Abstract
Invasive species are a leading threat to native ecosystems, and research regarding their effective control is at the forefront of applied ecology. Exotic facilitation has been credited with advancing the success of several aggressive invasive species. Here, we suggest using the knowledge of exotic facilitations to control invasive earthworm populations. In northern hardwood forests, the invasive shrubs Rhamnus cathartica (buckthorn) and Lonicera x bella (honeysuckle) produce high quality leaf litter, and their abundance is positively correlated with exotic earthworms, which increase nutrient cycling rates. We performed an invasive plant removal experiment in two northern hardwood forest stands, one dominated by buckthorn and the other by honeysuckle. Removal of invasive shrubs reduced exotic earthworm populations by roughly 50% for the following 3 years. By targeting invasive species that are part of positive feedback loops, land managers can multiply the positive effects of invasive species removal.
Similar content being viewed by others
References
Allison S, Vitousek P (2004) Rapid nutrient cycling in leaf litter from invasive plants in Hawai’i. Oecologia 141:612–619
Aplet G (1990) Alteration of earthworm community biomass by the alien Myrica faya in Hawaii. Oecologia 82:414–416
Bartelt-Ryser J, Joshi J, Schmid B, Brandl H, Balser T (2005) Soil feedbacks of plant diversity on soil microbial communities and subsequent plant growth. Perspect Plant Ecol Evol Syst 7:27–49
Boege K, Marquis R (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448
Bohlen P, Groffman P, Fahey T, Fisk M, Suarez E, Pelletier D, Fahey R (2004a) Ecosystem consequences of exotic earthworm invasion of north temperate forests. Ecosystems 7:1–12
Bohlen P, Scheu S, Hale C, McLean M, Migge S, Groffman P, Parkinson D (2004b) Non-native invasive earthworms as agents of change in northern temperate forests. Front Ecol Environ 2:427–435
Callaham M Jr, Gonzalez G, Hale C, Heneghan L, Lachnicht S, Zou X (2006) Policy and management responses to earthworm invasions in North America. Biol Invasions 8:1317–1329
Catling P (1997) The problem of invading alien trees and shrubs: some observations in Ontario and a Canadian checklist. Can Field Nat 111:338–342
Collier M, Vankat J, Hughes M (2002) Diminished plant richness and abundance below Lonicera maackii, an invasive shrub. Am Midl Nat 147:60–71
Dorning M, Cipollini D (2006) Leaf and root extracts of the invasive shrub, Lonicera maackii, inhibit seed germination of three herbs with no autotoxic effects. Plant Ecol 184:287–296
Ehrenfeld J (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523
Fagan M, Peart D (2004) Impact of the invasive shrub glossy buckthorn (Rhamnus frangula L.) on juvenile recruitment by canopy trees. For Ecol Manag 194:95–107
Frelich L, Hale C, Scheu S, Holdsworth A, Heneghan L, Bohlen P, Reich P (2006) Earthworm invasion into previously earthwormfree temperate and boreal forests. Biol Invasions 8:1235–1245
Gates G (1970) Miscellanea Megadrilogica VII. Megadrilogica 1:1–6
Gates G (1982) Farewell to North American megadriles. Megadrilogica 4:12–77
Godwin H (1943) Biological flora of the British Isles: Rhamnaceae. J Ecol 31:66–92
Gould A, Gorchov D (2000) Effects of the exotic invasive shrub Lonicera maackii, Amur Honeysuckle, on survival and fecundity of native forest annual herbs. Am Midl Nat 144:36–50
Groffman P, Bohlen P, Fisk M, Fahey T (2004) Exotic earthworm invasion and microbial biomass in temperate forest soils. Ecosystems 7:45–54
Hale C, Frelich L, Reich P (2005a) Exotic European earthworm invasion dynamics in northern hardwood forests of Minnesota, USA. Ecol Appl 15:848–860
Hale C, Frelich L, Reich P, Pastor J (2005b) Effects of European earthworm invasion on soil characteristics in northern hardwood forests of Minnesota, USA. Ecosytems 8:911–927
Hendriksen N (1990) Leaf litter selection by detrivore and geophagous earthworms. Biol Fertil Soils 10:17–21
Hendrix P, Bohen P (2002) Exotic earthworm invasions in North America: ecological and policy implications. Bioscience 52:801–811
Heneghan L, Steffen J, 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
Holdsworth A, Frelich L, Reich P (2007) Effects of earthworm invasion on plant species richness in northern Hardwood forests. Conserv Biol 21:997–1008
Hutchinson T, Vankat J (1997) Invasibility and effects of Amur honeysuckle in southwestern Ohio forests. Conserv Biol 11:1117–1124
James S (2004) Planetary processes and their interactions with earthworm distributions and ecology. In: Edwards CA (ed) Earthworm ecology, 2nd edn. CRC Press, Boca Raton, pp 53–62
Kardol P, Cornips N, van Kempen M, Bakx-Schotman J, van der Putter W (2007) Microbe-mediated plant-soil feedback causes historical contingency effects in plant community assembly. Ecol Monogr 77:147–162
Knight K, Kurylo J, Endress A, Stewart J, Reich P (2007) Ecology and ecosystem impacts of common buckthorn (Rhamnus cathartica): a review. Biol Invasions (online)
Kourtev P, Ehrenfeld J, Huang W (1998) Effects of exotic plant species on soil properties in hardwood forests of New Jersey. Water Air Soil Pollut 105:493–501
Lawrence A, Bowers M (2002) A test of the ‘hot’ mustard extraction method of sampling earthworms. Soil Biol Biochem 34:549–552
Luken J (1988) Population structure and biomass allocation of the naturalized shrub Lonicera maackii (Rupr.) Maxim. in forest and open habitats. Am Midl Nat 119:258–267
Luken J, Kuddes L, Tholemeir T (1997) Response of understory species to gap formation and soil disturbance in Lonicera maackii thickets. Restor Ecol 5:229–235
Madritch M, Donaldson J, Lindroth R (2007) Canopy herbivory can mediate the influence of plant genotype on soil processes through frass deposition. Soil Biol Biochem 39:1192–1201
McLean M, Parkinson D (1997) Changes in structure, organic matter and microbial activity in pine forest soil following the introduction of Dendrobaena octaedra (Oligochaeta, Lumbricidae). Soil Biol Biochem 29:537–540
Migge-Kleian S, McLean M, Maerz J, Heneghan L (2006) The influence of invasive earthworms on indigenous fauna in ecosystems previously uninhabited by earthworms. Biol Invasions 8:1275–1285
Mulvaney R (1996) Nitrogen—inorganic forms. In: Bartels JM (ed) Methods of soil analysis: part 3 chemical methods. Soil Science Society of America, Madison, WI, pp 1123–1184
Pergams O, Norton J (2006) Treating a single stem can kill the whole shrub: a scientific assessment of buckthorn control methods. Nat Area J 26:300–309
Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288
Possessky S, Williams C, Moriarty W (2000) Glossy Buckthorn, Rhamnus frangula L.: a threat to riparian plant communities of the northern allegheny plateau (USA). Nat Area J 20:290–292
Ragsdale D, Voegtlin D, O’Neil R (2004) Soybean aphid biology in North America. Ann Entomol Soc Am 97:204–208
Reynolds J (1977) The earthworms (Lumbricidae and Sparganophilidae) of Ontario. Royal Ontario Museum Miscellaneous Publication, Toronto, Ontario
Saya-Cork K, Sinsabaugh R, Zak D (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315
Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9:912–919
Simberloff D, Von Holle B (1999) Positive interactions of nonindenous species: invasional meltdown? Biol Invasions 1:21–32
Wilcove D, Rothstein D, Dubow J, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States. Bioscience 48:607–615
Acknowledgements
Funding was provided by NSF DEB-0344019 to RLL and MDM. We thank the UW Arboretum for site use permission, P. Zedler for sparking our interest in the topic, and K. Lawson for field assistance.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Madritch, M.D., Lindroth, R.L. Removal of invasive shrubs reduces exotic earthworm populations. Biol Invasions 11, 663–671 (2009). https://doi.org/10.1007/s10530-008-9281-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-008-9281-7