Soil-mediated impacts of an invasive thistle inhibit the recruitment of certain native plants
Invasive plants may outcompete and replace native plant species through a variety of mechanisms. Recent evidence indicates that soil microbial pathways such as pathogen accumulation may have a considerable role in facilitating competition between native and invasive plants. To assess microbe-mediated pathways of invasion, we tested the impacts of invaded and non-invaded field soils on plant establishment using naturally occurring populations of the common Eurasian invader Cirsium arvense (Canada thistle) in Southern Ontario, Canada. Linked field and greenhouse experiments were used to quantify differences in the germinability and early growth rates of native plant species, depending on exposure to the microbial community in invaded or non-invaded soils. The invaded microbial community significantly reduced early growth rates for two of the seven native species surveyed, and decreased seed germination for another. In contrast, the germination and growth of invasive Cirsium were not affected by its own soil microbial community. These results demonstrate that the invasion of C. arvense can reduce the performance of some native plant species through changes to the soil microbial community. Different effects on different species suggest that this invader may also change the relative importance of certain natives in the invaded community. If these effects influence plant abundance in the field, microbially mediated interactions in the soil may aid the invasion of C. arvense and facilitate the disruption of invaded communities.
KeywordsBiological invasions Recruitment Seeds Seedlings Soil microbes
This research was supported by a Natural Sciences and Engineering Research Council of Canada Discovery Grant (PMK). We thank K. Nunes for her advice and help in the lab; A. Longley for her help in the field and lab; S. Shukla and R. Matar for their work in the greenhouse and with weighing; S. Schneider and all the KSR staff for ensuring that field experiments ran smoothly; two anonymous reviewers who provided comments to improve the manuscript. This article does not contain any studies with human participants or animals performed by any of the authors.
Author contribution statement
PMK conceived the initial idea, and JDV and PMK designed the experiments. JDV conducted the experiments and analysis of data, and PMK provided guidance. JDV wrote the manuscript, and PMK provided editorial advice.
Compliance with ethical standards
Conflict of interest
The authors declare no conflict of interest.
Upon acceptance of the manuscript, data will be archived in the Dryad Digital Repository.
- Berns AE, Philipp H, Narres HD, Burauel P, Vereecken H, Tappe W (2008) Effect of gamma-sterilization and autoclaving on soil organic matter structure as studied by solid state NMR, UV and fluorescence spectroscopy. Eur J Soil Sci 59:540–550. https://doi.org/10.1111/j.1365-2389.2008.01016.x CrossRefGoogle Scholar
- Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. Br Ecol Soc 85:561–573Google Scholar
- Bever JD, Platt TG, Morton ER (2012) Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Annu Rev Microbiol 66:265–283. https://doi.org/10.1146/annurev-micro-092611-150107 CrossRefGoogle 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. https://doi.org/10.1111/j.1365-2745.2006.01158.x CrossRefGoogle Scholar
- Crawley MJ (2000) Seeds: the ecology of regeneration in plant communities, 2nd edn. CABI International, WallingfordGoogle Scholar
- Dickie IA, Bufford JL, Cobb RC, Desprez-Loustau ML, Grelet G, Hulme PE, Klironomos J, Makiola A, Nuñez MA, Pringle A, Thrall PH, Tourtellot SG, Waller L, Williams NM (2017) The emerging science of linked plant–fungal invasions. New Phytol 215:1314–1332. https://doi.org/10.1111/nph.14657 CrossRefGoogle Scholar
- Dunn AM, Torchin ME, Hatcher MJ, Kotanen PM, Blumenthal DM, Byers JE, Coon CAC, Frankel VM, Holt RD, Hufbauer RA, Kanarek AR, Schierenbeck KA, Wolfe LM, Perkins SE (2012) Indirect effects of parasites in invasions. Funct Ecol 26:1262–1274. https://doi.org/10.1111/j.1365-2435.2012.02041.x CrossRefGoogle Scholar
- Gupta A (2010) Management of fungal plant pathogens. CABI International, OxfordshireGoogle Scholar
- Harper JL (1977) Population biology of plants. Academic Press, LondonGoogle Scholar
- Holm LG, Plucknett DL, Pancho JV, Herberger JP (1977) The world’s worst weeds: distribution and biology. University Press of Hawaii, HonoluluGoogle Scholar
- Packer A, Clay K (2003) Soil pathogens and Prunus serotina seedling and sapling growth near conspecific trees. Ecology 84:108–119. https://doi.org/10.1890/0012-9658(2003)084%5b0108:SPAPSS%5d2.0.CO;2 CrossRefGoogle Scholar
- R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
- Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmanek M (2000) Plant invasions—the role of mutualisms. Biol Rev 75:65–93. https://doi.org/10.1111/j.1469-185X.1999.tb00041.x CrossRefGoogle Scholar
- Schafer M, Kotanen PM (2004) Impacts of naturally-occurring soil fungi on seeds of meadow plants. Plant Ecol 175:19–35. https://doi.org/10.1023/B:VEGE.0000048096.00772.23 CrossRefGoogle Scholar
- 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 4:727–731. https://doi.org/10.1371/journal.pbio.0040140 CrossRefGoogle Scholar
- Torgeson DC (1969) Fungicides: an advanced treatise. Academic Press, New YorkGoogle Scholar
- Wolfe BE, Klironomos JN (2005) Breaking new ground: soil communities and exotic plant invasion. Bioscience 55:477–487. https://doi.org/10.1641/0006-3568(2005)055%5b0477:bngsca%5d2.0.co;2 CrossRefGoogle Scholar