Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-14T06:02:07.088Z Has data issue: false hasContentIssue false
  • English
  • Français

A Powdery Mildew Fungus Levels the Playing Field for Garlic Mustard (Alliaria petiolata) and a North American Native Plant

Published online by Cambridge University Press:  20 January 2017

Don Cipollini  and
Stephanie Enright
Don Cipollini*
Affiliation:
Wright State University, Department of Biological Sciences, 3640 Colonel Glenn Highway, Dayton, OH 45435
Stephanie Enright
Affiliation:
Wright State University, Department of Biological Sciences, 3640 Colonel Glenn Highway, Dayton, OH 45435
*
Corresponding author's E-mail: don.cipollini@wright.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

When exposed to native or introduced herbivores and pathogens, invasive plants may become weaker competitors with more benign impacts on individual plants and plant communities. In a greenhouse pot study, we tested whether the presence of powdery mildew disease caused by Erysiphe cruciferarum could alter the competitive impact of garlic mustard on Impatiens pallida, a North American native understory plant. Target I. pallida plants were grown alone or with one, two, or three garlic mustard neighbors. Half of the pots exposed to garlic mustard were inoculated with conidia of E. cruciferarum. Competition with garlic mustard moderately affected aboveground growth of I. pallida, particularly at high garlic mustard density, but it strongly reduced seed output across all densities. In contrast, inoculation of garlic mustard plants with E. cruciferarum completely abolished their competitive impact on seed output of I. pallida across all densities, independent of effects on aboveground growth of target plants. This effect was likely due to alteration in the ability of garlic mustard to compete for belowground resources. Even without killing garlic mustard, these results indicate that the presence of powdery mildew disease in the field will likely dampen the competitive impact of garlic mustard on individual plants and plant communities. Escape from such attackers has likely contributed to the invasiveness and impacts of garlic mustard in North America.

Keywords

Powdery mildew, Erysiphe cruciferarum Opiz ex. L. Junellgarlic mustard, Alliaria petiolata (Bieb.) Cavara & Grandepale jewelweed, Impatiens pallida Nutt.Competitionenemy releaseinvasive speciesplant-pathogen interactions
Type
Research
Information
Invasive Plant Science and Management , Volume 2 , Issue 3 , July 2009 , pp. 253 - 259
Copyright
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.)

References

Literature Cited

Blossey, B. and Nötzold, R. 1995. Evolution of increased competitive ability in invasive non-indigenous plants: a hypothesis. J. Ecol 83:887–889.CrossRefGoogle Scholar
Blossey, B., Nuzzo, V., Hinz, H., and Gerber, E. 2001. Developing biological control of Alliaria petiolata (M. Bieb.) Cavara and Grande (garlic mustard). Nat. Areas J 21:357–367.Google Scholar
Bossdorf, O., Prati, D., Auge, H., and Schmid, B. 2004. Reduced competitive ability in an invasive plant. Ecol. Lett 7:346–353.Google Scholar
Brooks, D. H. 1972. Observations of the effects of mildew, Erysiphe graminis, on growth of spring and winter barley. Ann. Appl. Bot 70:149–156.Google Scholar
Callaway, R. M., Cipollini, D., Barto, E. 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 89:1043–1055.CrossRefGoogle Scholar
Callaway, R. M. and Ridenour, W. M. 2004. Novel weapons: invasive success and the evolution of increased competitive ability. Front. Ecol. Environ 2:436–444.Google Scholar
Carlson, A. M. 2002. Effects of Herbicide on Alliaria petiolata (Garlic Mustard) and Subsequent Effects on Native Plants in the Old-Growth and Second-Growth Forests of a Southwestern Ohio Nature Preserve. Masters thesis. Oxford, OH Miami University.Google Scholar
Carlson, A. M. and Gorchov, D. L. 2004. Effects of herbicide on the invasive biennial Alliaria petiolata (garlic mustard) and initial responses of native plants in a southwestern Ohio forest. Restor. Ecol 12:559–567.CrossRefGoogle Scholar
Carpenter, D. and Cappuccino, N. 2005. Herbivory, time since introduction and the invasiveness of exotic plants. J. Ecol 93:315–321.Google Scholar
Cipollini, D. and Gruner, B. 2007. Cyanide in the chemical arsenal of garlic mustard, Alliaria petiolata . J. Chem. Ecol 33:85–94.Google Scholar
Cipollini, D., Mbagwu, J., Hillstrom, C., Barto, E. K., and Enright, S. 2005. Expression of constitutive and inducible chemical defenses in native and invasive populations of Alliaria petiolata . J. Chem. Ecol 31:1243–1255.Google Scholar
Cipollini, K. A., McClain, G. Y., and Cipollini, D. 2008. Separating effects of allelopathy and shading by Alliaria petiolata and Lonicera maackii on growth, reproduction and survival of Impatiens capensis . Am. Midl. Nat 160:117–128.Google Scholar
Davis, A. S., Landis, D. A., Nuzzo, V., Blossey, B., Gerber, E., and Hinz, H. L. 2006. Demographic models inform selection of biocontrol agents for garlic mustard (Alliaria petiolata). Ecol. Appl 16:2399–2410.Google Scholar
Durka, W., Bossdorf, O., Prati, D., and Auge, H. 2005. Molecular evidence for multiple introductions of garlic mustard (Alliaria petiolata, Brassicaceae) to North America. Mol. Ecol 14:1697–1706.Google Scholar
Ellis, M. B. and Ellis, J. P. 1997. Microfungi on Land Plants. Slough, UK Richmond Publishing.Google Scholar
Elton, C. S. 1958. The Ecology of Invasions by Animals and Plants. London, UK Methuen.Google Scholar
Enright, S. and Cipollini, D. 2007. Infection by powdery mildew Erysiphe cruciferarum (Erysiphacaeae) strongly affects growth and fitness of garlic mustard Alliaria petiolata (Brassicaceae). Am. J. Bot 94:1813–1820.CrossRefGoogle Scholar
Evans, J. A. and Landis, D. A. 2007. Pre-release monitoring of Alliaria petiolata (garlic mustard) invasions and the impacts of extant natural enemies in southern Michigan forests. Biol. Control 42:300–307.CrossRefGoogle Scholar
Gerber, E., Hinz, H. L., and Blossey, B. 2007. Impact of the belowground herbivore and potential biological control agent, Ceutorhynchus scrobicollis, on Alliaria petiolata performance. Biol. Control 42:355–364.Google Scholar
Jenkyn, J. F. and Rowlinson, C. J. 1977. Effects of fungicides and insecticides on mildew, viruses, and root yields of Swedes. Plant Pathol 26:166–174.Google Scholar
Keeler, M. S. and Chew, F. S. 2008. Escaping an evolutionary trap: preference and performance of a native insect on an exotic invasive host. Oecologia 156:559–568.CrossRefGoogle Scholar
Koike, S. T. 1997. First report of powdery mildew, caused by Erysiphe cruciferarum, on broccoli raab in California. Plant Dis 81:1093.CrossRefGoogle ScholarPubMed
Lehman, R. D. 1999. Multiflora rose, rose-rosette disease, and Phyllocoptes fructiphilus . Regul. Hortic 25:25–30.Google Scholar
Levine, J. M., Vila, M., D'Antonio, C. M., Dukes, J. S., Grigulis, K., and Lavorel, S. 2003. Mechanisms underlying the impacts of exotic plant invasions. Proc. R. Soc. Lond., Ser. B: Biol. Sci 270:775–781.Google Scholar
McCarthy, B. C. 1997. Response of a forest understory community to experimental removal of an invasive nonindigenous plant (Alliaria petiolata, Brassicaceae). Pages 117–130. In Luken, J. O. and Thieret, L. W. Assessment and Management of Plant Invasions. New York Springer-Verlag.Google Scholar
Meekins, J. F. and McCarthy, B. C. 1999. Competitive ability of Alliaria petiolata (garlic mustard, Brassicaceae), an invasive nonindigenous forest herb. Int. J. Plant Sci 160:743–752.Google Scholar
Meekins, J. F. and McCarthy, B. C. 2000. Responses of the biennial forest herb Alliaria petiolata to variation in population density, nutrient addition and light availability. J. Ecol 88:447–463.Google Scholar
Meekins, J. F., Ballard, H. E. Jr., and McCarthy, B. C. 2001. Genetic variation and molecular biogeography of a North American invasive plant species (Alliaria petiolata, Brassicaceae). Int. J. Plant Sci 162:161–169.Google Scholar
Nuzzo, V. A. 2002. Element Stewardship Abstract for Alliaria petiolata (Alliaria officinalis), Garlic Mustard. Arlington, VA Nature Conservancy.Google Scholar
Pardini, E. A., Drake, J. M., Chase, J. M., and Knight, T. M. 2009. Complex population dynamics and control of the invasive biennial Alliaria petiolata (garlic mustard). Ecol. Appl 19:387–397.Google Scholar
Prati, D. and Bossdorf, O. 2004. Allelopathic inhibition of germination by Alliaria petiolata (Brassicaceae). Am. J. Bot 91:285–288.Google Scholar
Rebek, K. A. and O'Neil, R. J. 2005. Impact of simulated herbivory on Alliaria petiolata survival, growth, and reproduction. Biol. Control 34:283–289.Google Scholar
Renwick, J. A. A., Zhang, W., Haribal, M., Attygalle, A. B., and Lopez, K. D. 2001. Dual chemical barriers protect a plant against different larval stages of an insect. J. Chem. Ecol 27:1575–1583.Google Scholar
Roberts, K. J. and Anderson, R. C. 2001. Effect of garlic mustard [Alliaria petiolata (Bieb. Cavara & Grande)] extracts on plants and arbuscular mycorrhizal (AM) fungi. Am. Midl. Nat 146:146–152.Google Scholar
Schemske, D. W. 1984. Population structure and local selection in Impatiens pallida (Balsaminaceae), a selfing annual. Evolution 38:817–832.CrossRefGoogle ScholarPubMed
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 4:727–731.Google Scholar
Susko, D. J. and Lovett-Doust, L. 2000. Plant-size and fruit-position effects on reproductive allocation in Alliaria petiolata (Brassicaceae). Can. J. Bot 78:1398–1407.Google Scholar
Wolfe, B. E., Rodgers, V. L., Stinson, K. A., and Pringle, A. 2008. The invasive plant Alliaria petiolata (garlic mustard) inhibits ectomycorrhizal fungi in its introduced range. J. Ecol 96:777–783.Google Scholar