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Broad and local-scale patterns of exotic earthworm functional groups in forests of National Wildlife Refuges of the Upper Midwest, USA

Abstract

The National Wildlife Refuge System is the world’s largest network of lands set aside specifically for wildlife conservation. For refuge planners and managers tasked with maintaining ecological integrity and wildlife habitat, many uncertainties exist. In forests in the Upper Midwest, for instance, exotic earthworms are impacting ecosystem structure and function, but their community composition and effects on refuges is unknown. We examined the association of earthworm functional group abundance and community composition within upland forests of refuges with broad scale patterns of anthropogenic land use and local scale differences in forest characteristics. Patterns of anthropogenic land cover, including proportion of the land, mean patch area, and largest patch index, were strongly correlated with the biomass of epi-endogeic earthworms. Earthworm community diversity, however, was inversely related to patterns of dominating anthropogenic land cover, and increased under high ratios of natural to anthropogenic lands in the surrounding ecoregion. Within forests, earthworm community composition could be partially explained by variables representing both dispersal opportunities and habitat suitability. In general, heavily-invaded forests had low conifer dominance, high silt content, high basal area, greater amounts of anthropogenic cover within 500 m, and were closer to roads and farther from agriculture. However, the relationship between local forest characteristics and biomass differed greatly among earthworm functional groups and between refuges dominated by natural lands and those dominated by anthropogenic lands. For refuges with high earthworm loads and well developed earthworm communities, managers may be confounded in restoring historic conditions and may need to look at multiple tools, including artificial regeneration, to mitigate for current earthworm effects. In refuges seemingly in earlier stages of earthworm invasion, future planning and management should be tempered by potential effects observed in those refuges in more anthropogenic landscapes.

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References

  1. 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 

  2. Asshoff R, Scheu S, Eisenhauer N (2010) Different earthworm ecological groups interactively impact seedling establishment. Eur J Soil Biol 14:330–334

    Article  Google Scholar 

  3. Bechtold WA, Patterson PL (2005) The enhanced forest inventory and analysis program: national sampling design and estimation procedures. USDA forest service southern research station general technical report SRS-80, Asheville, NC

  4. 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 

  5. 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

    Article  Google Scholar 

  6. Bouché MB (1977) Strategies lombriciennes. In: Lohm U, Persson T (eds) Soil organisms as components of the ecosystem, vol 25. Ecological bulletins (Stockholm). Swedish Natural Science Research Council, Stockholm, pp 122–132

  7. Bouyoucos GJ (1962) Hydrometer method improved for making particle size analyses of soils. Agron J 54:464–465

    Article  Google Scholar 

  8. Cameron EK, Bayne EM, Clapperton MJ (2007) Human-facilitated invasion of exotic earthworms into northern boreal forests. Ecoscience 14:482–490

    Article  Google Scholar 

  9. Cleland DT, Ayers RE, McNab WH, Jensen ME, Bailey RG, King T, Russell WE (1997) National hierarchical framework of ecological units. In: Boyce MS, Haney A (eds) Ecosystem management: applications for sustainable forest and wildlife resources. Yale University Press, New Haven

    Google Scholar 

  10. Corace RG III, Shartell LM, Schulte LA, Brininger WL Jr, McDowell MKD, Kashian DM (2012) An ecoregional context for forest management on National Wildlife Refuges of the Upper Midwest, USA. Environ Manag 49:359–371

    Article  Google Scholar 

  11. Edwards CA, Bohlen PJ (1996) Biology and Ecology of Earthworms. Chapman & Hall, London 426

    Google Scholar 

  12. Flinn KM, Marks PL (2007) Agricultural legacies in forest environments: tree communities, soil properties, and light availability. Ecol Appl 17:452–463

    Article  PubMed  Google Scholar 

  13. 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

    Article  Google Scholar 

  14. George TL, Zack S (2001) Spatial and temporal considerations for restoring wildlife, habitat. Restor Ecol 9:272–279

    Article  Google Scholar 

  15. Griffith B, Scott JM, Adamcik R, Ashe D, Czech B, Fischman R, Gonzalez P, Lawler J, McGuire AD, Pidgorna A (2009) Climate change adaptation for the U.S. National Wildlife Refuge System. Environ Manag 44:1043–1052

    Article  Google Scholar 

  16. Gundale MJ, Jolly WM, Deluca TH (2005) Susceptibility of a northern hardwood forest to exotic earthworm invasion. Conserv Biol 19:1075–1083

    Article  Google Scholar 

  17. Gunn A (1992) The use of mustard to estimate earthworm populations. Pedobiologia 36:65–67

    Google Scholar 

  18. Hale CM (2008) Evidence for human-mediated dispersal of exotic earthworms: support for exploring strategies to limit further spread. Mol Ecol 17:1165–1169

    Article  PubMed  Google Scholar 

  19. Hale CM, Frelich LE, Reich PB (2004) Allometric equations for estimation of ash-free dry mass from length measurements for selected European earthworm species (Lumbricidae) in the western Great Lakes region. Am Midl Nat 15:179–185

    Article  Google Scholar 

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

    Article  Google Scholar 

  21. Hale CM, Frelich LE, Reich PB (2006) Changes in hardwood forest understory plant communities in response to European earthworm invasions. Ecology 87:1637–1649

    Article  PubMed  Google Scholar 

  22. Heimpel GE, Frelich LE, Landis DA, Hopper KR, Hoelmer KA, Sezen Z, Asplen MK, Wu K (2010) European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biol Invasions 12:2913–2931

    Article  Google Scholar 

  23. Hendriksen NB (1990) Leaf litter selection by detritivore and geophagous earthworms. Biol Fertil Soils 10:17–21

    Google Scholar 

  24. Hendrix PF, Bohlen PJ (2002) Exotic earthworm invasions in North America: ecological and policy implications. Bioscience 52:801–811

    Article  Google Scholar 

  25. Holdsworth AR, Frelich LE, Reich PB (2007a) Effects of earthworm invasion on plant species richness in northern hardwood forests. Conserv Biol 21:997–1008

    Article  PubMed  Google Scholar 

  26. Holdsworth AR, Frelich LE, Reich PB (2007b) Regional extent of an ecosystem engineer: earthworm invasion in northern hardwood forests. Ecol Appl 17:1666–1677

    Article  PubMed  Google Scholar 

  27. Hopfensperger KN, Leighton GM, Fahey TJ (2011) Influence of invasive earthworms on above and belowground vegetation in a northern hardwood forest. Am Midl Nat 166:53–62

    Article  Google Scholar 

  28. Lavelle P (1997) Faunal activities and soil processes: adaptive strategies that determine ecosystem function. In: Bergon M, Fitter AH (eds) Advances in ecological research. Academic Press, San Diego, pp 93–122

    Google Scholar 

  29. Lawrence AP, Bowers MA (2002) A test of the ‘hot’ mustard extraction method of sampling earthworms. Soil Biol Biochem 34:549–552

    CAS  Article  Google Scholar 

  30. Lodge DM, Shrader-Frechette K (2003) Nonindigenous species: ecological explanation, environmental ethics, and public policy. Conserv Biol 17:31–37

    Article  Google Scholar 

  31. 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

    Article  PubMed  Google Scholar 

  32. Madritch MD, Lindroth RL (2008) Removal of invasive shrubs reduces exotic earthworm populations. Biol Invasions 11:663–671

    Article  Google Scholar 

  33. 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

    Article  PubMed  Google Scholar 

  34. McCune B, Mefford MJ (1999) PC-ORD. Multivariate analysis of ecological data. Version 5.0 Gleneden Beach. MjM Software, OR

  35. McGarigal K, Cushman SA, Neeland MC, Ene E (2002) FRAGSTATS: spatial pattern analysis program for categorical maps. University of Massachusetts, Amherst

    Google Scholar 

  36. Meretsky VJ, Fischman RL, Karr JR, Ashe DA, Scott JM, Noss RF, Schroeder RL (2006) New directions in conservation for the National Wildlife Refuge System. Bioscience 56:135–143

    Article  Google Scholar 

  37. Nieminen M, Ketoja E, Mikola J, Terhivuo J, Siren T, Nuutinen V (2011) Local land use effects and regional environmental limits on earthworm communities in Finnish arable landscapes. Ecol Appl 21:3162–3177

    Article  Google Scholar 

  38. Nuzzo VA, Maerz JC, Blossey B (2009) Earthworm invasion as the driving force behind plant invasion and community change in northeastern American forests. Conserv Biol 23:966–974

    Article  PubMed  Google Scholar 

  39. Petrillo HA, Corace RG III (2011) Rapid ecological assessment of forests in the Laurentian Mixed Forest-Great Lakes Coastal biological network, Midwest Region, National Wildlife Refuge System, US Fish and Wildlife Service: field manual. Seney NWR for the Midwest Regional Office, Fort Snelling

    Google Scholar 

  40. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  41. 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

    Article  Google Scholar 

  42. 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

    Article  Google Scholar 

  43. Scheu S (2003) Effects of earthworms on plant growth: patterns and perspectives. Pedobiologia 47:846–856

    Google Scholar 

  44. Schroeder RL, Holler JI, Taylor JP (2004) Managing National Wildlife Refuges for historic and nonhistoric conditions: determining the role of the refuge in the ecosystem. Nat Resour J 44:1185–1210

    Google Scholar 

  45. Scott JM, Loveland T, Gergely K, Strittholt J, Staus N (2004) National Wildlife Refuge System:ecological context and integrity. Nat Resour J 44:1041–1066

    Google Scholar 

  46. Shartell LM, Nagel LM, Storer AJ (2011) Multi-criteria risk model for garlic mustard (Alliaria petiolata) in Michigan’s Upper Peninsula. Am Midl Nat 165:116–127

    Article  Google Scholar 

  47. Smith J, Potts SG, Woodcock BA, Eggleton P (2008) Can arable field margins be managed to enhance their biodiversity, conservation and functional value for soil macrofauna? J Appl Ecol 45:269–278

    Article  Google Scholar 

  48. Suarez ER, Pelletier DM, Fahey TJ, Groffman PM, Bohlen PJ, Fisk MC (2003) Effects of exotic earthworms on soil phosphorus cycling in two broadleaf temperate forests. Ecosystems 7:28–44

    Article  Google Scholar 

  49. Suarez ER, Fahey TJ, Yavitt JB, Groffman PM, Bohlen PJ (2006) Patterns of litter disappearance in a northern hardwood forest invaded by exotic earthworms. Ecol Appl 16:154–165

    Article  PubMed  Google Scholar 

  50. Subler S, Baranski CM, Edwards CA (1997) Earthworm additions increased short-term nitrogen availability and leaching in two grain-crop agroecosystems. Soil Biol Biochem 29:413–421

    CAS  Article  Google Scholar 

  51. Tiunov AV, Hale CM, Holdsworth AR, Vsevolodova-Perel TS (2006) Invasion patterns of Lumbricidae into the previously earthworm-free areas of northeastern Europe and the western Great Lakes region of North America. Biol Invasions 8:1223–1234

    Article  Google Scholar 

  52. United States Geological Survey (USGS) (2011) National Land Cover Database 2006. Multi-resolution land characteristics (MRLC) consortium. http://www.mrlc.gov/nlcd2006_update

  53. Waddell KL (2002) Sampling coarse woody debris for multiple attributes in extensive resource inventories. Ecol Indic 1:139–153

    Article  Google Scholar 

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Acknowledgments

Funding was provided by the U.S. Fish and Wildlife Service Midwest Region, the refuges of study, Seney Natural History Association, Michigan Technological University, and Wayne State University. Forest structure and composition data were provided by Holly Petrillo, University of Wisconsin-Steven’s Point. The authors appreciate the support of colleagues in the NWRS, particularly Patricia Heglund (Regional Biologist), Mark Vaniman and Laurie Tansy (Seney NWR), Ron Huffman (Ottawa NWR), Michelle Vander Haar (Shiawassee NWR), Michelle McDowell (Rice Lake NWR), Wayne Brininger (Tamarac NWR), and Wendy Woyczik (Horicon NWR). We would also like to thank those who assisted: Ashlee Baker, Alina Neel, Dakota Hunter, Joe May, Max Henschell, Adam Komar, John Otterbein, Erin Marchand, and other NWRS staff and volunteers. The authors thank the anonymous reviewer for their helpful comments and suggestions that improved this manuscript. The findings and conclusions in this article are those of the authors and do not necessarily represent the views of the U.S. Fish and Wildlife Service.

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Correspondence to Lindsey M. Shartell.

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Shartell, L.M., Corace, R.G., Storer, A.J. et al. Broad and local-scale patterns of exotic earthworm functional groups in forests of National Wildlife Refuges of the Upper Midwest, USA. Biol Invasions 17, 3591–3607 (2015). https://doi.org/10.1007/s10530-015-0982-4

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Keywords

  • Invasive species
  • Great Lakes Region
  • Anthropogenic land cover
  • Forest management