Skip to main content

Advertisement

SpringerLink
Log in

Invasive Earthworms Deplete Key Soil Inorganic Nutrients (Ca, Mg, K, and P) in a Northern Hardwood Forest

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

Hardwood forests of the Great Lakes Region have evolved without earthworms since the Last Glacial Maximum, but are now being invaded by exotic earthworms introduced through agriculture, fishing, and logging. These exotic earthworms are known to increase soil mixing, affect soil carbon storage, and dramatically alter soil morphology. Here we show, using an active earthworm invasion chronosequence in a hardwood forest in northern Minnesota, that such disturbances by exotic earthworms profoundly affect inorganic nutrient cycles in soils. Soil nutrient elemental concentrations (Ca, Mg, K, and P) were normalized to biogeochemically inert Zr to quantify their losses and gains. This geochemical normalization revealed that elements were highly enriched in the A horizon of pre-invasion soils, suggesting tight biological recycling of the nutrients. In the early stage of invasion, epi-endogeic earthworm species appeared to have been responsible for further enriching the elements in the A horizon possibly by incorporating leaf organic matter (OM). The arrival of geophagous soil mixing endogeic earthworms, however, was associated with near complete losses of these enrichments, which was related to the loss of OM in soils. Our study highlights that elemental concentrations may not be sufficient to quantify biogeochemical effects of earthworms. The geochemical normalization approach, which has been widely used to study soil formation, may help when determining how invasive soil organisms affect soil elemental cycles. More generally, this approach has potential for much wider use in studies of belowground nutrient dynamics. The results support the existing ecological literature demonstrating that invasive earthworms may ultimately reduce productivity in formerly glaciated forests under climate change.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8
Figure 9

Similar content being viewed by others

References

  • ALS Chemex [Internet]. 2014. http://www.alsglobal.com/. Accessed 2 Oct 2014.

  • Bartlett MD, Harris JA, James IT, Ritz K. 2006. Inefficiency of mustard extraction technique for assessing size and structure of earthworm communities in UK pasture. Soil Biol Biochem 38:2990–2.

    Article  CAS  Google Scholar 

  • 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 

  • 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 2:427–35.

    Article  Google Scholar 

  • Brimhall GH, Dietrich WE. 1987. Constitutive mass balance relations between chemical composition, volume, density, porosity, and strain in metasomatic hydrochemical systems: results on weathering and pedogenesis. Geochim Cosmochim Acta 51:567–87.

    Article  CAS  Google Scholar 

  • Chadwick OA, Derry LA, Vitousek PM, Huebert BJ, Hedin LO. 1999. Changing sources of nutrients during four million years of ecosystem development. Nature 397:491–7.

    Article  CAS  Google Scholar 

  • Crumsey JM, Moine L, Capowiez Y, Goodsitt MM, Larson SC, Kling GW, Nadelhoffer KJ. 2013. Community-specific impacts of exotic earthworm invasions on soil carbon dynamics in a sandy temperate forest. Ecology 94:2827–37.

    Article  PubMed  Google Scholar 

  • Dempsey MA, Fisk MC, Fahey TJ. 2011. Earthworms increase the ratio of bacteria to fungi in northern hardwood forest soils, primarily by eliminating the organic horizon. Soil Biol Biochem 43:2135–41.

    Article  CAS  Google Scholar 

  • Eisenhauer N, Milcu A, Sabais ACW, Scheu S. 2008. Animal ecosystem engineers modulate the diversity–invasibility relationship. PLoS ONE 3(10):e3489.

    Article  PubMed Central  PubMed  Google Scholar 

  • Fahey TJ, Yavitt JB, Sherman RE et al. 2013a. Earthworm effects on the incorporation of litter C and N into soil organic matter in a sugar maple forest. Ecol Appl 23(5):1185–201.

    Article  PubMed  Google Scholar 

  • Fahey TJ, Yavitt JB, Sherman RES, Maerz JC, Groffman PM, Fisk MC, Bohlen PJ. 2013b. Earthworms, litter and soil carbon in a northern hardwood forest. Biogeochemistry 114(1–3):269–80.

    Article  Google Scholar 

  • Fassel VA, Kniseley RN. 1974. Inductively coupled plasma optical emission spectroscopy. Anal Chem 46(13):1110A–20A.

    Article  CAS  Google Scholar 

  • Finzi AC, Canham CD, Van Breemen N. 1998. Canopy tree–soil interactions within temperate forests: species effects on pH and cations. Ecol Appl 8(2):447–54.

    Google Scholar 

  • Fisk MC, Fahey TJ, Groffman PM, Bohlen PJ. 2004. Earthworm invasion, fine root distribution and soil respiration in hardwood forests. Ecosystems 7:55–62.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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(6):1235–45.

    Article  Google Scholar 

  • Frelich LE, Peterson RO, Dovciak M, Reich PB, Vucetich JA, Eisenhauer N. 2012. Tropic cascades, invasive species and body-size hierarchies interactively modulate climate change responses of ecotonal temperate-boreal forest. Philos Trans R Soc B 367:2955–61.

    Article  Google Scholar 

  • Gundale MJ. 2002. Influence of exotic earthworms on the soil organic horizon and the rare fern Botrychiummormo. Conserv Biol 16(6):1555–61.

    Article  Google Scholar 

  • Gutierrez JL, Jones CG. 2006. Physical ecosystem engineers as agents of biogeochemical heterogeneity. Bioscience 56(3):227–36.

    Article  Google Scholar 

  • Hale CM. 2007. Earthworms of the Great Lakes. Duluth, MN: Kollath and Stensaas Publishing. p 36.

    Google Scholar 

  • Hale CM. 2008. Evidence for human-mediated dispersal of exotic earthworms: support for exploring strategies to limit further spread. Mol Ecol 17:1165–9.

    Article  PubMed  Google Scholar 

  • 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 15:179–85.

  • Hale CM, Frelich LE, Reich PB. 2005a. Exotic European earthworm invasion dynamics in northern hardwood forests of Minnesota, U.S.A. Ecol Appl 15:848–60.

    Article  Google Scholar 

  • Hale CM, Frelich LE, Reich PB. 2005b. Effects of European earthworm invasion on soil characteristics in northern hardwood forests of Minnesota. Ecosystems 8:911–27.

    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(7):1637–49.

    Article  PubMed  Google Scholar 

  • Hale CME, Reich PB, Pastor J. 2008. Exotic earthworm effects on hardwood forest floor, nutrient availability and native plants: a mesocosm study. Oecologia 155(3):509–18.

    Article  PubMed  Google Scholar 

  • Hendrix PF, Bohlen PJ. 2002. Exotic earthworm invasions in North American: ecological and policy implications. Bioscience 52(9):801–11.

    Article  Google Scholar 

  • Hendrix PF, Callaham MA, Drake JM, Huang C, James SW, Snyder BA, Zhang W. 2008. Pandora’s box contained bait: the global problem of introduced earthworms. Ann Rev Ecol Evol Syst 39:593–613.

    Article  Google Scholar 

  • Holdsworth AR, Frelich LE, Reich PB. 2007. Effects of earthworm invasion on plant specie richness in northern hardwood forests. Conserv Biol 21(4):997–1008.

    Article  PubMed  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(4):536–44.

    Article  Google Scholar 

  • Hole FD. 1981. Effects of animals on soil. Geoderma 25:75–112.

    Article  Google Scholar 

  • Johnson DL, Domier JEJ, Johnson DN. 2005. Reflections on the nature of soil and its biomantle. Ann Assoc Am Geogr 95(1):11–31.

    Article  Google Scholar 

  • Jones CG, Lawton JH, Shachak M. 1997. Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78(7):1946–57.

    Article  Google Scholar 

  • Kurtz AC, Derry LA, Chadwick OA, Alfano MJ. 2000. Refractory element mobility in volcanic soils. Geology 28:683–6.

    Article  CAS  Google Scholar 

  • Larson ER, Kipfmueller KF, Hale CM, Frelich LE, Reich PB. 2009. Tree rings detect earthworm invasions and their effects in northern Hardwood forests. Biol Invasions 12:1053–66.

    Article  Google Scholar 

  • Likens GE, Driscoll CT, Buso DC, Siccama TG, Johnson CE, Lovett GM, Fahey TJ, Reiners WA, Ryan DF, Martin CW, Bailey SW. 1998. The biogeochemistry of calcium at Hubbard Brook. Biogeochemistry 41:89–173. doi:10.1023/A:1005984620681.

    Article  CAS  Google Scholar 

  • 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(5):983–92.

    Article  PubMed  Google Scholar 

  • Lyttle, A. 2013. Carbon–mineral interactions and bioturbation: an earthworm invasion chronosequence in a sugar maple forest in Northern Minnesota. MS Thesis, University of Minnesota.

  • Lyttle A, Yoo K, Hale C, Aufdenkampe A, Sebestyen SD, Resner K, Blum A. 2014. Impact of exotic earthworms on organic carbon sorption on mineral surfaces and soil carbon inventories in a northern hardwood forest. Ecosystems. doi:10.1007/s10021-014-9809-x.

  • Maerz JC, Nuzzo VA, Blossey B. 2009. Declines in woodland salamander abundance associated with non-native earthworm and plant invasions. Conserv Biol 23(4):975–81.

    Article  PubMed  Google Scholar 

  • McLaughlin SB, Wimmer R. 1999. Tansley Review No. 104: calcium physiology and terrestrial ecosystem processes. New Phytol 142:373–417.

    Article  CAS  Google Scholar 

  • Munter RC, Grande RA. 1981. Plant tissue and soil extract analysis by ICP-AES. In: Barnes RM, Ed. Developments in atomic plasma spectrochemical analysis. Philadelphia, PA: Heydon and Son. p 653–73.

    Google Scholar 

  • Oades JM. 1998. The retention of organic matter in soils. Biogeochemistry 5:35–70.

    Article  Google Scholar 

  • Pare D, Bernier B. 1989. Origin of the phosphorus deficiency observed in declining sugar maple stands in the Quebec Appalachians. Can J For Res 19(1):24–34.

    Article  Google Scholar 

  • Resner K. 2013. Impacts of earthworm bioturbation on elemental cycles in soils: an application of a geochemical mass balance to an earthworm invasion chronosequence in a sugar maple forest in Northern Minnesota. MS Thesis, University of Minnesota.

  • Resner K, Yoo K, Hale CM, Aufdenkampe A, Blum A, Sebestyen S. 2011. Elemental and mineralogical changes in soils due to bioturbation along an earthworm invasion chronosequence in northern Minnesota. Appl Geochem 26:S127–31.

    Article  CAS  Google Scholar 

  • Reynolds JW. 1977. The earthworms (Lumbricidae and Sparganophilidae) of Ontario. Toronto: Royal Ontario Museum Miscellaneous Publication.

    Google Scholar 

  • Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssesn IA, Kleber M, Kögel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE. 2011. Persistence of soil organic matter as an ecosystem property. Nature 478:49–56.

    Article  CAS  PubMed  Google Scholar 

  • Schwert DP. 1990. Oligochaeta: Lumbricidae. In: Dindal DL, Ed. Soil biology guide. New York: Wiley. p 341–56.

    Google Scholar 

  • Soil Survey Staff, Natural Resources Conservation Service, United States Department of Agriculture. Official Soil Series Descriptions. 2014. http://www.nrcs.usda.gov/wps/portal/nrcs/detailfull/soils/home/?cid=nrcs142p2_053587. Accessed 2 Oct 2014.

  • 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 62:124–30.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Thomas GW. 1982. Exhangeable cations. In: Page AL, Ed. Methods of soil analysis. Part 2: Chemical and microbiological properties. 2nd edn. Madison, WI: ASA Agron. p 159–65.

    Google Scholar 

Download references

Acknowledgments

The authors are thankful for the generous support from USDA NRI program to K. Yoo, A.K. Aufdenkmape, and C. Hale. Yoo’s effort was also partly supported by Hatch Fund from Agricultural Experimental Station. We thank Cristina Fernandez, Tyler Nigon, Rebecca D. Knowles, and Andrew Haveles for field assistance, and Jennifer Wang and Justene Davis for lab assistance.

Author information

Authors and Affiliations

  1. Department of Soil, Water, and Climate, University of Minnesota, 439 Borlaug Hall, 1991 Upper Buford Circle, St. Paul, Minnesota, 55108, USA

    Kit Resner, Kyungsoo Yoo & Amy Lyttle

  2. Northern Research Station, USDA Forest Service, 1831 HWY 169E, Grand Rapids, Minnesota, 55744, USA

    Stephen D. Sebestyen

  3. Stroud Water Research Center, 970 Spencer Road, Avondale, Pennsylvania, 19311, USA

    Anthony Aufdenkampe

  4. University of Minnesota-Duluth, The Natural Resources Research Institute, 5013 Miller Trunk Hwy, Duluth, Minnesota, 55811, USA

    Cindy Hale

  5. US Geological Survey, 3215 Marine St, Boulder, Colorado, 80303, USA

    Alex Blum

Authors
  1. Kit Resner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kyungsoo Yoo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stephen D. Sebestyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anthony Aufdenkampe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cindy Hale
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Amy Lyttle
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alex Blum
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kyungsoo Yoo.

Additional information

Author contributions

K.R. conducted part of the laboratory and data analyses, and wrote the first draft of the manuscript. K.Y. conceived and designed the study, led and supervised field and laboratory works, data analysis, and paper writing. A.A. and S.D.S. assisted with study design, laboratory analysis, and manuscript writing. C.H. supervised earthworm survey and identification and coordinated the 2009 field trip. A.L. participated in determining earthworm biomass and identification. A.B. conducted and interpreted quantitative XRD.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1134 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Resner, K., Yoo, K., Sebestyen, S.D. et al. Invasive Earthworms Deplete Key Soil Inorganic Nutrients (Ca, Mg, K, and P) in a Northern Hardwood Forest. Ecosystems 18, 89–102 (2015). https://doi.org/10.1007/s10021-014-9814-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-014-9814-0

Keywords

Search

Navigation