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Lumbricus terrestris Prefers to Consume Garlic Mustard (Alliaria petiolata) Seeds

Published online by Cambridge University Press:  20 January 2017

Patricia M. Quackenbush ,
RaeLynn A. Butler ,
Nancy C. Emery ,
Michael A. Jenkins ,
Eileen J. Kladivko  and
Kevin D Gibson
Patricia M. Quackenbush
Affiliation:
Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907
RaeLynn A. Butler
Affiliation:
Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907
Nancy C. Emery
Affiliation:
Department of Biological Sciences and Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907
Michael A. Jenkins
Affiliation:
Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN 47907
Eileen J. Kladivko
Affiliation:
Department of Agronomy, Purdue University, West Lafayette, IN 47907
Kevin D Gibson*
Affiliation:
Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907
*
Corresponding author's E-mail: kgibson@purdue.edu
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Abstract

Temperate and boreal forests in Canada and the northeastern United States have been invaded by several exotic species, including European earthworms (family Lumbricidae) and garlic mustard. Earthworms and garlic mustard co-occur and are both known to adversely impact some native plant species. However, relatively little is known about potential interactions between these two invaders. In a series of growth chamber experiments, we determined the palatability of garlic mustard and six native herbaceous forest species (shooting star, columbine, wild geranium, sweet cicely, butterfly milkweed, and yellow jewelweed) to the common nightcrawler. We also assessed the ability of the common nightcrawler to bury and digest garlic mustard and wild geranium. When offered seeds from garlic mustard and a native plant species, the earthworms ingested more garlic mustard seeds than seeds from four of the six native species. In a mesocosm experiment, the common nightcrawlers apparently digested 72 and 27% of garlic mustard and wild geranium seeds, respectively, that were placed on the soil surface. No seeds were observed on the soil surface at the end of the experiment but the majority of recovered seeds for both species were found within the top 10 cm (3.94 in). More seeds were recovered in 0- to 10-cm and 31- to 40-cm sections for wild geranium than for garlic mustard. No difference in seed recovery was detected at the other depths. Garlic mustard seed is readily consumed by common nightcrawlers and appears to be preferred over some native plant species suggesting that common nightcrawlers may reduce the size of the garlic mustard seed bank.

Keywords

Common nightcrawler, Lumbricus terrestris L.garlic mustard, Alliaria petiolata (M. Bieb.) Cavara & Grande ALAPEcolumbine, Aquilegia canadensis L.butterfly milkweed, Asclepias tuberosa L. ASCTUcommon shooting star, Dodecatheon meadia L.wild geranium, Geranium maculata L.yellow jewelweed, Impatiens pallida Nuttsweet cicely, Osmorhiza claytonia (Michx.) C.B. ClarkeNative plantsinvasive plantsseed predationinvasive earthwormforestseed burial
Type
Research Article
Information
Invasive Plant Science and Management , Volume 5 , Issue 2 , June 2012 , pp. 148 - 154
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Alban, D. H. and Berry, E. C. 1994. Effects of earthworm invasion on morphology, carbon and nitrogen of a forest soil. Appl. Soil Ecol. 1:243–249.Google Scholar
Belote, R. T. and Jones, R. H. 2009. Tree leaf litter composition and non-native earthworms influence plant invasion in experimental forest floor mescosms. Biol. Invasions 11:1045–1052.Google Scholar
Bohlen, P. J., Scheu, S., Hale, C. M., McLean, M. A., Migge, S., Groffman, P. M., and Parkinson, D. 2004. Non-native invasive earthworms as agents of change in northern temperate forests. Front. Ecol. Environ. 2:427–435.Google Scholar
Didham, R. K., Tylianakis, J. M., Hutchison, M. A., Ewers, R. M., and Gemmell, N. J. 2005. Are invasive species the drivers of ecological change? Trends Ecol. Evol. 20:470–474.Google Scholar
Dukes, J. S. and Mooney, H. A. 1999. Does global change increase the success of biological invaders? Trends Ecol. Evol. 14:135–139.Google Scholar
Ehrenfeld, J. G. 2003. Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523.Google Scholar
Ehrenfeld, J. G., Kourtev, P., and Huang, W. Z. 2001. Changes in soil functions following invasions of exotic understory plants in deciduous forests. Ecol. Appl. 11:1287–1300.Google Scholar
Eisenhauer, N., Butenschoen, O., Radsick, S., and Scheu, S. 2010. Earthworms as seedling predators: importance of seeds and seedlings for earthworm nutrition. Soil Biol. Biochem. 42:1245–1252.Google Scholar
Eisenhauer, N. and Scheu, S. 2008. Invasibility of experimental grassland communities: the role of earthworms, plant functional group identity and seed size. Oikos 117:1026–1036.Google Scholar
Eisenhauer, N., Schuy, M., Butenschoen, O., and Scheu, S. 2009. Direct and indirect effects of endogeic earthworms on plant seeds. Pedobiologia 52:151–162.Google Scholar
Frelich, L. E., Hale, C. M., Scheu, S., Holdsworth, A. R., Heneghan, L., Bohlen, P. J., and Reich, P. B. 2006. Earthworm invasion into previously earthworm-free temperate and boreal forests. Biol. Invasions 8:1235–1245.Google Scholar
Hale, C. M. 2007. Earthworms of the Great Lakes. Duluth, MN Kollath and Stensaas. 36 p.Google Scholar
Hale, C. M., Frelich, L. E., and Reich, P. B. 2005. Exotic European earthworm invasion dynamics in northern hardwood forests of Minnesota, USA. Ecol. Appl. 15:848–860.Google Scholar
Hale, C. M., Frelich, L. E., Reich, P. B., and Pastor, J. 2008. Exotic earthworm effects on hardwood forest floor, nutrient availability and native plants: a mesocosm study. Oecologia 155:509–518.Google Scholar
Heimpel, G. E., Frelich, L. E., Landis, D. A., Hopper, K. R., Hoelmer, K. A., Sezen, Z., Asplen, M. K., and Wu, K. M. 2010. European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biol. Invasions 12:2913–2931.Google Scholar
Heneghan, L., Steffen, J., and Fagen, K. 2007. Interactions of an introduced shrub and introduced earthworms in an Illinois urban woodland: impact on leaf litter decomposition. Pedobiologia 50:543–551.Google Scholar
Kalisz, P. J. 1993. Native and exotic earthworms in deciduous forest soils of eastern North America. Pages 93–100 in McKnight, B. N., ed. Biological Pollution: The Control and Impact of Invasive Exotic Species. Indianapolis Indiana Academy of Science.Google Scholar
Kalisz, P. J. and Dotson, D. B. 1989. Land-use history and the occurrence of exotic earthworms in the mountains of eastern Kentucky. Am. Midl. Nat. 122:288–297.Google Scholar
Kladivko, E. J. 1993. Earthworms and Crop Management. West Lafayette, IN Purdue University Cooperative Extension Service AY-279. 5 p.Google 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 83:3152–3166.Google Scholar
Kourtev, P. S., Ehrenfeld, J. G., and Huang, W. Z. 1998. Effects of exotic plant species on soil properties in hardwood forests of New Jersey. Water Air Soil Poll. 105:493–501.Google Scholar
Lawrence, B., Fisk, M. C., Fahey, T. J., and Suarez, E. R. 2003. Influence of nonnative earthworms on mycorrhizal colonization of sugar maple (Acer saccharum). New Phytol. 157:145–153.Google Scholar
Lazcano, C., Sampedro, L., Zas, R., and Dominguez, J. 2010. Assessment of plant growth promotion by vermicompost in different progenies of maritime pine (Pinus pinaster Ait.). Compost Sci. Util. 18:111–118.Google Scholar
MacDougall, A. S. and Turkington, R. 2005. Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86:42–55.Google Scholar
Madritch, M. D. and Lindroth, R. L. 2009. Removal of invasive shrub reduces exotic earthworm populations. Biol. Invasions 11:663–671.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
Milcu, A., Schumacher, J., and Scheu, S. 2006. Earthworms (Lumbricus terrestris) affect plant seedling recruitment and microhabitat heterogeneity. Funct. Ecol. 20:261–268.Google Scholar
Mooney, H. A. and Cleland, E. E. 2001. The evolutionary impact of invasive species. Proc. Natl. Acad. Sci. U. S. A. 98:5446–5451.Google Scholar
Natural Resources Conservation Service. 2011. The PLANTS Database. http://plants.usda.gov. Accessed May 15, 2011.Google Scholar
Nuzzo, V. A., Maerz, J. C., and Blossey, B. 2009. Earthworm invasion as the driving force behind plant invasion and community change in northeastern North American forests. Conserv. Biol. 23:966–974.Google Scholar
Prati, D. and Bossdorf, O. 2004. Allelopathic inhibition of germination by Alliaria petiolata (Brassicaceae). Am. J. Bot. 91:285–288.Google Scholar
Regnier, E., Harrison, S. K., Liu, J., Schmoll, J. T., Edwards, C. A., Arancon, N., and Holloman, C. 2008. Impact of an exotic earthworm on seed dispersal of an indigenous US weed. J. Appl. Ecol. 45:1621–1629.Google Scholar
Sanders, N. J., Gotelli, N. J., Heller, N. E., and Gordon, D. M. 2003. Community disassembly by an invasive species. Proc. Natl. Acad. Sci. U. S. A. 100:2474–2477.Google Scholar
Shumway, D. L. and Koide, R. T. 1994. Seed preferences of Lumbricus terrestris L. Appl. Soil Ecol. 1:11–15.Google Scholar
Simberloff, D. and Von Holle, B. 1999. Positive interactions of nonindigenous species: invasional meltdown? Biol. Invasions 1:21–32.Google 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. 4:727–731.Google Scholar
Vitousek, P. M., D'Antonio, C. M., Loope, L. L., and Westbrooks, R. 1996. Biological invasions as global environmental change. Am. Sci. 84:468–478.Google Scholar
Willems, J. H. and Huijsmans, K. G. A. 1994. Vertical seed dispersal by earthworms: a quantitative approach. Ecography 17:124–130.Google Scholar
Yatskievych, K. 2002. Field Guide to Indiana Wildflowers. Bloomington Indiana University Press. 357 p.Google Scholar
Zavaleta, E. S., Hobbs, R. J., and Mooney, H. A. 2001. Viewing invasive species removal in a whole-ecosystem context. Trends Ecol. Evol. 16:454–459.Google Scholar