Skip to main content

Invasive lumbricid earthworms in northeastern North American forests and consequences for leaf-litter fauna

Biological Invasions volume 21, pages 2081–2093 (2019)Cite this article

Abstract

Colonization of North America by exotic earthworms has been implicated in undesirable changes in soil structure, nutrient cycling, and biodiversity. Invasion by putative European earthworms has a long history in northeastern North America. Partly for this reason, factors that may be continuing to facilitate expansion of earthworm distributions and the consequences of earthworm spread in the Northeast get relatively little attention. We sampled earthworms and environmental attributes at 85 sites in central New York. We additionally sampled leaf-litter fauna at 25 of these sites. We detected no earthworms at 27 of 71 forested sites (38%). Forested sites without detectable earthworm populations were farther from the nearest road and had soils of lower pH than forested sites with earthworms. Proximity of the nearest road was strongly associated with earthworm diversity and abundance, and earthworm biomass was highest in low, moist areas. We found a strong, negative relationship between the biomass of earthworms and abundance of invertebrates in the litter layer. This association was likely mediated by the abundance of organic litter, which was lower at sites with high biomass of earthworms. Sites with only the putative native Bimastos (Dendrodrilus) rubidus had a high mass of leaf litter and large numbers of leaf litter animals despite high densities of this species. We believe that there is potential for further expansion of European earthworm taxa in the Northeast and strong evidence for negative consequences of this expansion. Additional regulations on activities that promote introduction may be necessary.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

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 

  • Alerich CL, Drake DA (1995) Forest statistics for New York: 1980 and 1993. Resource Bulletin NE-132. USDA Forest Service, Northeastern Experiment Station, Radnor, PA, USA

  • Ammer S, Weber K, Abs C, Ammer C, Prietzel J (2006) Factors influencing the distribution and abundance of earthworm communities in pure and converted Scots pine stands. Appl Soil Ecol 33:10–21

    Article  Google Scholar 

  • Ashton IW, Hyatt LA, Howe KM, Gurevitch J, Lerdau M (2005) Invasive species accelerate decomposition and litter nitrogen loss in a mixed deciduous forest. Ecol Appl 15:1263–1272

    Article  Google Scholar 

  • Bernard MJ, Neatrour MA, McCay TS (2009) Influence of soil buffering capacity on earthworm growth, survival, and community composition in the Western Adirondacks and Central New York. Northeast Nat 16:269–284

    Article  Google Scholar 

  • Braun EL (1950) Deciduous forests of eastern North America. Blakiston, Philadelphia

    Google Scholar 

  • Burtis JC, Fahey TJ, Yavitt JB (2014) Impact of invasive earthworms on Ixodes scapularis and other litter-dwelling arthropods in hardwood forests, central New York state, USA. Appl Soil Ecol 84:148–157

    Article  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 (2012) Invasion by a non-native ecosystem engineer alters distribution of a native predator. Divers Distrib 18:1190–1198

    Article  Google Scholar 

  • Cameron EK, Bayne EM (2015) Spatial patterns and spread of exotic earthworms at local scales. Can J Zool 93:721–726

    Article  Google Scholar 

  • Cassin CM, Kotanen PM (2016) Invasive earthworms as seed predators of temperate forest plants. Biol Invasions 18:1–14

    Article  Google Scholar 

  • Chan KY, Mead JA (2003) Soil acidity limits colonization by Aporrectodea trapezoides, an exotic earthworm. Pedobiologia 47:225–229

    Article  Google Scholar 

  • Chang C-H, Johnston MR, Gorres JH, Davalos A, McHugh D, Szlavecz K (2018) Co-invasion of three Asian earthworms, Metaphire hilgendorfi, Amynthas agrestis and Amynthas tokioensis in the USA. Biol Invasions 20:843–848

    Article  Google Scholar 

  • Craven D et al (2017) The unseen invaders: introduced earthworms as drivers of change in plant communities in North American forests (a meta-analysis). Glob Change Biol 23:1065–1074

    Article  Google Scholar 

  • Cressie NAC (1993) Statistics for spatial data, revised edn. Wiley, New York

    Google Scholar 

  • Csuzdi C, Chang C-H, Pavlícek T, Szederjesi T, Esopi D, Szlávecz K (2017) Molecular phylogeny and systematics of native North American lumbricid earthworms (Clitellata: Megadrili). PLoS ONE 12:e0181504. https://doi.org/10.1371/journal.pone.0181504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dindal DL (1990) Soil biology guide. Wiley, New York

    Google Scholar 

  • Eisenhauer N, Straube D, Scheu S (2008) Efficiency of two widespread non-destructive extraction methods under dry soil conditions for different ecological earthworm groups. Eur J Soil Biol 44:141–145

    Article  Google Scholar 

  • Fenneman NM (1917) Physiographic subdivision of the United States. Proc Natl Acad Sci USA 3:17–22

    Article  CAS  PubMed  Google Scholar 

  • Ferlian O, Eisenhauer N, Aguirrebengoa M, Camara M, Ramirez-Rojas I, Santos F, Tanalgo K, Thakur MP (2018) Invasive earthworms erode soil biodiversity: a meta-analysis. J Anim Ecol 2018:162–172

    Article  Google Scholar 

  • Gates GE (1929) The earthworm fauna of the United States. Science 70:266

    Article  CAS  PubMed  Google Scholar 

  • Gates GE (1966) Requiem—for megadrile utopias. A contribution toward the understanding of the earthworm fauna of North America. Proc Biol Soc Wash 79:239–254

    Google Scholar 

  • Görres JH, Connolly ST, Chang C-H, Carpenter NR, Keller EL, Nouri-Aiin M, Schall JJ (2018) Winter hatching in New England populations of invasive pheretimoid earthworms Amynthas agrestis and Amynthas tokioensis: a limit on population growth, or aid in peripheral expansion? Biol Invasions 20:1651–1655

    Article  Google Scholar 

  • Greiner HG, Costello DM, Tiegs SD (2010) Allometric estimation of earthworm ash-free dry mass from diameters and lengths of select megascolecid and lumbricid species. Pedobiologia 53:247–252

    Article  Google Scholar 

  • Greiner HG, Kashian DR, Tiegs SD (2012) Impacts of invasive Asian (Amynthas hilgendorfi) and European (Lumbricus rubellus) earthworms in a North American temperate deciduous forest. Biol Invasions 14:2017–2027

    Article  Google Scholar 

  • Gundale MJ (2002) Influence of exotic earthworms on the soil organic horizon and the rare fern Botrychium mormo. Cons Biol 16:1555–1561

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    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 Midl Nat 151:179–185

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hale CM, Freilich LE, Reich PB (2006) Changes in cold-temperate hardwood forest understory plant communities in response to invasion by European earthworms. Ecology 87:1637–1649

    Article  PubMed  Google Scholar 

  • Hanna WE (1981) Soil survey of Madison County, New York. USDA Soil Conservation Service, Washington

    Google Scholar 

  • Hendershot WH, Lalande H, Duquette M (1993) Soil reaction and exchangeable acidity. In: Carter MR (ed) Soil sampling and methods of analysis. Lewis Publishers, Boca Raton, pp 141–145

    Google Scholar 

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

    Article  Google Scholar 

  • Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314

    Google Scholar 

  • James SW (1995) Systematics, biogeography, and ecology of Nearctic earthworms from eastern, central, southern, and southwestern United States. In: Hendrix PF (ed) Earthworm ecology and biogeography in North America. Lewis Publishers, Boca Raton, pp 29–52

    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, pp 75–88

    Google Scholar 

  • Karam A (1993) Chemical properties of organic soils. In: Carter MR (ed) Soil sampling and methods of analysis. Lewis Publishers, Boca Raton, pp 459–471

    Google Scholar 

  • Keller R, Cox A, Van Loon C, Lodge D, Herborg L, Rothlisberger J (2007) From bait shops to the forest floor: earthworm use and disposal by anglers. Am Midl Nat 158:321–328

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Maerz JC, Nuzzo VA, Blossey B (2009) Declines in woodland salamander abundance associated with non-native earthworm and plant invasions. Cons Biol 23:975–981

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • McCay TS, Pinder RA, Alvarado E, Hanson WC (2017) Distribution and habitat of the endemic earthworm Eisenoides lonnbergi (Michaelsen) in the northeastern United States. Northeast Nat 24:239–248

    Article  Google Scholar 

  • McCune B, Mefford MJ (2016) PC-ORD: Multivariate analysis of ecological data, V7. MjM Software Design, Gleneden Beach, Oregon

    Google Scholar 

  • Moore ID, Gessler PE, Nielsen GA, Petersen GA (1993) Terrain attributes: estimation methods and scale effects. In: Jakeman AJ, Beck MB, McAleer MJ (eds) Modeling change in environmental systems. Wiley, Chichester, pp 189–214

    Google Scholar 

  • Moore J-D, Görres JH, Reynolds JW (2018) Exotic Asian pheretimoid earthworms (Amynthas spp., Metaphire spp.): potential for colonisation of south-eastern Canada and effects on forest ecosystems. Environ Rev 26:113–120

    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. Cons Biol 23:966–974

    Article  Google Scholar 

  • Owen RB Jr, Galbraith WJ (1989) Earthworm biomass in relation to forest types, soil, and land use: implications for woodcock management. Wildl Soc B 17:130–136

    Google Scholar 

  • Paudel S, Wilson GWT, MacDonald B, Longcore T, Loss SR (2016) Predicting spatial extent of invasive earthworms on an oceanic island. Divers Distrib 22:1013–1023

    Article  Google Scholar 

  • Peck JE (2016) Multivariate analysis for ecologists: Step-by-step, 2nd edn. MjM Software Design, Gleneden Beach, Oregon

    Google Scholar 

  • Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644

    Article  Google Scholar 

  • Reynolds JW (1977) The earthworms (Lumbricidae and Sparganophilidae) of Ontario. Life Sciences Miscellaneous Publications. Royal Ontario Museum, Toronto

    Google Scholar 

  • Reynolds JW (1994) The distribution of the earthworms (Oligochaeta) of Indiana: a case for the Post Quaternary Introduction Theory of megadrile migration in North America. Megadrilogica 5:13–32

    Google Scholar 

  • Roberts DW, Cooper SV (1989) Concepts and techniques of vegetation mapping. In: Ferguson DE, Johnson FD, Morgan P (eds) Proceedings, land classifications based on vegetation: applications for resource management. USDA Forest Service Intermountain Research Station, GTR 257, Ogden, Utah, pp 90–96

  • Rogers JA, Collins CD (2017) Ecological predictors and consequences of non-native earthworms in Kennebec County, Maine. Northeast Nat 24:121–136

    Article  Google Scholar 

  • Saltmarsh DM, Bowser ML, Morton JM, Lang S, Shain D, Dial R (2016) Distribution and abundance of exotic earthworms within a boreal forest system in southcentral Alaska. Neobiota 28:67–86

    Article  Google Scholar 

  • Schwert DP (1990) Oligochaeta: Lumbricidae. In: Dindal DL (ed) Soil biology guide. Wiley, New York, pp 341–356

    Google Scholar 

  • Schwert DP, Dance KW (1979) Earthworm cocoons as a drift component in a southern Ontario stream. Can Field-Nat 93:180–183

    Google Scholar 

  • Shartell LM, Lilleskov EA, Storer AJ (2013) Predicting exotic earthworm distribution in the northern Great Lakes region. Biol Invasions 15:1665–1675

    Article  Google Scholar 

  • Shartell LM, Corace RG III, Storer AJ, Kashian DM (2015) Broad and local-scale patterns of exotic earthworm functional groups in forests of National Wildlife Refuges in the Upper Midwest, USA. Biol Invasions 17:3591–3607

    Article  Google Scholar 

  • Simmons WA, Dávalos A, Blossey B (2015) Forest successional history and earthworm legacy affect earthworm survival and performance. Pedobiologia 58:153–164

    Article  Google Scholar 

  • Stoscheck LM, Sherman RE, Suarez ER, Fahey TJ (2012) Exotic earthworm distributions did not expand over a decade in a hardwood forest in New York State. Appl Soil Ecol 62:124–130

    Article  Google Scholar 

  • Suarez ER, Fahey TJ, Groffman PM, Yavitt JB, Bohlen PJ (2006) Spatial and temporal dynamics of exotic earthworm communities along invasion fronts in a temperate hardwood forest in South-Central New York (USA). Biol Invasions 8:553–564

    Article  Google Scholar 

Download references

Acknowledgments

The State of New York Department of Environmental Conservation, the Cazenovia Preservation Foundation, K. Ingram, R. Fuller, C. Gavilondo, and E. Spadola allowed access to properties. M. Baimas-George, Z. Cardell, H. Elder, D. Goldstein, M. Kryachko, M. Lancaster, E. Moore, W. Morgan, N. Nguyen, A. Nugent, and M. Zimmerman provided assistance in the field or lab. S. Berardi and J. Montaquila provided comments on the manuscript. The Upstate Institute at Colgate University provided funding in support of this project.

Author information

Authors and Affiliations

  1. Department of Biology and Program in Environmental Studies, Colgate University, Hamilton, NY, 13346, USA

    Timothy S. McCay

  2. Department of Geography, Colgate University, Hamilton, NY, 13346, USA

    Peter Scull

Authors
  1. Timothy S. McCay
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter Scull
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Timothy S. McCay.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

McCay, T.S., Scull, P. Invasive lumbricid earthworms in northeastern North American forests and consequences for leaf-litter fauna. Biol Invasions 21, 2081–2093 (2019). https://doi.org/10.1007/s10530-019-01959-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-019-01959-1

Keywords

  • Bimastos
  • Earthworms
  • Leaf litter
  • Lumbricidae
  • Roads
  • Soils