Biological Invasions

, Volume 8, Issue 6, pp 1235–1245 | Cite as

Earthworm invasion into previously earthworm-free temperate and boreal forests

  • Lee E. FrelichEmail author
  • Cindy M. Hale
  • Stefan Scheu
  • Andrew R. Holdsworth
  • Liam Heneghan
  • Patrick J. Bohlen
  • Peter B. Reich
Original paper


Earthworms are keystone detritivores that can influence primary producers by changing seedbed conditions, soil characteristics, flow of water, nutrients and carbon, and plant–herbivore interactions. The invasion of European earthworms into previously earthworm-free temperate and boreal forests of North America dominated by Acer, Quercus, Betula, Pinus and Populus has provided ample opportunity to observe how earthworms engineer ecosystems. Impacts vary with soil parent material, land use history, and assemblage of invading earthworm species. Earthworms reduce the thickness of organic layers, increase the bulk density of soils and incorporate litter and humus materials into deeper horizons of the soil profile, thereby affecting the whole soil food web and the above ground plant community. Mixing of organic and mineral materials turns mor into mull humus which significantly changes the distribution and community composition of the soil microflora and seedbed conditions for vascular plants. In some forests earthworm invasion leads to reduced availability and increased leaching of N and P in soil horizons where most fine roots are concentrated. Earthworms can contribute to a forest decline syndrome, and forest herbs in the genera Aralia, Botrychium, Osmorhiza, Trillium, Uvularia, and Viola are reduced in abundance during earthworm invasion. The degree of plant recovery after invasion varies greatly among sites and depends on complex interactions with soil processes and herbivores. These changes are likely to alter competitive relationships among plant species, possibly facilitating invasion of exotic plant species such as Rhamnus cathartica into North American forests, leading to as yet unknown changes in successional trajectory.


Aporrectodea Dendrobaena Exotic earthworm invasion Lumbricus rubellus Lumbricus terrestris Keystone species Minnesota forests New York forests 


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Funding from the National Science Foundation (DEB-0075236) and University of Minnesota Center for Hardwood Ecology is gratefully acknowledged.


  1. Alban DH, Berry EC (1994) Effects of earthworm invasion on morphology, carbon, and nitrogen of a forest soil. Appl Soil Ecol 1:243–249CrossRefGoogle Scholar
  2. Augustine DJ, Frelich LE, Jordan PA (1998) Evidence for two alternate stable states in an ungulate grazing system. Ecol Appl 8:1260–1269Google Scholar
  3. Bal L (1982) Zoological ripening of soils. Centre for Agricultural Publishing and Documents, Wageningen, The NetherlandsGoogle Scholar
  4. Baskin CC, Baskin JM (1998) Seeds: ecology, biogeography and evolution of dormancy and germination. Academic Press, San DiegoGoogle Scholar
  5. Beals EW, Cottam G, Vogel RJ (1960) Influence of deer on vegetation of the Apostle Islands, Wisconsin. J Wildl Manage 24:68–80Google Scholar
  6. Blair JM, Parmalee RW, Allen MF, McCartney DA, Stinner BR (1997) Changes in soil N pools in response to earthworm population manipulations in agroecosystems with different N sources. Soil Biol Biochem 29:361–36CrossRefGoogle Scholar
  7. Bohlen PJ, Groffman PM, Fahey TJ, Fisk MC, Suarez E, Pelletier DM, Fahey RT (2004a) Ecosystem consequences of exotic earthworm invasion of north temperate forests. Ecosystems 7:1–12CrossRefGoogle Scholar
  8. Bohlen PJ, Scheu S, Hale CM, McLean MA, Migge S, Groffman PM, Parkinson D (2004b) Non-native invasive earthworms as agents of change in northern temperate forests. Front Ecol Environ 2:427–435Google Scholar
  9. Bohlen PJ, Pelletier DM, Groffman PM, Fahey TJ, Fisk MC (2004c) Influence of earthworm invasion on redistribution and retention of soil carbon and nitrogen in northern temperate forests. Ecosystems 7:13–27CrossRefGoogle Scholar
  10. Brundrett MC, Kendrick B (1988) The mycorrhizal status, root anatomy and phenology of plants in a sugar maple forest. Can J Bot 66:1153–1173CrossRefGoogle Scholar
  11. Brussaard L (1999) On the mechanisms of interactions between earthworms and plants. Pedobiologia 43:880–885Google Scholar
  12. Burtelow AE, Bohlen PJ (1998) Influence of exotic earthworm invasion on soil organic matter, microbial biomass and denitrification potential in forest soils of the northeastern United States. Appl Soil Ecol 9:197–202CrossRefGoogle Scholar
  13. Cain ML, Damman H, Muir A (1998) Seed dispersal and the Holocene migration of woodland herbs. Ecol Monogr 68:325–347CrossRefGoogle Scholar
  14. Canham CD, Finzi AC, Pacala SW, Burbank DH (1994) Causes and consequences of resource heterogeneity in forests: interspecific variation in light transmission by canopy trees. Can J For Res 24:337–349Google Scholar
  15. Côté SD, Rooney TP, Tremblay J-P, Dussault CD, Waller DM (2004) Ecological impacts of deer overabundance. Ann Rev Ecol Syst 35:113–147CrossRefGoogle Scholar
  16. Cothrel SR, Vimmerstedt JP, Kost DA (1997) In situ recycling of urban deciduous litter. Soil Biol Biochem 29:295–298CrossRefGoogle Scholar
  17. Curry JP (1998) Factors affecting earthworm abundance in soils. In: Edwards A (ed) Earthworm ecology. St. Lucie Press, Boca Raton FL, pp 37–64Google Scholar
  18. Curtis JT (1959) The vegetation of Wisconsin. University of Wisconsin Press, Madison WI, 657 ppGoogle Scholar
  19. Dymond P, Scheu S, Parkinson D (1997) Density and distribution of Dendrobaena octaedra (Lumbricidae) in aspen and pine forests in the Canadian Rocky Mountains (Alberta). Soil Biol Biochem 29:265–273CrossRefGoogle Scholar
  20. Edwards CA, Bohlen P (1995) Biology and ecology of earthworms. Chapman and Hall, New York, 426 ppGoogle Scholar
  21. Edwards CA (ed) (2004) Earthworm ecology, 2nd edn. CRC Press, Boca Raton FL, 456 ppGoogle Scholar
  22. Francis R, Read DJ (1994) The contributions of mycorrhizal fungi to the determination of plant community structure. Plant Soil 159:11–25Google Scholar
  23. Grime JP (1979) Plant strategies and vegetation processes. John Wiley and Sons, Chichester England, 222 ppGoogle Scholar
  24. Gundale MJ (2002) Influence of exotic earthworms on the soil organic horizon and the rare fern Botrychium mormo. Conserv Biol 16:1555–1561CrossRefGoogle Scholar
  25. Hale CM, Frelich LE, Reich PB (2005a) Effects of European earthworm invasion on soil characteristics in northern hardwood forests of Minnesota. Ecosystems 8:911–927Google Scholar
  26. Hale CM, Frelich LE, Reich PB (2005b) Exotic European earthworm invasion dynamics in northern hardwood forests of Minnesota, U.S.A. Ecol Appl 15:848–860Google Scholar
  27. Hale CM (2004) Ecological consequences of exotic invaders: interactions involving European earthworms and native plant communities in hardwood forests. PhD Thesis, Department of Forest Resources, University of Minnesota, 169 ppGoogle Scholar
  28. Harper JL, Williams JT, Sager GR (1965) The behavior of seeds in soil: the heterogeneity of soil surfaces and its role in determining the establishment of plants from seeds. J Ecol 53:273–286CrossRefGoogle Scholar
  29. Hendriksen NB (1990) Leaf litter selection by detrivore and geophagous earthworms. Biol Fertil Soil 10:17–21Google Scholar
  30. Heneghan L, Clay C, Brundage C (2002) Rapid decomposition of buckthorn litter may change soil nutrient levels. Ecol Restor 20:108–111Google Scholar
  31. Heneghan L (2003) And when they got together... The impacts of eurasian earthworm and invasive shrubs on Chicago woodland ecosystems. Chic Wild J1:27–31Google Scholar
  32. Horsley SB, Stout SL, deCalesta DS (2003) White-tailed deer impact on the vegetation dynamics of a northern hardwood forest. Ecol Appl 13:98–118Google Scholar
  33. Johnson NC, Tilman GD, Wedin D (1992) Plant and soil controls on mycorrhizal fungal communities. Ecology 73:2034–2042CrossRefGoogle Scholar
  34. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386Google Scholar
  35. Kostel-Hughes F (1995) The role of soil seed banks and leaf litter in the regeneration of native and exotic tree species in urban forests. PhD Thesis, Graduate Program in Ecology, Fordham University, Bronx, NY, 236 ppGoogle Scholar
  36. Kubiena WL (1948) Entwicklungslehre des Bodens. Springer, WienGoogle Scholar
  37. Langmaid KK (1964) Some effects of earthworm invasion in virgin podsols. Can J Soil Sci 44:34–37CrossRefGoogle Scholar
  38. Leck MA, Parker VT, Simpson RL (eds) (1989) The ecology of soil seed banks. Academic Press, San Diego California, 462 ppGoogle Scholar
  39. Lawrence B, Fisk MC, Fahey TJ, Suarez ER (2003) Influence of nonnative earthworms on mycorrhizal colonization of sugar maple (Acer saccharum). New Phytol 157:145–153CrossRefGoogle Scholar
  40. Lee KE (1985) Earthworms – Their ecology and relationships with soils and land use. Academic Press, Sydney, 411 ppGoogle Scholar
  41. Lunt HA, Jacobson HGM (1944) The chemical composition of earthworm casts. Soil Sci 58:367–375Google Scholar
  42. Marquis DA (1975) Seed storage and germination under northern hardwood forests. Can J For Res 5:478–484Google Scholar
  43. McLean MA, Parkinson D (1997a) 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
  44. McLean MA, Parkinson D (1997b) Soil impacts of the epigeic earthworm Dendrobaena octaedra on organic matter and microbial activity in lodgepole pine forest. Can J For Res 27:1907–1913CrossRefGoogle Scholar
  45. McLean MA, Parkinson D (1998a) Impacts of epigeic earthworm Dendrobaena octaedra on oribatid mite community diversity and microarthropod abundances in pine forest floor: a mesocosm study. Appl Soil Ecol 7:125–136CrossRefGoogle Scholar
  46. McLean MA, Parkinson D (1998b) Impacts of the epigeic earthworm Dendrobaena octaedra on microfungal community structure in pine forest floor – a mesocosm study. Appl Soil Ecol 8:61–75CrossRefGoogle Scholar
  47. McLean MA, Parkinson D (2000) Field evidence of the effects of the epigeic earthworm Dendrobaena octaedra on the microfungal community in pine forest floor. Soil Biol Biochem 32:351–360CrossRefGoogle Scholar
  48. Migge S (2001) The effect of earthworm invasion on nutrient turnover, microorganisms and microarthropods in Canadian aspen forest soil. PhD Thesis, Technische Universität Darmstadt, Darmstadt, GermanyGoogle Scholar
  49. Mladenoff DJ (1985) Dynamics of soil seed banks, vegetation and nitrogen availability in treefall gaps. PhD Thesis, Department of Botany, University of Wisconsin–Madison, 164 ppGoogle Scholar
  50. Motzkin GD, Foster DR, Allen A, Harrod J, Boone R (1996) Controlling site to evaluate history: vegetation patterns of a New England sand plain. Ecol Monogr 66:345–365CrossRefGoogle Scholar
  51. Nielson GA, Hole FD (1963) A study of the natural processes of incorporation of organic matter into soil in the University of Wisconsin Arboretum. Wisc Acad Sci Arts Lett 52:213–227Google Scholar
  52. Nielson GA, Hole FD (1964) Earthworms and the development of coprogenous A1 horizons in forest soils of Wisconsin. Soil Sci Soc Am Proc 28:426–430CrossRefGoogle Scholar
  53. Nixon W (1995) As the worm turns. Am For 101:34–36Google Scholar
  54. Newman EI, Reddell P (1988) Relationship between mycorrhizal infection and diversity in vegetation: evidence from the Great Smoky Mountains. Funct Ecol 2:259–262CrossRefGoogle Scholar
  55. Nordström S, Rundgren S (1974) Environmental factors and lumbricid associations in southern Sweden. Pedobiologia 14:1–27Google Scholar
  56. Paré D, Bernier B (1989) Origin of phosphorous deficiency observed in declining sugar maple stands in the Quebec Appalachians. Can J For Res 19:24–34Google Scholar
  57. Parkin TB, Berry EC (1994) Nitrogen transformations associated with earthworm casts. Soil Biol Biochem 26:1233–1238CrossRefGoogle Scholar
  58. Parkinson D, McLean MA, Scheu S (2004) Impacts of earthworms on the community structure of other biota in forest soils. In: Edwards CA (ed) Earthworm ecology, 2nd edn. CRC Press, Boca Raton FL, pp 241–259Google Scholar
  59. Pastor J, Dewey B, Moen R, Mladenoff DJ, White MA, Cohen Y (1998) Spatial patterns in the moose-forest-soil ecosystem on Isle Royale, Michigan, USA. Ecol Appl 8:411–424Google Scholar
  60. Pickett STA and McDonnell MJ (1989) Seed bank dynamics in temperate deciduous forest. In: Leck MA, Parker VT, Simpson RL (eds) The ecology of soil seed banks. Academic Press, San Diego CA, pp 123–145Google Scholar
  61. Ponge JF, Delhaye L (1995) The heterogeneity of humus profiles and earthworm communities in a virgin beech forest. Biol Fertil Soil 20:24–32CrossRefGoogle Scholar
  62. Proulx N (2003) Ecological risk assessment of non-indigenous earthworm species. Prepared for U.S. Fish and Wildlife Service, International Affairs, Division of Scientific Authority by Minnesota Department of Natural Resources, St. Paul, MinnesotaGoogle Scholar
  63. Rogers R (1990) Quercus alba L. White oak. In: Burns RM and Honkala BH (Technical Coordinators), Silvics of North America, Volume 2, Hardwoods, United States Department of Agriculture, Forest Service, Agriculture Handbook 654, Washington DC, pp 605–613Google Scholar
  64. Sander I.L (1990) Quercus rubra L. Northern red oak. In: Burns RM and Honkala BH (Technical Coordinators), Silvics of North America, Volume 2, Hardwoods, United States Department of Agriculture, Forest Service, Agriculture Handbook 654, Washington DC, pp 727–733Google Scholar
  65. Schaefer M (1991) Animals in European temperate deciduous forest. In: Röhrig E, Ulrich B (eds) Temperate deciduous forests. Ecosystems of the world 7. Elsevier, Amsterdam, pp 503–525Google Scholar
  66. Scheu S (1987) The influence of earthworms (Lumbricidae) on the nitrogen dynamics in the soil litter system of a deciduous forest. Oecologia 72:197–201CrossRefGoogle Scholar
  67. Scheu S (2003) Effects of earthworms on plant growth: patterns and perspectives. Pedobiologia 47:846–856Google Scholar
  68. Scheu S, Parkinson D (1994a) Effects of invasion of an aspen forest (Canada) by Dendrobaena octaedra (Lumbricidae) on plant growth. Ecology 75:2348–2361CrossRefGoogle Scholar
  69. Scheu S, Parkinson D (1994b) Effects of earthworms on nutrient dynamics, carbon turnover, and microorganisms in soil from cool temperate forests of the Canadian Rocky Mountains – laboratory studies. Appl Soil Ecol 1:113–125CrossRefGoogle Scholar
  70. Shaw C, Pawluk S (1986) The development of soil structure by Octolasion tyrtaeum, Aporrectodea turgida and Lumbricus terrestris in parent materials belonging to different textural classes. Pedobiologia 29:327–339Google Scholar
  71. Suarez ER, Fahey TJ, Groffman PM, Bohlen PJ, Fisk MC (2004) Effects of exotic earthworms on soil phosphorous cycling in two broadleaf temperate forests. Ecosystems 7:28–44CrossRefGoogle Scholar
  72. Sydes C, Grime JP (1981) Effects of tree leaf litter on herbaceous vegetation in deciduous woodland: an experimental investigation. J Ecol 69:249–262CrossRefGoogle Scholar
  73. Syers JK, Sharpley AN, Keeney DR (1979) Cycling of nitrogen by surface casting earthworms in pasture ecosystems. Soil Biol Biochem 11:181–185CrossRefGoogle Scholar
  74. Tiunov AV, Hale CM, Holdsworth AR, Perel TS (2006) Invasion patterns of lumbricidae into the previously earthworm-free areas of north-eastern Europe and the western Great Lakes Region of North America. Biological Invasions (in press)Google Scholar
  75. Tomlin AD, Shipitalo MJ, Edwards WM, Protz R (1995) Earthworms and their influence on soil structure and infiltration. In: Hendrix PF (ed) Earthworm ecology and biogeography in North America. CRC Press, Boca Raton FL, pp 159–184Google Scholar
  76. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolfengel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Lee E. Frelich
    • 1
    Email author
  • Cindy M. Hale
    • 1
    • 2
  • Stefan Scheu
    • 3
  • Andrew R. Holdsworth
    • 1
  • Liam Heneghan
    • 4
  • Patrick J. Bohlen
    • 5
  • Peter B. Reich
    • 1
  1. 1.Department of Forest ResourcesUniversity of MinnesotaSt. PaulUSA
  2. 2.Natural Resources Research InstituteUniversity of Minnesota–DuluthDuluthUSA
  3. 3.Institut für ZoologieTechnische Universität DarmstadtDarmstadtGermany
  4. 4.Environmental Science ProgramDePaul UniversityChicagoUSA
  5. 5.Archbold Biological StationLake PlacidUSA

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