Abstract
Identifying influences of earthworm invasion and distribution in the northern Great Lakes is an important step in predicting the potential extent and impact of earthworms across the region. The occurrence of earthworm signs, indicating presence in general, and middens, indicating presence of Lumbricus terrestris exclusively, in the Huron Mountains located in the Upper Peninsula of Michigan were modeled using generalized linear models and stepwise regression to identify important environmental variables. Models were then applied to earthworm occurrence data from Seney National Wildlife Refuge, also located in the Upper Peninsula of Michigan to validate results. Occurrence of earthworm signs was associated with high soil pH, high basal area of earthworm preferred overstory species, and north facing aspects. Middens of L. terrestris were associated with high soil pH, high basal area of preferred species, and close proximity to roads. The resulting model for L. terrestris was incorporated into a geographic information system (GIS) to map the expected distribution, both current and potential, across the study area. Results indicate that L. terrestris has not yet fully saturated its potential habitat, as it is currently found close to roads and has yet to establish in most interior forests sampled. Comparing field measured data to GIS layers revealed limitations in the precision of publicly available spatial data layers that should be addressed in future attempts to predict the extent of earthworm invasion across the larger Great Lakes region. However, within the Huron Mountains, it is predicted that the distribution of L. terrestris will cover, at minimum, 41 % of the area.
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References
Barley KP (1961) Abundance of earthworms in agricultural land and their possible significance in agriculture. Adv Agron 13:249–268
Bohlen PJ, Groffman PM, Fahey TJ, Fisk MC, Suarez E, Pelletier DM, Fahey RT (2004) Ecosystem consequences of exotic earthworm invasion of north temperate forests. Ecosystems 7:1–12
Cameron EK, Bayne EM, Coltman DW (2008) Genetic structure of invasive earthworms Dendrobaena octaedra in the boreal forest of Alberta: insights into introduction mechanisms. Mol Ecol 17:1189–1197
Clapperton MJ, Baker GH, Fox CA (2008) Earthworms. In: Carter MR, Gregorich EG (eds) Soil sampling and methods of analysis, 2nd edn. CRC Press, Boca Raton, pp 427–444
Dormann CF (2007) Assessing the validity of autologistic regression. Ecol Model 207:234–242
Edwards CA, Bohlen PJ (1996) The biology and ecology of earthworms, 3rd edn. Chapman and Hall, London
Environmental Systems Research Institute (ESRI) (2011) ArcGIS Desktop: Release 10. Environmental Systems Research Institute, Redlands
Frelich LE, Hale CM, Scheu S, Holdsworth AR, Heneghan L, Bohlen PJ, Reich PB (2006) Earthworm invasion into previously earthworm-free temperate and boreal forests. Biol Invasions 8:1235–1245
Gundale MJ, Jolly WM, DeLuca TH (2005) Susceptibility of a northern hardwood forest to exotic earthworm invasion. Con Biol 19:1075–1083
Hale CM (2008) Evidence for human-mediated dispersal of exotic earthworms: support for exploring strategies to limit further spread. Mol Ecol 17:1165–1169
Hale CM, Frelich LE, Reich PB (2005) Exotic earthworm invasion dynamics in northern hardwood forests of Minnesota, USA. Ecol Appl 15:848–860
Hale CM, Frelich LE, Reich PB, Pastor J (2008) Exotic earthworm effects on hardwood forest floor, nutrient availability and native plants: a mesocosm study. Oecologia 155:509–518
Hanley JA, McNeil BJ (1982) The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143:839–843
Hendriksen NB (1990) Leaf litter selection by detritivore and geophagous earthworms. Biol Fertil Soils 10:17–21
Hendrix PF, Bohlen PJ (2002) Exotic earthworm invasions in North America: ecological and policy implications. Bioscience 52:801–811
Holdsworth AR, Frelich LE, Reich PB (2007) Regional extent of an ecosystem engineer: earthworm invasion in northern hardwood forests. Ecol Appl 17:1666–1677
Holmstrup M, Westh P (1995) Effects of dehydration on water relations and survival of lumbricid earthworm egg capsules. J Comp Physio 165:377–383
James SW, Hendrix PF (2004) Invasion of exotic earthworms into North America and other regions. In: Edwards CA (ed) Earthworm ecology. CRC Press, Boca Raton, pp 75–88
Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386
Karberg NJ, Lilleskov EA (2009) White-tailed deer (Odocoileus virginianus) fecal pellet decomposition is accelerated by the invasive earthworm Lumbricus terrestris. Biol Invasions 11:761–767
Lee KE (1985) Earthworms: their ecology and relationships with soils and land use. Academic Press, Sydney
Loss SR, Blair RB (2011) Reduced density and nest survival of ground-nesting songbirds relative to earthworm invasions in northern hardwood forests. Conserv Biol 25:983–992
Maerz JC, Nuzzo VA, Blossey B (2009) Declines in woodland salamander abundance associated with non-native earthworm and plant invasions. Conserv Biol 23:975–981
Michigan Department of Natural Resources (MI DNR) (2001) Michigan 2001 integrated forest monitoring, assessment, and prescription (IFMAP) gap land cover dataset. http://www.mcgi.state.mi.us/mgdl
Natural Resources Conservation Service (NRCS) (2006) Soil Survey geographic (SSURGO) database. http://soildatamart.nrcs.usda.gov
Pearce J, Ferrier S (2000) Evaluating the predictive performance of habitat models developed using logistic regression. Ecol Model 133:225–245
Petrillo HA, Corace RG III (2011) Rapid ecological assessment of forests in the Laurentian mixed forest-Great Lakes coastal biological network. National Wildlife Refuge System, US Fish and Wildlife Service, Midwest Region
Reich PB, Oleksyn J, Modrzynski J, Mrozinski P, Hobbie SE, Eissenstat DM, Chorover J, Chadwick OA, Hale CM, Tjoelker MG (2005) Linking litter calcium, earthworms and soil properties: a common garden test with 14 tree species. Ecol Lett 8:811–818
Sackett TE, Smith SM, Basiliko N (2012) Exotic earthworm distribution in a mixed-use northern temperate forest region: influence of disturbance type, development age, and soils. Can J For Res 42:375–381
Schaetzl RJ, Krist FJ, Stanley K, Hupy CM (2009) The natural soil drainage index: an ordinal estimate of long-term soil wetness. Phys Geogr 30:383–409
Scheu S, Parkinson D (1994) Effects of earthworms on nutrient dynamics, carbon turnover and microorganisms in soils from cold temperate forests of the Canadian Rocky Mountains—laboratory studies. Appl Soil Ecol 1:113–125
Schwert DP, Dance KW (1979) Earthworm cocoons as a drift component in a southern Ontario stream. Can Field Nat 93:180–183
Shartell LM (2012) Invasion patterns of emerald ash borer and European earthworms in forested ecosystems. Dissertation, Michigan Technological University
Shartell LM, Corace RG III, Storer AJ (2012) Exotic earthworm communities within upland deciduous forests of National Wildlife Refuges in the Upper Midwest. J Fish Wildl Manag 3:332–340
Simpson TB, Stuart PE, Barnes BV (1990) Landscape ecosystems and cover types of the reserve area and adjacent lands of the Huron Mountain Club. Huron Mountain Wildlife Foundation, Big Bay
State of Michigan (2009) Michigan Geographic Data Library. Center for Geographic Information, Department of Information Technology. http://mcgi.state.mi.us/mgdl
Suarez ER, Tierney GL, Fahey TJ, Fahey R (2006) Exploring patterns of exotic earthworm distribution in a temperate hardwood forest in south-central New York, USA. Landsc Ecol 21:297–306
R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://R-project.org
Thomas GW (1996) Soil pH and soil acidity. In: Sparks DL (ed) Methods of soil analysis, part 3—chemical methods. Soil Science Society of America, Madison, pp 475–490
Tiunov AV, Hale CM, Holdsworth AR, Vsevolodova-Peral TS (2006) Invasion patterns of Lumbricidae into previously earthworm-free areas of northeastern Europe and the western Great Lakes region of North America. Biol Invasions 8:1223–1234
United States Geological Survey (USGS) (2011) National Land Cover Database 2006. Multi-resolution land characteristics (MRLC) Consortium. http://www.mrlc.gov/nlcd2006_update
Yatso K, Lilleskov E (unpublished) Effects of tree litter type and soil type on growth of an introduced earthworm (Lumbricus terrestris): implications for invasion dynamics
Acknowledgments
Funding for this work was provided by the U.S. Forest Service, Northern Research Station. The authors thank Kerry Woods and the Huron Mountain Wildlife Foundation for initial support of earthworm work in the Huron Mountains, and for access to field sites. The authors thank Karl Romanowicz and Lynette Potvin for field data collection, and Ann Maclean, Nancy Auer, and three anonymous reviewers for comments on earlier versions of this manuscript.
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Shartell, L.M., Lilleskov, E.A. & Storer, A.J. Predicting exotic earthworm distribution in the northern Great Lakes region. Biol Invasions 15, 1665–1675 (2013). https://doi.org/10.1007/s10530-012-0399-2
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DOI: https://doi.org/10.1007/s10530-012-0399-2