Abstract
Recent studies on earthworm invasion of North American soils report dramatic changes in soil structure, nutrient dynamics and plant communities in ecosystems historically free of earthworms. However, the direct and indirect impacts of earthworm invasions on animals have been largely ignored. This paper summarizes the current knowledge on the impact of earthworm invasion on other soil fauna, vertebrates as well as invertebrates.
Earthworm invasions can have positive effects on the abundance of other soil invertebrates, but such effects are often small, transient, and restricted to habitats with harsh climates or a long history of earthworm co-occurrence with other soil invertebrates. Middens and burrows can increase soil heterogeneity and create microhabitats with a larger pore size, high microbial biomass, and microclimates that are attractive to microand mesofauna. Under harsh climatic conditions, the aggregates formed by earthworms may increase the stability of soil microclimates. Positive effects can also be seen when comminution and mucus secretion increase the palatability of unpalatable organic material for microorganisms which are the main food of most micro- and mesofaunal groups. For larger invertebrates or small vertebrates, invasive earthworms may become important prey, with the potential to increase resource availability.
In the longer-term, the activity of invading earthworms can have a strong negative impact on indigenous faunal groups across multiple trophic levels. Evidence from field and laboratory studies indicates that the restructuring of soil layers, particularly the loss of organic horizons, physical disturbance to the soil, alteration of understory vegetation, and direct competition for food resources, lead directly and indirectly to significant declines in the abundance of soil micro- and mesofauna. Though studies of invasive earthworm impacts on the abundance of larger invertebrates or vertebrates are generally lacking, recent evidence suggests that reduced abundance of small soil fauna and alteration of soil microclimates may be contributing to declines in vertebrate fauna such as terrestrial salamanders. Preliminary evidence also suggests the potential for earthworm invasions to interact with other factors such as soil pollution, to negatively affect vertebrate populations.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsPreview
Unable to display preview. Download preview PDF.
References
Aira M, Monroy F, Dominguez J (2003) Effects of two species of earthworms (Allolobophora spp) on soil systems: a microfaunal and biochemical analysis. Pedobiologia 47:877–881
Anderson JM (1978) Inter-and intra-habitat relationships between woodland Cryptostigmata species diversity and the diversity of soil and litter microhabitats. Oecologia 32:341–348
Bayoumi BM (1978) Significance of the microhabitat on the distribution of oribatid mites in a hornbeam-oak mixed forest. Opuscula Zoologica (Budapest) 15:51–59
Bohlen PJ, Scheu S, Hale C, McLean MA, Migge S, Groffman P, Parkinson D (2004a) Non-native invasive earthworms as agents of change in northern temperate forests. Front Ecol Environ 2:427–435
Bohlen PJ, Groffman PM, Fahey TJ, Fisk MC, Suárez E, Pelletier DM, Fahey RT (2004b) Ecosystem consequences of exotic earthworm invasion of north temperate forests. Ecosystems 7:1–12
Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162:617–631
Bonkowski M, Schaefer M (1997) Interactions between earthworms and soil protozoa: a trophic component in the soil food web. Soil Biol Biochem 29:499–502
Bratton SP (1975) The effect of the European wild boar, Sus scrofa, on grey beech forest in the Great Smoky Mountains. Ecology 56:1356–1366
Brown GG (1995) How do earthworms affect microfloral and faunal community diversity? Plant Soil 170:209–231
Burton TM (1976) An analysis of the feeding ecology of salamanders (Amphibia, Urodela) of the Hubbard Brook Experimental Forest, New Hampshire. J Herpetol 10:187–204
Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310
Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166
Dash MC, Senapati BK, Mishra CC (1980) Nematode feeding by tropical earthworms. Oikos 34:322–325
Dózsa-Farkas K (1978) The ecological importance of microhabitats in the distribution of some Enchytraeidspecies. Pedobiologia 18:366–372
Dunger W (1991) Zur Primärsukzession humiphager Tiergruppen auf Bergbauflächen. Zoologische Jahrbücher Abteilung für Systematik Ökologie und Geographie der Tiere 118:423–447
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 29:265–273
Edwards CA, Bohlen PJ (1996) Biology and ecology of earthworms. Chapman and Hall, New York
Edwards WM, Shipitalo MJ (1998) Consequences of earthworms in agricultural soils: aggregation and porosity. In: Edwards CA (ed) Earthworm ecology. St. Lucie Press, Boca Raton, pp 147–161
Feder ME (1983) Integrating the ecology and physiology of plethodontid salamanders. Herpetologica 39:291–310
Foissner W, Berger H, Xu K, Zechmeister-Boltenstern S (2005) A huge, undescribed soil ciliate (Protozoa: Ciliophora) diversity in natural forest stands of Central Europe. Biod Conserv 14:617–701
Frelich L, Hale C, Scheu S, Holdsworth A, Heneghan LJ, Bohlen PJ, Reich R. Earthworm invasion into previously earthworm-free temperate and boreal forests. Biol Invasions (this issue)
Gates GE (1982) Farewell to North American megadriles. Megadrilogica 4:12–77
Groffman PM, Bohlen PJ, Fist MC, Fahey TJ (2004) Exotic earthworm invasion and microbial biomass in temperate forest soils. Ecosystems 7:45–54
Gutiérrez López M, Ramajo Matesanz M, Jesús Lidón JB and Díaz Cosín DJ (2003) The effect of Hormogaster elisae (Hormogastridae) on the abundance of soil Collembola and Acari in laboratory cultures. Biol Fert Soils 37:231–236
Haimi J, Boucelham M (1991) Influence of a litter feeding earthworm, Lumbricus rubellus, on soil processes in a simulated coniferous forest floor. Pedobiologia 35:247–256
Hale CM (2004) Ecological consequences of exotic invaders: interactions involving European earthworms and native plant communities in hardwood forests (PhD Dissertation). University of Minnesota, St Paul, MN
Hale CM, Frelich LE, Reich PB (2005) Exotic European earthworm invasion dynamics in northern hardwood forests of Minnesota, USA. Ecol Appl 15:848–860
Hamilton WE, Sillman DY (1989) Influence of earthworm middens on the distribution of soil microarthropods. Biol Fert Soils 8:279–284
Hendrix PF, Baker G, Barois I, Callaham M, Damoff G, Fragoso C, Fraser T, Gonzalez G, James S, Lachnicht S, Winsome T and Zou XM. Invasion of exotic earthworms into native earthworm communities. Biol Invasions (this issue)
Heneghan L, Clay C, Brundage C (2002) Rapid decomposition of buckthorn litter may change soil nutrient levels. Ecol Res 20:108–111
Hewitt JE, Thrush SE, Halliday J, Duffy C (2005) The importance of small-scale habitat structure for maintaining beta diversity. Ecology 86:1619–1626
Huhta V, Viberg K (1999) Competitive interactions between the earthworm Dendrobaena octaedra and the enchytraeid Cognettia sphagnetorum. Pedobiologia 43:886–890
Ilieva-Makulec K, Makulec G (2002) Effect of the earthworm Lumbricus rubellus on the nematode community in a peat meadow soil. Eur J Soil Biol 38:195–198
Ireland MP (1977) Lead retention in toads Xenopus laevis fed increasing levels of lead-contaminated earthworms. Environ Poll 12:85–92
Ireland MP (1979) Metal accumulation by the earthworms Lumbricus rubellus, Dendrobaena veneta and Eiseniella tetraedra living in heavy metal polluted sites. Environ Poll 19:201–206
Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386
Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946–1957
Koutika L-S, Didden WAM, Marinissen JCY (2001) Soil organic matter distribution as influenced by enchytraeid and earthworm activity. Biol Fert Soils 33:294–300
Lagerlöf J, Lofs-Holmin A (1987) Relationships between earthworms and soil mesofauna during decomposition of crop residues. In: Striganova BR (ed) Proceedings of the international colloquium of soil zoology, Moscow, pp 377–381
Lee KE, Foster RC (1991) Soil fauna and soil structure. Aust J Soil Res 19:745–775
Loranger G, Ponge JF, Blanchart E, Lavelle P (1998) Impact of earthworms on the diversity of microarthropods in a vertisol (Martinique). Biol Fert Soils 27:21–26
Lowe CN, Butt KR (1999) Interspecific interactions between earthworms: a laboratory-based investigation. Pedobiologia 34:808–817
Lukasiewicz J (1996) Predation by the beetle Carabus granulatus L (Coleoptera, Carabidae) on soil macrofauna in grassland on drained peats. Pedobiologia 40:364–376
MacArthur RH, MacArthur JW (1961) On bird species diversity. Ecology 42:594–598
Maerz JC (2000) Prey Availability and Phenotypic Differences between Local Terrestrial Salamander Populations. PhD Dissertation State University of New York at Binghamton, Binghamton, New York
Maerz JC, Karuzas JM, Madison DM, Blossey B (2005) Introduced invertebrates are important prey for a generalist predator. Diversity and Distributions, 11:83–90
Maerz JC, Madison DM (2000) Environmental variation and territorial behavior in a terrestrial salamander. In: Bruce RC, Jaeger RG, Houck LD (eds) The biology of plethodontid salamanders. Kluwer Academic/Plenum Publishing, New York, New York, USA, pp 395–406
Maraun M, Alphei J, Beste P, Bonkowski M, Buryn R, Migge S, Peter M, Schaefer M, Scheu S (2001) Indirect effects of carbon and nutrient amendment on the soil meso-and microfauna of a beechwood. Biol Fert Soils 34:222–229
Maraun M, Alphei J, Bonkowski M, Buryn R, Migge S, Peter M, Schaefer M, Scheu S (1999) Middens of the earthworm Lumbricus terrestris (Lumbricidae): microhabitats for micro-and mesofauna in forest soil. Pedobiologia 43:276–287
Maraun M, Salamon JA, Schneider K, Schaefer M, Scheu S (2003) Oribatid mite and collembolan diversity, density and community structure in a moder beech forest (Fagus sylvatica): effects of mechanical perturbations. Soil Biol Biochem 35:1387–1394
Maraun M, Scheu S (2000) The structure of oribatid mite communities (Acari, Oribatida): patterns, mechanisms and implications for future research. Ecography 23:374–383
Marinissen JCY, Bok J (1988) Earthworm-amended soil structure: its influence on Collembola populations in grassland. Pedobiologia 32:243–252
Mattsson B (2001) Relationship between multi-scale habitat features and breeding biology of ground nesting birds. MS Thesis, Department of Biology, University of Minnesota Duluth
McLean MA, 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
McLean MA, Parkinson D (1998a) Impacts of the epigeic earthworm Dendrobaena octaedra on oribatid mite community diversity and microarthropod abundances in pine forest floor: a mesocosm study. Appl Soil Ecol 7:125–136
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 8:61–75
McLean MA, Parkinson D (2000a) Introduction of the epigeic earthworm Dendrobaena octaedra changes the oribatid community and microarthropod abundances in a pine forest. Soil Biol Biochem 32:1671–1681
McLean MA, Parkinson D (2000b) 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
McLean MA, Migge-Kleian S, Parkinson D. Earthworm invasions of ecosystems devoid of earthworms: Effects on soil microbes. Biol Invasions (this issue)
Migge S (2001) The effect of earthworm invasion on nutrient turnover, microorganisms and microarthropods in Canadian aspen forest soil. PhD Thesis, Technische Universität Darmstadt, Cuvillier Verlag, Göttingen
Mitchell MJ (1978) Vertical and horizontal distributions of oribatid mites (Acari: Cryptostigmata) in an aspen woodland soil. Ecology 59:516–525
Parkinson D, McLean MA (1998) Impacts of earthworms on the community structure of other biota in forest soils. In: Edwards CA (ed) Earthworm ecology. St Lucie Press, Boca Raton, pp 213–226
Parkinson D, McLean MA, Scheu S (2004) Impacts of earthworms on other biota in forest soils, with some emphasis on cool temperate montane forests. In: Edwards CA (ed) Earthworm ecology. CRC Press, Boca Raton, pp 241–259
Petranka JW, Eldridge ME, Haley KE (1993) Effect of timber harvesting on southern Appalachian salamanders. Conserv Biol 7:363–377
Piearce TG, Phillips MJ (1980) The fate of ciliates in the earthworm gut: an in vitro study. Microbial Ecol 5:313–320
Pop VV, Pop AA. Lumbricid Earthworm Invasion in the Carpathians and some other sites from Romania. Biol Invasions (this issue)
Poser G (1988) Chilopoden als Prädatoren in einem Laubwald. Pedobiologia 31:261–281
Pough FH, Smith EM, Rhodes DH, Collazo A (1987) The abundance of salamanders in forest stands with different histories of disturbance. Forest Ecol Manage 20:1–9
Räty M, Huhta V (2003) Earthworms and pH affect communities of nematodes and enchytraeids in forest soil. Biol Fert Soils 38:52–58
Reinecke AJ, Reinecke SA, Musilbono DE, Chapman A (2000) The transfer of lead (Pb) from earthworms to shrews (Myosorex varius). Arch Environ Contaminat Toxicol 39:392–397
Salmon S (2001) Earthworm excreta (mucus and urine) affect the distribution of springtails in forest soils. Biol Fert Soils 34:304–310
Salmon S, Ponge J-F (1999) Distribution of Heteromurus nitidus (Hexapoda, Collembola) according to soil acidity: interactions with earthworms and predator pressure. Soil Biol Biochem 31:1161–1170
Schaefer M, Schauermann J (1990) The soil fauna of beech forests: comparison between a mull and a moder soil. Pedobiologia 34:299–314
Schaefer M (1999) The diversity of the fauna of two beech forests: some thoughts about possible mechanisms causing the observed patterns. In: Kratochwil A (ed) Biodiversity in ecosystems: principles and case studies of different complexity levels. Kluwer Academic Publishers, Dordrecht, pp 45–64
Scheu S, McLean MA (1993) The earthworm (Lumbricidae) distribution in Alberta (Canada). Megadrilogica 4:175–180
Scheu S, Parkinson D (1994) Effects of earthworms on nutrient dynamics, carbon turnover and microorganisms in soils from cool temperate forests of the Canadian Rocky Mountains—laboratory studies. Appl Soil Ecol 1:113–125
Schrader S, Seibel C (2001) Impact on cultivation management in an agroecosystem on hot spot effects of earthworm middens. Eur J Soil Biol 37:107–111
Shaw C, Pawluk S (1986) Faecal microbiology of Octolasion tyrtaeum, Aporrectodea turgida and Lumbricus terrestris and its relation to the carbon budgets of three artificial soils. Pedobiologia 29:377–389
Singer FJ, Swank WT, Clebsch EEC (1984) Effects of wild pig rooting in a deciduous forest. J Wildlife Manage 48:464–473
Symondson WOC, Glen DM, Erickson DM, Liddell JE, Langdon CJ (2000) Do earthworms help to sustain the slug predator Pterostichus melanarius (Coleoptera: Carabidae) within crops? Investigations using monoclonal antibodies. Mol Ecol 9:1279–1292
Tiunov AV, Bonkowski M, Alphei J, Scheu S (2001) Microflora, protozoa and Nematoda in Lumbricus terrestris burrow walls: a laboratory experiment. Pedobiologia 45:46–60
Tiunov AV, Hale CM, Holdsworth AR, Perel TS. Invasion patterns of Lumbricidae into the previously earthworm-free areas of north-eastern Europe and the western Great Lakes region of North America. Biol Invasions (this issue)
Tiunov AV, Scheu S (2000a) Microfungal communities in soil, litter and casts of Lumbricus terrestris L. (Lumbricidae): a laboratory experiment. Appl Soil Ecol 14:17–26
Tiunov AV, Scheu S (2000b) Microbial biomass, biovolume and respiration in Lumbricus terrestris L. cast material of different age. Soil Biol Biochem 32:265–275
Wanner M, Dunger W (2002) Primary immigration and succession of soil organisms on reclaimed opencast coal mining areas in eastern Germany. Eur J Soil Biol 38:137–143
Wickenbrock L, Heisler C (1997) Influence of earthworm activity on the abundance of Collembola in soil. Soil Biol Biochem 29:517–521
Wolters V (1998) Long-term dynamics of a collembolan community. Appl Soil Ecol 9:221–227
Yeates GW (1981) Soil nematode populations depressed in the presence of earthworms. Pedobiologia 22:191–204
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2006 Springer Science+Business Media B.V.
About this chapter
Cite this chapter
Migge-Kleian, S., McLean, M.A., Maerz, J.C., Heneghan, L. (2006). The influence of invasive earthworms on indigenous fauna in ecosystems previously uninhabited by earthworms. In: Hendrit, P.F. (eds) Biological Invasions Belowground: Earthworms as Invasive Species. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-5429-7_8
Download citation
DOI: https://doi.org/10.1007/978-1-4020-5429-7_8
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-1-4020-5428-0
Online ISBN: 978-1-4020-5429-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)