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Invasions of non-native earthworms related to population declines of ground-nesting songbirds across a regional extent in northern hardwood forests of North America

Abstract

Non-native invasive earthworms (Lumbricus spp.) substantially change previously earthworm-free hardwood forests of North America by consuming the leaf litter layer, reducing cover and richness of herbaceous plants, and increasing dominance of sedges and grasses. These changes have been associated with reduced density of Ovenbirds (Seiurus aurocapilla) and Hermit Thrushes (Catharus guttatus) in 10–20 ha forest stands, and with reduced Ovenbird nesting success. Whether earthworms reduce songbird populations across a regional extent is unclear. We investigated relationships among Lumbricus, vegetation structure, landscape patterns of forest cover, and density of four ground-nesting songbird species at points scattered across the Chequamegon-Nicolet (Wisconsin) and Chippewa (Minnesota) National Forests, USA. In both national forests, Ovenbird density was significantly lower at invaded points than Lumbricus-free points, but only in sugar maple (Acer saccharum) and sugar maple/basswood (Tilia americana) (hereafter, maple-basswood) woodlands. Density of the Hermit Thrush, Black-and-white Warbler (Mniotilta varia), and Veery (Catharus fuscescens) did not differ in relation to Lumbricus. In maple-basswood forests, Lumbricus biomass was the best predictor of Ovenbird density, with greater biomass associated with reduced density. Vegetation structure and landscape pattern variables received weak support as density predictors. Across all forest types, Ovenbird density was most strongly related to forest cover within 500 and 1,000 m radii. Our results suggest that earthworm invasions may pose a regional threat to Ovenbirds within maple-basswood forests of the U.S. northern Midwest.

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References

  • 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 

  • Bohlen PJ, Scheu S, Hale CM, McLean MA, Migge S, Groffman PM, Parkinson D (2004) Non-native invasive earthworms as agents of change in northern temperate forests. Front Ecol Environ 2:427–435

    Article  Google Scholar 

  • Burke DM, Nol E (1998) Influence of food abundance, nest site habitat, and forest fragmentation on breeding Ovenbirds. Auk 115:96–104

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Cameron EK, Bayne EM (2009) Road age and its importance in earthworm invasion of northern boreal forests. J Appl Ecol 46:28–36

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Collins SL (1983) Geographic variation in habitat structure for the wood warblers in Maine and Minnesota. Oecologia 59:246–252

    Article  Google Scholar 

  • Crawford HS, Hooper RG, Titterington RW (1981) Songbird population response to silvicultural practices in central Appalachian hardwoods. J Wildl Manag 45:680–692

    Article  Google Scholar 

  • Crowl TA, Crist TP, Parmenter RR, Belovsky GB, Lugo AE (2008) The spread of invasive species and infectious disease as drivers of ecosystem change. Front Ecol Environ 6:238–246

    Article  Google Scholar 

  • Donovan TM, Lamberson RH, Kimber A, Thompson FR III, Faaborg J (1995) Modeling the effects of habitat fragmentation on source and sink demography of neotropical migrant birds. Conserv Biol 9:1396–1407

    Article  Google Scholar 

  • Etterson MA, Niemi GJ, Danz NP (2009) Estimating the effects of detection heterogeneity and overdispersion on trends estimated from avian point counts. Ecol Appl 19:2049–2066

    PubMed  Article  Google Scholar 

  • Flaspohler DJ, Temple SA, Rosenfield RN (2001) Effects of forest edges on Ovenbird demography in a managed forest landscape. Conserv Biol 15:173–183

    Google Scholar 

  • Fox VL, Buehler CP, Byers CM, Drake SE (2010) Forest composition, leaf litter, and songbird communities in oak- vs. maple-dominated forests in the eastern United States. For Ecol Manag 259:2426–2432

    Article  Google Scholar 

  • Frelich LE, Reich PB (2009) Will environmental changes reinforce the impact of global warming on the prairie-forest border of North America? Front Ecol Environ 8:371–378

    Article  Google Scholar 

  • 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 

  • Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19:470–474

    PubMed  Article  Google Scholar 

  • Hale C (2007) Earthworms of the Great Lakes. Kollath and Stensaas, Duluth

    Google Scholar 

  • Hale CM, Reich PB, Frelich LE (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 Mid Nat 151:179–185

    Article  Google Scholar 

  • Hale CM, Frelich LE, Reich PB, Pastor J (2005) Effects of European earthworm invasion on soil characteristics in northern hardwood forests of Minnesota, USA. Ecosystems 8:911–927

    Article  CAS  Google Scholar 

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

    PubMed  Article  Google Scholar 

  • 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 155:508–519

    Article  Google Scholar 

  • Hanowski JM, Lind J, Danz N, Niemi G, Jones J (2005) Regional breeding bird monitoring in western Great Lakes national forests. In: Ralph CJ, Rich TD (eds) Bird conservation implementation and integration in the Americas. Proceedings of the third international partners in flight conference, vol 2, Asilomar, March 2002, pp 974–981. U.S. Forest Service General Technical Report PSW-GTR-191, Albany

  • Haskell DG (2000) Effects of forest roads on macroinvertebrate soil fauna of the southern Appalachian Mountains. Conserv Biol 14:57–63

    Article  Google Scholar 

  • Heneghan L, Steffen J, Fagen F (2007) Interactions of an introduced shrub and introduced earthworms in an Illinois urban woodland: impact on leaf litter decomposition. Pedobiologia 50:543–551

    Article  Google Scholar 

  • Hochachka WM, Dhondt AA (2000) Density-dependent decline of host abundance resulting from a new infectious disease. Proc Natl Acad Sci USA 97:5303–5306

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  • Holdsworth AR, Frelich LE, Reich PB (2008) Litter decomposition in earthworm-invaded northern hardwood forests: role of invasion degree and litter chemistry. Ecoscience 15:536–544

    Article  Google Scholar 

  • Homer CJ, Dewitz J, Fry M, Coan M, Hossain N, Larson C, Herold N, McKerrow A, VanDriel JN, Wickham J (2007) Completion of the 2001 National Land Cover Database for the conterminous United States. Photogram Eng Remote Sens 73:337–341

  • James FC (1971) Ordination of habitat relationships among breeding birds. Wilson Bull 83:213–236

    Google Scholar 

  • Kricher JC (1995) Black-and-white Warbler (Mniotilta varia). In: Poole A (ed) The birds of North America online. Cornell Laboratory of Ornithology, Ithaca. http://bna.birds.cornell.edu.ezp2.lib.umn.edu/bna/species/158. Accessed Feb 2012

  • LaDeau SL, Kilpatrick AM, Marra PP (2007) West Nile virus emergence and large-scale declines of North American bird populations. Nature 447:710–714

    PubMed  Article  CAS  Google Scholar 

  • Larson ER, Kipfmueller KF, Hale CM, Frelich LE, Reich PB (2010) Tree rings detect earthworm invasions and their effects in northern hardwood forests. Biol Invasions 12:1053–1066

    Article  Google Scholar 

  • Lawrence B, Fisk MC, Fahey TJ, Suarez ER (2003) Influence of nonnative earthworms on mycorrhizal colonization of sugar maple (Acer saccharum). New Phytol 157:145–153

    Article  Google Scholar 

  • Lloyd P, Martin TE, Redmond RL, Langner U, Hart MM (2005) Linking demographic effects of habitat fragmentation across landscapes to continental source-sink dynamics. Ecol Appl 15:1504–1514

    Article  Google Scholar 

  • Loss SR, Blair RB (2011) Reduced density and nest survival of ground-nesting songbirds in relation to earthworm invasions in northern hardwood forests. Conserv Biol 25:983–992

    Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FM (2000) Biotic invasions: causes epidemiology, global consequences, and control. Ecol Appl 10:678–689

    Article  Google Scholar 

  • Maerz JC, Karuzas JM, Madison DM, Blossey B (2005) Introduced invertebrates are important prey for a generalist predator. Divers Distrib 11:83–90

    Article  Google Scholar 

  • 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

    PubMed  Article  Google Scholar 

  • Manolis JC, Andersen DE, Cuthbert FJ (2000) Patterns in clearcut edge and fragmentation effect studies in northern hardwood-conifer landscapes: retrospective power analysis and Minnesota results. Wildl Soc B 28:1088–1101

    Google Scholar 

  • Marinissen JCH, van den Bosch F (1992) Colonization of new habitats by earthworms. Oecologia 91:371–376

    Article  Google Scholar 

  • Mattsson BJ, Niemi GJ (2006) Factors influencing predation on Ovenbird (Seiurus aurocapilla) nests in northern hardwoods: interactions across spatial scales. Auk 123:82–96

    Article  Google Scholar 

  • Miles PD, Brand GJ, Mielke MA (2004) Minnesota’s Forest Resources 2004. North Central Research Station Resource Bulletin NC-262, St. Paul

  • Mitchell MS, Lancia RA, Gerwin JA (2001) Using landscape-level data to predict the distribution of birds on a managed forest: effects of scale. Ecol Appl 11:1692–1708

    Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  • 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

    Google Scholar 

  • Robinson SK, Thompson FR III, Donovan TM, Whitehead DR, Faaborg J (1995) Regional forest fragmentation and the nesting success of migratory birds. Science 267:1987–1990

    PubMed  Article  CAS  Google Scholar 

  • Rodewald AD, Yahner RH (2000) Influence of landscape and habitat characteristics on Ovenbird pairing success. Wilson Bull 112:238–242

    Article  Google Scholar 

  • Sauer JR, Hines JE, Fallon JE, Pardieck KL, Ziolkowski DJ Jr, Link WA (2011) The North American Breeding Bird Survey, Results and Analysis 1966–2009, Version 3.23.2011 USGS Patuxent Wildlife Research Center, Laurel, MD. Accessed Dec 2011

  • Smith KG (1977) Distribution of summer birds along a forest moisture gradient in an Ozark watershed. Ecology 58:810–819

    Article  Google Scholar 

  • Smith TM, Shugart HH (1987) Territory size variation in the Ovenbird: the role of habitat structure. Ecology 68:695–704

    Article  Google Scholar 

  • Smith KM, Keeton WS, Donovan TM, Mitchell B (2008) Stand-level forest structure and avian habitat: scale dependencies in predicting occurrence in a heterogeneous forest. For Sci 54:36–46

    Google Scholar 

  • 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. Landscape Ecol 21:297–306

    Article  Google Scholar 

  • Sutherland WJ, Barsley S, Bennun L, Clout M, Cote IM, Depledge MH, Dicks LV, Dobson AP, Fellman L, Fleishman E, Gibbons DW, Impey AJ, Lawton JH, Lickorish F, Lindenmayer DB, Lovejoy TE, Mac Nally R, Madgwick J, Peck LS, Pretty J, Prior SV, Redford KH, Scharlemann JPW, Spalding M, Watkinson AR (2010) Horizon scan of global conservation issues for 2011. Trends Ecol Evol 26:10–16

    Google Scholar 

  • Temple SA, Cary JR (1988) Modeling dynamics of habitat-interior bird populations in fragmented landscapes. Conserv Biol 4:340–347

    Article  Google Scholar 

  • Thomas L, Buckland ST, Rexstad EA, Laake JL, Strindberg S, Hedley SL, Bishop JRB, Marques TA, Burnham KP (2010) Distance software: design and analysis of distance sampling surveys for estimating population size. J Appl Ecol 47:5–14

    Google Scholar 

  • Thompson FR III, Capen DE (1988) Avian assemblages in seral stages of a Vermont forest. J Wildl Manag 52:771–777

    Article  Google Scholar 

  • Van Horn MA (1990). The relationship between edge and the pairing success of the Ovenbird (Seiurus aurocapillus). MS Thesis, University of Missouri

  • Van Horn MA, Donovan TM (1994) Ovenbird (Seiurus aurocapilla). In: Poole A (ed) The birds of North America Online. Cornell Laboratory of Ornithology, Ithaca. http://bna.birds.cornell.edu/bna/species/088. doi:10.2173/bna.88. Accessed Feb 2012

  • Van Horn MA, Gentry RM, Faaborg J (1995) Patterns of Ovenbird (Seiurus aurocapilla) pairing success in Missouri forest tracts. Auk 112:98–106

    Google Scholar 

  • Vissage JS, Brand GJ, Mielke ME (2004). Wisconsin’s Forest Resources in 2004. North Central Research Station Resource Bulletin NC-237. St. Paul

  • Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States. Bioscience 48:607–661

    Article  Google Scholar 

  • Woudenberg SW, Conkling BL, O’Connell BM, LaPoint EB, Turner JA, Waddell KL (2010). General Technical Report RMRS-GTR-245. Rocky Mountain Research Station, U.S. Forest Service, U.S. Department of Agriculture, Fort Collins

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Acknowledgments

Research was funded by the American Museum of Natural History, Bell Museum of Natural History, Dayton-Wilkie Foundation, The Explorers Club, Minnesota Ornithologists’ Union, U.S. Department of Agriculture (Chequamegon-Nicolet National Forest), and Wisconsin Society for Ornithology. S.R.L. was supported by a University of Minnesota Graduate School Fellowship and National Science Foundation Interdisciplinary Graduate Education and Research Traineeship: Risk Analysis for Introduced Species/Genotypes (NSF-DGE-0653827). We thank C. Hakseth, L. Raab, and K. Bennett for earthworm sampling assistance, J. Bednar, P. Dolan-Linne, A. Bracey, J. Bailley, C. Lapin, D. Ostrowski, H. Seeland, and J. Smith for conducting bird surveys, and A. Grinde for compiling vegetation and bird data. We thank L.E. Frelich, D.E. Andersen, P. Bolstad, A. Holdsworth, and C. Hale for guiding the study’s development. Work was conducted with appropriate permits and approval by the University of Minnesota Institutional Animal Care and Use Committee.

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Correspondence to Scott R. Loss.

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Loss, S.R., Niemi, G.J. & Blair, R.B. Invasions of non-native earthworms related to population declines of ground-nesting songbirds across a regional extent in northern hardwood forests of North America. Landscape Ecol 27, 683–696 (2012). https://doi.org/10.1007/s10980-012-9717-4

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Keywords

  • Hermit Thrush
  • Invasive earthworms
  • Lumbricus
  • Minnesota, USA
  • Ovenbird
  • Wisconsin, USA