholar
Carey, E. V., Marler, M. J., and Callaway, R. M. 2004. Mycorrhizae transfer carbon from a native grass to an invasive weed: evidence from stable isotopes and physiology. Plant Ecol 172:133141.CrossRefGoogle Scholar
Corbin, J. D. and D'Antonio, C. M. 2004. Effects of exotic species on soil nitrogen cycling: implications for restoration. Weed Technol 18:14641467.CrossRefGoogle Scholar
Day, P. R. 1965. Particle fractionation and particle size analysis. Pages 545567. In Black, C. ed. Methods of Soil Analysis. Part 1. Madison, WI American Society of Agronomy and Soil Science Society of America.Google Scholar
Duda, J. J., Freeman, D. C., Emlen, J. M., Belnap, J., Kitchen, S. G., Zak, J. C., Sobek, E., Tracy, M., and Montante, J. 2003. Differences in native soil ecology associated with invasion of the exotic annual chenopod, Halogeton glomeratus . Biol. Fertil. Soils 38:7277.CrossRefGoogle Scholar
Ehrenfeld, J. G. 2003. Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503523.CrossRefGoogle Scholar
Enkhtuya, B., Poschl, M., and Vosatka, M. 2005. Native grass facilitates mycorrhizal colonisation and P uptake of tree seedlings in two anthropogenic substrates. Water Air Soil Pollut 166:217236.CrossRefGoogle Scholar
Grace, C. and Stribley, D. 1999. A safer procedure for routine staining of vesicular-arbuscular mycorrhizal fungi. Mycol. Res 95:11601162.CrossRefGoogle Scholar
Great Plains Flora Association 1986. Flora of the Great Plains. Pages 1400 p.Google Scholar
Hallett, S. G. 2006. Dislocation from coevolved relationships: a unifying theory for plant invasion and naturalization? Weed Sci 54:282290.CrossRefGoogle Scholar
Hartnett, D. C. and Wilson, G. W. T. 2002. The role of mycorrhizas in plant community structure and dynamics: lessons from grasslands. Plant Soil 244:319331.CrossRefGoogle Scholar
Haubensak, K. A., D'Antonio, C. M., and Alexander, J. 2004. Effects of nitrogen-fixing shrubs in Washington and coastal California. Weed Technol 18:14751479.CrossRefGoogle Scholar
Hawkes, C. V., Belnap, J., D'Antonio, C., and Firestone, M. K. 2006. Arbuscular mycorrhizal assemblages in native plant roots change in the presence of invasive exotic grasses. Plant Soil 281:2369.CrossRefGoogle Scholar
Hawkes, C. V., Wren, I. F., Herman, J. D., and Firestone, M. K. 2005. Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol. Lett 8:976985.CrossRefGoogle Scholar
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., Zhang, J., and Huerd, S. 2000. Arbuscular-mycorrhizal fungi: potential roles in weed management. Weed Res 40:397410.CrossRefGoogle Scholar
Klironomos, J. N. 2002. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:6770.CrossRefGoogle ScholarPubMed
Koide, R. T. and Li, M. G. 1989. Appropriate controls for vesicular arbuscular mycorrhiza research. New Phytol 111:3544.CrossRefGoogle Scholar
Kourtev, P. S., Ehrenfeld, J. G., and Haggblom, M. 2002. Exotic plant species alter the microbial community structure and function in the soil. Ecology 83:31523166.CrossRefGoogle Scholar
Kulmatiski, A. 2006. Exotic plants establish persistent communities. Plant Ecol 187 (2):261275.CrossRefGoogle Scholar
Kulmatiski, A., Beard, K. H., Stevens, J. R., and Cobbold, S. M. 2008. Plant–soil feedbacks: a meta-analytical review. Ecol. Lett 9:980992.CrossRefGoogle Scholar
Larson, J. L. and Siemann, E. 1998. Legumes may be symbiot limited during old field succession. Am. Midl. Nat 140:9095.CrossRefGoogle Scholar
Lockwood, J. L. and Samuels, C. L. 2004. Assembly models and restoration practice. Pages 5570. In Temperton, V., Hobbs, R., Halle, S., and Nuttle, T. eds. Assembly Rules and Restoration Ecology: Bridging the Gap between Theory and Practice. Washington DC Island Press.Google Scholar
Lombardo, K., Fehmi, J. S., Rice, K. J., 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
Lortie, C. J., Brooker, R. W., Choler, P., Kikvidze, Z., Michalet, R., Pugnaire, F. I., and Callaway, R. M. 2004. Rethinking plant community theory. Oikos 107:433438.CrossRefGoogle Scholar
Mangla, S., Inderjit, , and Callaway, R. M. 2008. Exotic invasive plant accumulates native soil pathogens which inhibit native plants. J. Ecol 96:5867.Google Scholar
McGonigle, T. P., Miller, M. H., Evans, D. G., Fairchild, G. L., and Swan, J. A. 1990. A new method which gives an objective measure of colonization of roots by vesicular- arbuscular mycorrhizal fungi. New Phytol 115:494501.CrossRefGoogle Scholar
Niu, H-B., Liu, W-X., Wan, F-H., and Wan, B. L. 2007. An invasive aster (Ageratina adenophora) invades and dominates forest understories in China: altered soil microbial communities facilitate the invader and inhibit natives. Plant Soil 294:7385.CrossRefGoogle Scholar
Noyd, R. K., Pfleger, F. L., and Russelle, M. P. 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
Oba, H., Shinozaki, N., Oyaizu, H., Tawaraya, K., Wagatsuma, T., Barraquio, W. L., and Saito, M. 2004. Arbuscular mycorrhizal fungal communities associated with some pioneer plants in the lahar area of Mt. Pinatubo, Philippines. Soil Sci. Plant Nutr 50:11951203.CrossRefGoogle Scholar
Ortega, Y. K. and Pearson, D. E. 2005. Weak vs. strong invaders of natural plant communities: assessing invasibility and impact. Ecol. Appl 15:651661.CrossRefGoogle Scholar
Padilla, F. M. and Pugnaire, F. I. 2006. The role of nurse plants in the restoration of degraded environments. Front. Ecol. Environ 4:196202.CrossRefGoogle Scholar
Peltzer, D. A., Bellingham, P. J., Kurokawa, H., Walker, L. R., Wardle, D. A., and Yeates, G. W. 2009. Punching above their weight: low-biomass non-native plant species alter soil properties during primary sucession. Oikos 118:10011014.CrossRefGoogle Scholar
Petermann, J. S., Fergus, A. J. F., Turnbull, L. A., and Schmid, B. 2008. Janzen–Connell effects are widespread and strong enough to maintain diversity in grasslands. Ecology 89:23992406.CrossRefGoogle ScholarPubMed
Raizada, P., Raghubanshi, A. S., and Singh, J. S. 2008. Impact of invasive alien plant species on soil processes: a review. Proc. Natl. Acad. Sci. India Sect. B (Biol. Sci.) 78:288298.Google Scholar
Reinhart, K. O. and Callaway, R. M. 2006. Soil biota and invasive plants. New Phytol 170:445457.CrossRefGoogle ScholarPubMed
Reynolds, H. L. and Haubensak, K. A. 2009. Soil fertility, heterogeneity, and microbes: towards an integrated understanding of grassland structure and dynamics. Appl. Veg. Sci 12:3344.CrossRefGoogle Scholar
Richardson, D. M., Allsop, N., D'Antonio, C. M., Milton, S. J., and Rejmanek, M. 2000. Plant invasions—the role of mutualisms. Biol. Rev 75:6593.CrossRefGoogle ScholarPubMed
Robertson, G. P., Coleman, D. C., Bledsoe, C. S., and Sollins, P. eds. 1999. Standard Soil Methods for Long-Term Ecological Research. Long-Term Ecological Research Network Series. New York, NY Oxford University Press.Google Scholar
Rout, M. E. and Callaway, R. M. 2009. An invasive plant paradox. Science 324:734735.CrossRefGoogle ScholarPubMed
Rowe, H. I. and Brown, C. S. 2008. Native plant growth and seedling establishment in soils influenced by Bromus tectorum . Rangeland Ecol. Manag 61:630639.CrossRefGoogle Scholar
Saggar, S., McIntosh, P., Hedley, C., and Knicker, H. 1999. Changes in soil microbial biomass, metabolic quotient and organic matter turnover under Hieracium pilosella L. Biol. Fertil. Soils 30:232238.CrossRefGoogle Scholar
Seifert, E. K., Bever, J. D., and Maron, J. L. 2009. Evidence for the evolution of reduced mycorrhizal dependence during plant invasion. Ecology 90:10551062.CrossRefGoogle ScholarPubMed
Smith, R. S., Shiel, R. S., Bardgett, R. D., Millward, D., Corkhill, P., Rolph, G., Hobbs, P. J., and Peacock, S. 2003. Soil microbial community, fertility, vegetation and diversity as targets in the restoration management of a meadow grassland. J. Appl. Ecol 40:5164.CrossRefGoogle Scholar
Smith, W. E. and Read, D. J. 1997. Mycorrhizal Symbiosis. 2nd ed. San Diego, CA Academic. ix+ 605 p.Google ScholarPubMed
Sperry, L. J., Belnap, J., and Evans, R. D. 2006. Bromus tectorum invasion alters nitrogen dynamics in an undisturbed arid grassland ecosystem. Ecology 87:603615.CrossRefGoogle Scholar
Standish, R. J., Cramer, V. A., and Hobbs, R. J. 2008. Land-use legacy and the persistence of invasive Avena barbata on abandoned farmland. J. Appl. Ecol 45:15761583.CrossRefGoogle Scholar
Stinson, K. A., Campbell, S. A., Powell, J. R., Wolfe, B. E., Callaway, R. M., Thelen, G. C., Hallett, S. G., Prati, D., and Klironomos, J. N. 2006. Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4:727731.CrossRefGoogle ScholarPubMed
Suding, K. N., Gross, K. L., and Houseman, G. R. 2004. Alternative states and positive feedbacks in restoration ecology. Trends Ecol. Evol 19:4653.CrossRefGoogle ScholarPubMed
Thorpe, A. S., Thelen, G. C., Diaconu, A., and Callaway, R. M. 2009. Root exudate is allelopathic in invaded community but not in native community: field evidence for the novel weapons hypothesis. J. Ecol 97:641645.CrossRefGoogle Scholar
Tilman, D., Hill, J., and Lehman, C. 2006a. Carbon-negative biofuels from low-input high-diversity grassland biomass. Science 314:15981600.CrossRefGoogle ScholarPubMed
Tilman, D., Reich, P. B., and Knops, J. M. H. 2006b. Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441:629632.CrossRefGoogle Scholar
van der Putten, W. H., Bardgett, R. D., de Ruiter, P. C., Hol, W. H. G., Meyer, K. M., Bezemer, T. M., Bradford, M. A., Christensen, S., Eppinga, M. B., Fukami, T., Hemerik, L., Molofsky, J., Schadler, M., Scherber, C., Strauss, S. Y., Vos, M., and Wardle, D. A. 2009. Empirical and theoretical challenges in aboveground–belowground ecology. Oecologia 161:114.CrossRefGoogle ScholarPubMed
Van Grunsven, R. H. A., van der Putten, W. H., Bezemer, T. M., Tamis, W. L. M., Berendse, F., and Veenendaal, E. M. 2007. Reduced plant–soil feedback of plant species expanding their range as compared to natives. J. Ecol 95:10501057.CrossRefGoogle Scholar
Vogelsang, K. M. and Bever, J. D. 2009. Mycorrhizal densities decline in association with nonnative plants and contribute to plant invasion. Ecology 90:399407.CrossRefGoogle ScholarPubMed
Wilson, G. W. T. and Hartnett, D. C. 1998. Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. Am. J. Bot 85:17321738.CrossRefGoogle Scholar
Wolfe, B. E. and Klironomos, J. N. 2005. Breaking new ground: soil communities and exotic plant invasion. Bioscience 55:477487.CrossRefGoogle Scholar
Yu, X. J., Yu, D., Lu, Z. J., and Ma, K. P. 2005. A new mechanism of invader success: exotic plant inhibits natural vegetation restoration by changing soil microbe community. Chin. Sci. Bull 50:11051112.CrossRefGoogle Scholar