Skip to main content

Advertisement

Log in

Invasion of exotic earthworms into ecosystems inhabited by native earthworms

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The most conspicuous biological invasions in terrestrial ecosystems have been by exotic plants, insects and vertebrates. Invasions by exotic earthworms, although not as well studied, may be increasing with global commerce in agriculture, waste management and bioremediation. A number of cases has documented where invasive earthworms have caused significant changes in soil profiles, nutrient and organic matter dynamics, other soil organisms or plant communities. Most of these cases are in areas that have been disturbed (e.g., agricultural systems) or were previously devoid of earthworms (e.g., north of Pleistocene glacial margins). It is not clear that such effects are common in ecosystems inhabited by native earthworms, especially where soils are undisturbed. We explore the idea that indigenous earthworm fauna and/or characteristics of their native habitats may resist invasion by exotic earthworms and thereby reduce the impact of exotic species on soil processes. We review data and case studies from temperate and tropical regions to test this idea. Specifically, we address the following questions: Is disturbance a prerequisite to invasion by exotic earthworms? What are the mechanisms by which exotic earthworms may succeed or fail to invade habitats occupied by native earthworms? Potential mechanisms could include (1) intensity of propagule pressure (how frequently and at what densities have exotic species been introduced and has there been adequate time for proliferation?); (2) degree of habitat matching (once introduced, are exotic species faced with unsuitable habitat conditions, unavailable resources, or unsuited feeding strategies?); and (3) degree of biotic resistance (after introduction into an otherwise suitable habitat, are exotic species exposed to biological barriers such as predation or parasitism, “unfamiliar” microflora, or competition by resident native species?). Once established, do exotic species co-exist with native species, or are the natives eventually excluded? Do exotic species impact soil processes differently in the presence or absence of native species? We conclude that (1) exotic earthworms do invade ecosystems inhabited by indigenous earthworms, even in the absence of obvious disturbance; (2) competitive exclusion of native earthworms by exotic earthworms is not easily demonstrated and, in fact, co-existence of native and exotic species appears to be common, even if transient; and (3) resistance to exotic earthworm invasions, if it occurs, may be more a function of physical and chemical characteristics of a habitat than of biological interactions between native and exotic earthworms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abbott I (1985) Distribution of introduced earthworms in northern jarrah forest of Western Australia. Aust J␣Soil Res 23:263–270

    Article  Google Scholar 

  • Alban DH, Berry EC (1994) Effects of earthworm invasion on morphology, carbon and nitrogen of a forest soil. Appl Soil Ecol 1:243–249

    Article  Google Scholar 

  • Baker G, Carter P, Barrett V, Hirth J, Mele P, Gourley C (2002) Does the deep-burrowing earthworm, Aporrectodea longa, compete with resident earthworm communities when introduced to pastures in south-eastern Australia? Eur J Soil Biol 38:39–42

    Article  Google Scholar 

  • Beddard FE (1912) Earthworms and their allies. Cambridge University Press, London, p 145

    Google Scholar 

  • Bhadauria T, Ramakrishnan PS, Srivastava KN (2000) Diversity and distribution of endemic and exotic earthworms in natural and regenerating ecosystems in the central Himalayas, India. Soil Biol Biochem 32:2045–2054

    Article  CAS  Google Scholar 

  • 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 7:1–12

    Article  Google Scholar 

  • 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 2:427–435

    Google Scholar 

  • Brown GG, Doube BM (2004) Functional interactions between earthworms, microorganisms, organic matter and plants. In: Edwards C (ed) Earthworm ecology. 2nd edn. CRC Press, Boca Raton, FL, pp␣213–239

    Google Scholar 

  • Burtelow AE, Bohlen PJ, Groffman PM (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 9:197–202

    Article  Google Scholar 

  • Callaham MA Jr, Hendrix PF (1997) Relative abundance and seasonal activity of earthworms (Lumbricidae and Megascolecidae) as determined by hand-sorting and formalin extraction in forest soils on the southern Appalachian piedmont. Soil Biol Biochem 29:317–321

    Article  CAS  Google Scholar 

  • Callaham MA Jr, Blair JM (1999) Influence of differing land management on the invasion of North American tallgrass prairie soils by European earthworms. Pedobiologia 43:507–512

    Google Scholar 

  • Callaham MA Jr, Blair JM, Hendrix PF (2001) Native North American and introduced European earthworms in tallgrass prairie: behavioral patterns and influences on plant growth. Biol Fertil Soil 34:49–56

    Article  CAS  Google Scholar 

  • Callaham MA Jr, Hendrix PF, Phillips RJ (2003) Occurrence of an exotic earthworm (Amynthas agrestis) in undisturbed soil of the southern Appalachian Mountains, USA. Pedobiologia 47:466–470

    Google Scholar 

  • Daane LL, Häggblom MM (1999) Earthworm egg capsules as vectors for the environmental introduction of biodegradative bacteria. Appl Environ Microbiol 65:2376–2381

    PubMed  CAS  Google Scholar 

  • Dalby PR, Baker GH, Smith SE (1998) Potential impact of an introduced lumbricid on a native woodland in South Australia. Appl Soil Ecol 9:351–354

    Article  Google Scholar 

  • Damoff GA (2005) Are east Texas bottomland forest soils being re-engineered by the exotic invasive earthworm Amynthas diffringens (Baird, 1869)? American Society of Agronomy International Annual Meetings, November 6–10, 2005, Salt Lake City, UT. Abstract 192-9

  • Decaëns T, Blanchart E, Fragoso C, Lavelle P, Jimenez JJ, Barros E, Chauvel A (2004) Soil macrofaunal communites in permanent pastures derived from tropical forest or savanna. Agric Ecosyst Environ 103:301–312

    Article  Google Scholar 

  • Dotson DB, Kalisz PJ (1989) Characteristics and ecological relationships of earthworm assemblages in undisturbed forest soils in the southern Appalachians of Kentucky, USA. Pedobiologia 33:211–220

    Google Scholar 

  • Edwards CA (ed) (2004) Earthworm ecology, 2nd edn. St.␣Lucie Press, Boca Raton, FL

    Google Scholar 

  • Edwards CA, Bohlen PJ (1996) The biology and ecology of earthworms, 3rd edn. Chapman and Hall, London

    Google Scholar 

  • Eisen G (1900) Researches in American Oligochaeta, with especial reference to those of the Pacific Coast and adjacent islands. Proc Calif Acad Sci II:85–276

    Google Scholar 

  • Fragoso C, Barois I, James S (1995) Native earthworms of the north Neotropical region: current status and controversies. In: Hendrix PF (ed) Earthworm ecology and biogeography in North America. Lewis Publishers, Boca Raton, FL

    Google Scholar 

  • Fragoso C, Lavelle P, Blanchart E, Senapati B, Jimenez J, de los Angeles Martinez M, Decaens T, Tondoh J (1999) Earthworm communities of tropical agroecosystems: origin, structure and influences of management practices. In: Lavelle P, Brussaard L, Hendrix P (eds) Earthworm management in tropical agroecosystems. CABI Publishing, New York, pp 27–55

    Google Scholar 

  • Gates GE (1970) Miscellanea Megadrilogica VII. Megadrilogica 1:1–6

    Google Scholar 

  • Ghilarov MS, Perel TS (1984) Transfer of earthworms (Lumbricidae, Oligochaeta) for soil amelioration in the USSR. Pedobiologia 27:107–113

    Google Scholar 

  • Gilot-Villenave C (1994) Determination of the origin of the different growing abilities of two populations of Millsonia anomala (Omodeo and Vaillaud), a tropical geophageous earthworm. Eur J Soil Biol 39:125–131

    Google Scholar 

  • González G, Zou X (1999) Earthworm influence on N availability and the growth of Cecropia schreberiana in tropical pasture and forest soils. Pedobiologia 43(6):824–829

    Google Scholar 

  • González G, Seastedt TR, Donato Z (2003) Earthworms, arthropods and plant litter decomposition in aspen (Populus tremuloides) and lodgepole pine (Pinus contorta) forests in Colorado, USA. Pedobiologia 47:863–869

    Google Scholar 

  • González G, Zou X, Borges S (1996) Earthworm abundance and species composition in abandoned tropical croplands: comparisons of tree plantations and secondary forests. Pedobiologia 40:385–391

    Google Scholar 

  • Graham RC, Wood HB (1991) Morphologic development and clay redistribution in lysimeter soils under chaparral and pine. Soil Sci Soc Am J 55:1638–1646

    Article  Google Scholar 

  • Graham RC, Ervin JO, Wood HB (1995) Aggregate stability under oak and pine after four decades of soil development. Soil Sci Soc Am J 59:1740–1744

    Article  CAS  Google Scholar 

  • Hale CM, Frelich LE, Reich PB (2005) Exotic European earthworm invasion dynamics in northern hardwood forests of Minnesota, USA. Ecol Appl 15:848–860

    Google Scholar 

  • Hendrix PF (ed) (1995) Earthworm ecology and biogeography in North America. Lewis Publishers, Boca Raton, FL

    Google Scholar 

  • Hendrix PF, Bohlen P (2002) Ecological assessment of exotic earthworm invasions in North America. Bioscience 52:801–811

    Article  Google Scholar 

  • Hendrix PF, Callaham MA Jr, Lachnicht SL, Blair JM, James SW, Zou X (1999a) Stable isotopic studies of resource utilization by nearctic earthworms (Diplocardia, Oligochaeta) in subtropical savanna and forest ecosystems. Pedobiologia 43:818–823

    Google Scholar 

  • Hendrix PF, Lachnicht SL, Callaham MA Jr, Zou X (1999b) Stable isotopic studies of earthworm feeding ecology in tropical ecosystems of Puerto Rico. Rapid Commun Mass Spectrom 13:1295–1299

    Article  CAS  Google Scholar 

  • Hendrix PF, Mueller BR, Bruce RR, Langdale GW, Parmelee RW (1992) Abundance and distribution of earthworms in relation to landscape factors on the Georgia Piedmont, USA. Soil Biol Biochem 24:1357–1361

    Google Scholar 

  • Hendrix PF, Peterson AC, Beare MH, Coleman DC (1998) Long-term effects of earthworms on microbial biomass nitrogen in coarse and fine textured soils. Appl Soil Ecol 9:375–380

    Article  Google Scholar 

  • Hoogerkamp M, Rogaar H, Eijsackers HJP (1983) Effect of earthworms on grassland on recently reclaimed polder soils in the Netherlands. In: Satchell JE (ed) Earthworm ecology from Darwin to vermiculture. Chapman and Hall, London, pp 85–105

    Google Scholar 

  • James SW (1982) Effects of fire and soil type on earthworm populations in a tallgrass prairie. Pedobiologia 24:37–40

    Google Scholar 

  • James SW (1991) Soil, nitrogen, phosphorus, and organic matter processing by earthworms in tallgrass prairie. Ecology 72:2101–2109

    Article  Google Scholar 

  • James SW, Hendrix PF (2004) Invasion of exotic earthworms into North America and other regions. In Edwards CA (ed) Earthworm ecology, 2nd edn. CRC Press, Boca Raton, FL, pp 75–88

    Google Scholar 

  • Jiménez JJ, Moreno AG, Decaëns T, Lavelle P, Fisher MJ, Thomas RJ (1998) Earthworm communities in native savannas and man-made pastures of the Eastern Plains of Colombia. Biol Fertil Soils 28:101–110

    Article  Google Scholar 

  • Jiménez JJ, Rossi JP, Lavelle P (2001) Spatial distribution of earthworms in acid-soil savannas of the eastern plains of Colombia. Appl Soil Ecol 17:267–278

    Article  Google Scholar 

  • Kalisz P (1993) Native and exotic earthworms in deciduous forest soils of eastern North America. In: Knight BN (ed) Biological pollution: the control and impact of invasive exotic species. Indiana Academy of Science, Indianapolis, IN, pp 93–100

    Google Scholar 

  • Kalisz PJ, Dotson DB (1989) Land-use history and the occurance of exotic earthworms in the mountains of eastern Kentucky. Am Midl Nat 122:288–297

    Article  Google Scholar 

  • Kalisz PJ, Wood HB (1995) Native and exotic earthworms in wildland ecosystems. In: Hendrix P (ed) Earthworm ecology and biogeography in North America. Lewis Publishers, Boca Raton, FL, pp 117–126

    Google Scholar 

  • Lachnicht SL, Hendrix PF, Zou X (2002) Interactive effects of native and exotic earthworms on resource use and nutrient mineralization in a tropical wet forest soil of Puerto Rico. Biol Fertil Soil 36:43–52

    Article  CAS  Google Scholar 

  • Langmaid KK (1964) Some effects of earthworm invasion in virgin podsols. Can J Soil Sci 44:34–37

    Article  Google Scholar 

  • Lavelle P (1978) Les vers de terre de la savanne de Lamto (Côte d’Ivoire): peuplements, populations et functions de l’écosystème, vol 12. Publications Laboratorie Zoologie, ENS, Paris

    Google Scholar 

  • Lavelle P, Pashanasi B (1989) Soil macrofauna and land management in Peruvian Amazonia (Yurimaguas, Loreto). Pedobiologia 33:283–291

    Google Scholar 

  • Lavelle PC, Lattaud D, Barois TI (1995) Mutualism and biodiversity in soils. Plant Soil 170:23–33

    Article  CAS  Google Scholar 

  • Lavelle P, Brussaard L, Hendrix P (eds) (1999) Earthworm management in tropical agroecosystems. CABI Publishing, London

    Google Scholar 

  • Lawson LM (nee Wheeler) (1993) The distribution and abundance of native and introduced earthworms in an area of pasture and native vegetation near Cape Jervis, South Australia. Ph.D. Dissertation, School of Biological Sciences, Flinders University of South Australia

  • Lee KE (1961) Interactions between native and introduced earthworms. Proc NZ Ecol Soc 8:60–62

    Google Scholar 

  • Lee KE (1985) Earthworms, their ecology and relationships with soils and land use. Academic Press, Orlando, FL

    Google Scholar 

  • Liu ZG, Zou XM (2002) Exotic earthworms accelerate plant litter decomposition in a Puerto Rican pasture and a wet forest. Ecol Appl 12:1406–1417

    Google Scholar 

  • Ljungstrom PO (1972) Taxonomical and ecological notes on the earthworm genus Udeina and a requiem for the South African acanthodrilines. Pedobiologia 12:100–110

    Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences and control. Ecol Appl 10:689–710

    Google Scholar 

  • 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 32:351–360

    Article  CAS  Google Scholar 

  • Mele PM, Carter MR (1999a) Species abundance of earthworms in arable and pasture soils in south- eastern Australia. Appl Soil Ecol 12:129–137

    Article  Google Scholar 

  • Mele PM, Carter MR (1999b) Impact of crop management factors in conservation tillage farming on earthworm density, age structure and species abundance in south-eastern Australia. Soil Tillage Res 50:1–10

    Article  Google Scholar 

  • Parmelee RW, Beare MH, Cheng WX, Hendrix PF, Rider SJ, Crossley DA Jr, Coleman DC (1990) Earthworms and enchytraeids in conventional and no-tillage agroecosystems: a biocide approach to assess their role in organic matter breakdown. Biol Fertil Soil 10:1–10

    Google Scholar 

  • Peterson AC, Hendrix PF, Haydu C, Graham RC, Quideau SA (2001) Single-tree influence on earthworms and soil macroarthropods in the southern California chaparral. Pedobiologia 45:509–522

    Article  Google Scholar 

  • Reynolds JW (1995) Status of exotic earthworm systematics and biogeography in North America. In: Hendrix P (ed) Earthworm ecology and biogeography in North America. Lewis Publishers, Boca Raton, FL, pp 1–28

    Google Scholar 

  • Sampedro L, Whalen JK, Shanmugam B, Waheed T (2003) Changes in soil microbial community structure during transit through the earthworm gut. Abstr Soil Ecol Soc 9:69

    Google Scholar 

  • Satchell JE (ed) (1983) Earthworm ecology, from Darwin to vermiculture. Chapman and Hall, London

    Google Scholar 

  • Scheu S, Parkinson D (1994) Effects of invasion of an aspen forest (Canada) by Dendrobaena octaedra (Lumbridicae) on plant growth. Ecology 75:2348–2361

    Article  Google Scholar 

  • Simberloff D (1989) Introduced insects: a biogeographical and systematic perspective. In Mooney HA, Drake JA (eds) Ecology of biological invasions of North America and Hawaii ecological studies 58. Springer-Verlag, NY, pp 3–26

    Google Scholar 

  • Singleton DR, Hendrix PF, Coleman DC, Whitman WB (2003) Identification of uncultured bacteria tightly associated with the intestine of the earthworm Lumbricus rubellus (Lumbricidae; Oligochaeta). Soil Biol Biochem 35:1547–1555

    Article  CAS  Google Scholar 

  • Smith F (1928) An account of changes in the earthworm fauna of Illinois and a description of one new species. Ill Nat Hist Surv Bull 17:347–362

    Google Scholar 

  • Stebbings JH (1962) Endemic-exotic earthworm competition in the American Midwest. Nature 196:905–906

    Article  Google Scholar 

  • Steinberg DA, Pouyat RV, Parmelee RW, Groffman PM (1997) Earthworm abundance and nitrogen mineralization rates along an urban-rural gradient. Soil Biol Biochem 29:427–430

    Article  CAS  Google Scholar 

  • Stockdill SMJ (1982) Effect of introduced earthworms on the productivity of New Zealand pastures. Pedobiologia 24:29–35

    Google Scholar 

  • Williamson M (1996) Biological invasions. Chapman and Hall, London

    Google Scholar 

  • Winsome T (2003) Native and exotic earthworms in a California oak savanna ecosystem. Ph.D. Dissertation, University of Georgia, USA, p 124

  • Winsome T, Epstein L, Hendrix PF, Horwath WR (2006) Habitat quality and interspecific competition between native and exotic earthworm species in a California grassland. Appl Soil Ecol 32:38–53

    Google Scholar 

  • Wood HB, Oliver KL, James SW (1997) Relict Megascolecidae and exclusion of Lumbricidae from basalt-derived soils in southern California. Soil Biol Biochem 29:241–244

    Google Scholar 

  • Zou XM, Bashkin M (1998) Soil carbon accretion and earthworm recovery following revegetation in abandoned sugarcane fields. Soil Biol Biochem 30:825–830

    Article  CAS  Google Scholar 

  • Zou XM, Gonzalez G (1997) Changes in earthworm density and community structure during secondary succession in abandoned tropical pastures. Soil Biol Biochem 29:627–629

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This project was supported by the National Research Initiative of the USDA Co-operative State Research, Education and Extension Service, grant number 2003-35107-13876, and by National Science Foundation grant number 0236276 to the University of Georgia Research Foundation, Inc.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. F. Hendrix.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hendrix, P., Baker, G., Callaham, M. et al. Invasion of exotic earthworms into ecosystems inhabited by native earthworms. Biol Invasions 8, 1287–1300 (2006). https://doi.org/10.1007/s10530-006-9022-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-006-9022-8

Keywords

Navigation