Abstract
Invasive plants can have strong impacts on native communities, which have prompted intense efforts at invasive removal. However, relatively little is known about how native communities will reassemble after a dominant invader has been removed from the system. Legacy effects of invasive plants on soil microbial communities may alter native plant community reassembly long after the invader is gone. Here we found that arbuscular mycorrhizal fungal (AMF) communities have shown some recovery in experimental plots following 6 years of removal of the invasive Alliaria petiolata (garlic mustard, a species known to degrade AMF communities) in terms of taxonomic richness and community composition. However, despite this recovery, the density of A. petiolata at the beginning of the experiment (in 2004) still correlated with lower AMF richness and altered community composition after 6 years of annual weeding, suggesting long-term legacies of dense A. petiolata infestations. Because native plant and mycorrhizal fungal communities may show interdependence, reassembly of one community may be limited by the reassembly of the other. Restoration may be more effective if practices address both communities simultaneously.
Similar content being viewed by others
References
Anderson RC, Dhillion SS, Kelley TM (1996). Aspects of the ecology of an invasive plant, garlic mustard (Alliaria petiolata), in central Illinois. Restor Ecol 4:181–191
Anderson RC, Anderson MR, Bauer JT, Slater M, Herold J, Baumhardt P, Borowicz V (2010) Effect of removal of garlic mustard (Alliaria petiolata, Brassicaceae) on arbuscular mycorrhizal fungi inoculum potential in forest soils. Open Ecol J 3:41–47
Anderson RC, Anderson MR, Bauer JT et al (2012) Garlic mustard’s (Alliaria petiolata)effectiveness as an invader of Eastern North American deciduous forest groundlayers. Abstracts, ESA 97th meeting, Portland Oregon. http://esameetings.allenpress.com/2012/webprogram/Paper38382.html
Barto EK, Cipollini D (2009) Half-lives and field soil concentrations of Alliaria petiolata secondary metabolites. Chemosphere 76(1):71–75
Barto EK, Antunes PM, Stinson K, Koch AM, Klironomos JN, Cipollini D (2011) Differences in arbuscular mycorrhizal fungal communities associated with sugar maple seedlings in and outside of invaded garlic mustard forest patches. Biol Invasions 13(12):2755–2762. doi:10.1007/s10530-011-9945-6
Batten KM, Scow KM, Espeland EK (2008) Soil microbial community associated with an invasive grass differentially impacts native plant performance. Microb Ecol 55(2):220–228. doi:10.1007/s00248-007-9269-3
Bauer JT, Anderson RC, Anderson MR (2010) Competitive interactions among first-year and second-year plants of the invasive, biennial garlic mustard (Alliaria petiolata) and native ground layer vegetation. Restor Ecol 18(5):720–728
Cade BS, Noon BR (2003) A gentle introduction to quantile regression for ecologists. Front Ecol Environ 1(8):412–420. doi:10.2307/3868138
Callaway RM, Ridenour WM (2004) Novel weapons: a biochemically based hypothesis for invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443
Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasion. Nature 427(6976):731–733. doi:10.1038/nature02322
Callaway RM, Cipollini D, Barto K, Thelen GC, Hallett SG, Prati D, Stinson K, Klironomos J (2008) Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89(4):1043–1055
Cantor A, Hale A, Aaron J, Traw MB, Kalisz S (2011) Low allelochemical concentrations detected in garlic mustard-invaded forest soils inhibit fungal growth and AMF spore germination. Biol Invasions 13(12):3015–3025. doi:10.1007/s10530-011-9986-x
Catford JA, Jansson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15:22–40
Davison J, Opik M, Daniell TJ, Moora M, Zobel M (2011) Arbuscular mycorrhizal fungal communities in plant roots are not random assemblages. FEMS Microbiol Ecol 78(1):103–115. doi:10.1111/j.1574-6941.2011.01103.x
Dickie IA, FitzJohn RG (2007) Using terminal restriction fragment length polymorphism (T-RFLP) to identify mycorrhizal fungi: a methods review. Mycorrhiza 17(4):259–270. doi:10.1007/s00572-007-0129-2
Fitzjohn RG, Dickie IA (2007) TRAMPR: an R package for analysis and matching of terminal-restriction fragment length polymorphism (TRFLP) profiles. Mol Ecol Notes 7(4):583–587. doi:10.1111/j.1471-8286.2007.01744.x
Grove S, Haubensak KA, Parker IM (2012) Direct and indirect effects of allelopathy in the soil legacy of an exotic plant invasion. Plant Ecol 213(12):1869–1882. doi:10.1007/s11258-012-0079-4
Hallett SG (2006) Dislocation from coevolved relationships: a unifying theory for plant invasion and naturalization? Weed Sci 54(2):282–290
Herold J, Anderson MR, Bauer JT, Borowicz V, Anderson RC (2011) Comparison of the effect of early and late removal of second-year garlic mustard (Alliaria petiolata) on first-year plants and deciduous forest spring and summer dominant herbaceous groundlayer species in central Illinois, USA. Ecol Restor 29:225–233
Kardol P, Cornips NJ, van Kempen MML, Bakx-Schotman JMT, van der Putten WH (2007) Microbe-mediated plant–soil feedback causes historical contingency effects in plant community assembly. Ecol Monogr 77(2):147–162
Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417(6884):67–70
Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84(9):2292–2301
Kulmatiski A, Beard KH (2011) Long-term plant growth legacies overwhelm short-term plant growth effects on soil microbial community structure. Soil Biol Biochem 43(4):823–830. doi:10.1016/j.soilbio.2010.12.018
Kulmatiski A, Beard KH, Stark JM (2006) Soil history as a primary control on plant invasion in abandoned agricultural fields. J Appl Ecol 43(5):868–876. doi:10.1111/j.1365-2664.2006.01192.x
Lankau RA (2012) Interpopulation variation in allelopathic traits informs restoration of invaded landscapes. Evol Appl 5(3):270–282
Lankau RA, Nodurft RN (2013) An exotic invader drives the evolution of plant traits that determine mycorrhizal fungal diversity in a native competitor. Mol Ecol 22(21):5472–5485. doi:10.1111/mec.12484
Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65(2):339–349. doi:10.1111/j.1574-6941.2008.00531.x
Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316(5832):1746–1748. doi:10.1126/science.1143082
Marchante E, Kjoller A, Struwe S, Freitas H (2009) Soil recovery after removal of the N-2-fixing invasive Acacia longifolia: consequences for ecosystem restoration. Biol Invasions 11(4):813–823. doi:10.1007/s10530-008-9295-1
Middleton EL, Bever JD (2012) Inoculation with a native soil community advances succession in a grassland restoration. Restor Ecol 20(2):218–226. doi:10.1111/j.1526-100X.2010.00752.x
Oksanen J, Kindt R, O’HAre RB (2005) vegan:Community Ecology Package version 1.6-10
Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, Reier U, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188(1):223–241. doi:10.1111/j.1469-8137.2010.03334.x
Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN (2009) Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol Syst 40:699–715. doi:10.1146/annurev.ecolsys.39.110707.173454
Roberts KJ, Anderson RC (2001) Effect of garlic mustard [Alliaria petiolata (Beib. Cavara & Grande)] extracts on plants and arbuscular mycorrhizal (AM) fungi. Am Midl Nat 146(1):146–152
Rodgers VL, Stinson KA, Finzi AC (2008) Ready or not, garlic mustard is moving in: Alliaria petiolata as a member of eastern North American forests. Bioscience 58(5):426–436. doi:10.1641/b580510
Simberloff D (2009) We can eliminate invasions or live with them. Successful management projects. Biol Invasions 11(1):149–157. doi:10.1007/s10530-008-9317-z
Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, London
Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM, Thelen GC, Hallett SG, Prati D, Klironomos JN (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4(5):727–731. doi:10.1371/journal.pbio.0040140
van der Putten WH, Klironomos JN, Wardle DA (2007) Microbial ecology of biological invasions. ISME J 1(1):28–37. doi:10.1038/ismej.2007.9
van Grunsven RHA, van der Putten WH, Bezemer TM, Berendse F, Veenendaal EM (2010) Plant–soil interactions in the expansion and native range of a poleward shifting plant species. Glob Chang Biol 16(1):380–385. doi:10.1111/j.1365-2486.2009.01996.x
Wolfe BE, Klironomos JN (2005) Breaking new ground: soil communities and exotic plant invasion. Bioscience 55(6):477–487
Acknowledgments
We thank Rachel Nodurft for assistance with the molecular characterization of AMF communities, and the ParkLands Foundation for allowing us to conduct this study on the Merwin Preserve. This work was funded by NSF DEB Grant 0918450 to RAL.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lankau, R.A., Bauer, J.T., Anderson, M.R. et al. Long-term legacies and partial recovery of mycorrhizal communities after invasive plant removal. Biol Invasions 16, 1979–1990 (2014). https://doi.org/10.1007/s10530-014-0642-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-014-0642-0