Biological Invasions

, Volume 11, Issue 3, pp 663–671 | Cite as

Removal of invasive shrubs reduces exotic earthworm populations

Original Paper


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.


European earthworms Invasive species Invasion meltdown 



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.


  1. Allison S, Vitousek P (2004) Rapid nutrient cycling in leaf litter from invasive plants in Hawai’i. Oecologia 141:612–619PubMedCrossRefGoogle Scholar
  2. Aplet G (1990) Alteration of earthworm community biomass by the alien Myrica faya in Hawaii. Oecologia 82:414–416CrossRefGoogle Scholar
  3. 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 7:27–49CrossRefGoogle Scholar
  4. Boege K, Marquis R (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448PubMedCrossRefGoogle Scholar
  5. 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 7:1–12CrossRefGoogle Scholar
  6. 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 2:427–435CrossRefGoogle Scholar
  7. 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 8:1317–1329CrossRefGoogle Scholar
  8. Catling P (1997) The problem of invading alien trees and shrubs: some observations in Ontario and a Canadian checklist. Can Field Nat 111:338–342Google Scholar
  9. Collier M, Vankat J, Hughes M (2002) Diminished plant richness and abundance below Lonicera maackii, an invasive shrub. Am Midl Nat 147:60–71CrossRefGoogle Scholar
  10. 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 184:287–296CrossRefGoogle Scholar
  11. Ehrenfeld J (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523CrossRefGoogle Scholar
  12. Fagan M, Peart D (2004) Impact of the invasive shrub glossy buckthorn (Rhamnus frangula L.) on juvenile recruitment by canopy trees. For Ecol Manag 194:95–107CrossRefGoogle Scholar
  13. 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 8:1235–1245CrossRefGoogle Scholar
  14. Gates G (1970) Miscellanea Megadrilogica VII. Megadrilogica 1:1–6Google Scholar
  15. Gates G (1982) Farewell to North American megadriles. Megadrilogica 4:12–77Google Scholar
  16. Godwin H (1943) Biological flora of the British Isles: Rhamnaceae. J Ecol 31:66–92CrossRefGoogle Scholar
  17. 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 144:36–50CrossRefGoogle Scholar
  18. Groffman P, Bohlen P, Fisk M, Fahey T (2004) Exotic earthworm invasion and microbial biomass in temperate forest soils. Ecosystems 7:45–54CrossRefGoogle Scholar
  19. Hale C, Frelich L, Reich P (2005a) Exotic European earthworm invasion dynamics in northern hardwood forests of Minnesota, USA. Ecol Appl 15:848–860CrossRefGoogle Scholar
  20. 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 8:911–927CrossRefGoogle Scholar
  21. Hendriksen N (1990) Leaf litter selection by detrivore and geophagous earthworms. Biol Fertil Soils 10:17–21Google Scholar
  22. Hendrix P, Bohen P (2002) Exotic earthworm invasions in North America: ecological and policy implications. Bioscience 52:801–811CrossRefGoogle Scholar
  23. 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 50:543–551CrossRefGoogle Scholar
  24. Holdsworth A, Frelich L, Reich P (2007) Effects of earthworm invasion on plant species richness in northern Hardwood forests. Conserv Biol 21:997–1008PubMedCrossRefGoogle Scholar
  25. Hutchinson T, Vankat J (1997) Invasibility and effects of Amur honeysuckle in southwestern Ohio forests. Conserv Biol 11:1117–1124CrossRefGoogle Scholar
  26. 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 53–62Google Scholar
  27. 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 77:147–162CrossRefGoogle Scholar
  28. 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)Google Scholar
  29. 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 105:493–501CrossRefGoogle Scholar
  30. Lawrence A, Bowers M (2002) A test of the ‘hot’ mustard extraction method of sampling earthworms. Soil Biol Biochem 34:549–552CrossRefGoogle Scholar
  31. Luken J (1988) Population structure and biomass allocation of the naturalized shrub Lonicera maackii (Rupr.) Maxim. in forest and open habitats. Am Midl Nat 119:258–267CrossRefGoogle Scholar
  32. Luken J, Kuddes L, Tholemeir T (1997) Response of understory species to gap formation and soil disturbance in Lonicera maackii thickets. Restor Ecol 5:229–235CrossRefGoogle Scholar
  33. 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 39:1192–1201CrossRefGoogle Scholar
  34. 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 29:537–540CrossRefGoogle Scholar
  35. 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 8:1275–1285CrossRefGoogle Scholar
  36. 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 1123–1184Google Scholar
  37. Pergams O, Norton J (2006) Treating a single stem can kill the whole shrub: a scientific assessment of buckthorn control methods. Nat Area J 26:300–309CrossRefGoogle Scholar
  38. 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 52:273–288CrossRefGoogle Scholar
  39. 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 20:290–292Google Scholar
  40. Ragsdale D, Voegtlin D, O’Neil R (2004) Soybean aphid biology in North America. Ann Entomol Soc Am 97:204–208CrossRefGoogle Scholar
  41. Reynolds J (1977) The earthworms (Lumbricidae and Sparganophilidae) of Ontario. Royal Ontario Museum Miscellaneous Publication, Toronto, OntarioGoogle Scholar
  42. 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 34:1309–1315CrossRefGoogle Scholar
  43. Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9:912–919PubMedCrossRefGoogle Scholar
  44. Simberloff D, Von Holle B (1999) Positive interactions of nonindenous species: invasional meltdown? Biol Invasions 1:21–32CrossRefGoogle Scholar
  45. Wilcove D, Rothstein D, Dubow J, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States. Bioscience 48:607–615CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.Department of EntomologyUniversity of WisconsinMadisonUSA

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