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Impact of Exotic Earthworms on Organic Carbon Sorption on Mineral Surfaces and Soil Carbon Inventories in a Northern Hardwood Forest

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Abstract

Exotic earthworms are invading forests in North America where native earthworms have been absent since the last glaciation. These earthworms bioturbate soils and may enhance physical interactions between minerals and organic matter (OM), thus affecting mineral sorption of carbon (C) which may affect C cycling. We quantitatively show how OM-mineral sorption and soil C inventories respond to exotic earthworms along an earthworm invasion chronosequence in a sugar maple forest in northern Minnesota. We hypothesized that mineral surface area in A horizons would increase as burrowing earthworms incorporated clay minerals from the B horizons and that enhanced contacts between OM and minerals would increase the OM sorption on mineral surfaces and mineral-associated C inventories in A horizons. Contrary to our hypotheses, mineral surface areas within A horizons were lowered because earthworm burrows only extended into the silt-rich loess that separated the A and clay-rich B horizons. Furthermore, where endogeic earthworms were present, a smaller fraction of mineral surface area was covered with OM. OM sorption on minerals in the A horizons shifted from a limitation of mineral surface availability to a limitation of OM availability within a decade after the arrival of endogeic earthworms. C-mineral sorption depends on earthworm consumption of OM as well as the composition and vertical distribution of minerals. This finding may thus explain the contradictory results reported in earlier investigations. Our results highlight the rapid and drastic effects of exotic earthworms on key ecosystem processes in deciduous forests in post-glacial settings.

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References

  • Adams MB, Loughry LH, Plaugher LP. 2004. Experimental Forests and Ranges of the USDA Forest Service. Newtown Square (PA): US Department of Agriculture.

    Google Scholar 

  • Alban DH, Berry EC. 1994. Effects of earthworm invasion on morphology, carbon and nitrogen of a forest soil. Appl Soil Ecol 1:243–9.

    Article  Google Scholar 

  • Baldock JA, Skjemstad JO. 2000. Role of the soil matrix and minerals in protecting natural organic materials against biological attack. Org Geochem 31(7):697–710.

    Article  CAS  Google Scholar 

  • Bohlen PJ, Pelletier D, Groffman PM, Fahey TJ, Fist MC. 2004a. Ecosystem consequences of exotic earthworm invasion of north temperate forests. Ecosystems 7:1–12.

    Article  Google Scholar 

  • Bohlen PJ, Pelletier DM, Groffman PM, Fahey TJ, Fisk MC. 2004b. Influence of earthworm invasion on redistribution and retention of soil carbon and nitrogen in northern temperate forests. Ecosystems 7:13–27.

    Article  CAS  Google Scholar 

  • Bohlen PJ, Scheu S, Hale CM, McLean MA, Migge S, Groffman PM, Parkinson D. 2004c. Non-native invasive earthworms as agents of change in northern temperate forests. Front Ecol Environ 2(8):427–35.

    Article  Google Scholar 

  • Borggaard OK. 1982. The influence of iron oxides on the surface area of soil. J Soil Sci 33:443–9.

    Article  CAS  Google Scholar 

  • Burtelow AE, Bohlen PJ, Groffman PM. 1998. Influence of exotic earthworm invasion on soil organic matter, microbial biomass and denitrification potential in forest soils of the northeastern United States. Appl Soil Ecol 9:197–202.

    Article  Google Scholar 

  • Chiou CT. 1990. The surface area of soil organic matter. Environ Sci Technol 24:1164–6.

    Article  CAS  Google Scholar 

  • Cornell RM, Schwertmann U. 2003. The iron oxides: structure, properties, reactions, occurrences and uses. Weinheim (DE): Wiley. p 664.

    Book  Google Scholar 

  • Crooks J. 2002. Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–66.

    Article  Google Scholar 

  • Drake HL, Schramm HMA. 2006. Earthworm gut microbial biomes: their importance to soil microorganisms, denitrification, and the terrestrial production of the greenhouse gas N2O. Soil Biol 6:65–87.

    Article  CAS  Google Scholar 

  • Eberl DD. 2003. User’s guide to Rockjock: a program for determining quantitative mineralogy from powder X-ray diffraction data. US Geological Survey Open-File Report: 03-78. p. 46.

  • Essington ME. 2004. Soil and water chemistry: an integrative approach. Boca Raton (FL): CRC Press. p 534.

    Google Scholar 

  • Eusterhues K, Rumpel C, Kögel-Knabner I. 2005. Organo-mineral associations in sandy acid forest soils: importance of specific surface area, iron oxides and micropores. Eur J Soil Sci 56:753–63.

    CAS  Google Scholar 

  • Frelich LE, Hale CM, Scheu S, Holdsworth AR, Henegham L, Bohlen PJ, Reich PB. 2006. Earthworm invasion into previously earthworm-free temperate and boreal forests. Biol Invasions 8:1235–45.

    Article  Google Scholar 

  • Gundale MJ. 2002. The influence of exotic earthworms on soil organic horizon and the rare fern Botrychium mormo. Conserv Biol 16:1555–73.

    Article  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 J 151(1):179–85.

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Hale CM, Frelich LE, Reich PB. 2006. Changes in cold-temperate hardwood forest understory plan communities in response to invasion by European earthworms. Ecology 87:1637–49.

    Article  PubMed  Google Scholar 

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

    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 155:509–18.

    Article  PubMed  Google Scholar 

  • Hendrix PF, CallahamMA MA, Drake JM, Huang CY, James SW, Snyder BA, Zhang W. 2008. The global problem of introduced earthworms. Ann Rev Ecol Evol Syst 39:593–613.

    Article  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 

  • Holmgren GGS. 1967. A rapid citrate-dithionate extractable iron procedure. Soil Sci Soc Am Proc 31:210–11.

    Article  CAS  Google Scholar 

  • Kaiser K, Guggenberger G. 2000. The role of DOM sorption to mineral surfaces in the preservation of organic matter in soils. Org Geochem 31:711–25.

    Article  CAS  Google Scholar 

  • Kaiser K, Guggenberger G. 2003. Mineral surfaces and soil organic matter. Eur J Soil Sci 54:219–36.

    Article  CAS  Google Scholar 

  • Kaiser K, Guggenberger G. 2007. Sorptive stabilization of organic matter by microporous goethite: sorption into small pores vs. surface complexation. Eur J Soil Sci 58:45–59.

    Article  CAS  Google Scholar 

  • Kleber M, Sollins P, Sutton R. 2007. A conceptual model of organo-mineral interactions in soils: self-assembly of organic molecular fragments into zonal structures on mineral surfaces. Biogeochemsitry 85:9–24.

    Article  Google Scholar 

  • Lawrence AP, Bowers MA. 2002. A test of the ‘hot’ mustard extraction method of sampling earthworms. Soil Biol Biochem 34:549–52.

    Article  CAS  Google Scholar 

  • Mayer LM. 1999. Extent of coverage of interal surfaces by organic matter in marine sediments. Geochim Cosmochim Acta 63(2):207–15.

    Article  CAS  Google Scholar 

  • McKeague JA, Day JH. 1966. Dithionite and oxalate-extractable Fe and Al as aids in differentiating various classes of soils. Can J Soil Sci 46:13–22.

    Article  CAS  Google Scholar 

  • Minnesota State Climatology Office. 2003. Minnesota climatology working group website http://climate.umn.edu, Minnesota Department of Natural Resources and the University of Minnesota, Department of Soil, Water and Climate, St. Paul, MN 55108.

  • Oyedele DJ, Schjønning P, Amunsan AA. 2006. Physiochemical properties of earthworm casts and uningested parent soil from selected sites in southwestern Nigeria. Ecol Eng 28:106–13.

    Article  Google Scholar 

  • Pronk GJ, Heister K, Kögel-Knabner I. 2011. Iron oxides as major available interface component in loamy arable topsoils. Soil Sci Soc Am J 75:2158–68.

    Article  CAS  Google Scholar 

  • Ransom B, Kim D, Kastner M, Wainwright S. 1998. Organic matter preservation on continental slopes: importance of mineralogy and surface area. Geochim Cosmochim Acta 62:1329–45.

    Article  CAS  Google Scholar 

  • Remusat L, Hatton Pierre-Joseph, Nico Peter S, Zeller Bernd, Kleber Markus, Derrien Delphine. 2012. NanoSIMS study of organic matter associated with soil aggregates: advantages, limitations, and combination with STXM. Environ Sci Technol 46:3943–9.

    Article  CAS  PubMed  Google Scholar 

  • Resner KE. 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. p 182.

  • Resner KE, Yoo K, Hale C, Aufdenkampe A, Blum A, Sebestyen S. 2011. Elemental and mineralogical changes in soil 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 (ON): Royal Ontario Museum Miscellaneous Publication.

    Google Scholar 

  • Scheu S, Parkinson D. 1994a. Effects of earthworms on nutrient dynamics, carbon turnover and microorganisms in soil from cool temperate forests of the Canadian Rocky Mountains: laboratory studies. Appl Soil Ecol 1:113–25.

    Article  Google Scholar 

  • Scheu S, Parkinson D. 1994b. Effects of invasion of an aspen forest (Canada) by Dendrobaena octaedra (Lumbricidae) on plant growth. Ecology 75:2348–61.

    Article  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. Dindal DL, editor. Soil biology guide. New York: John Wiley and Sons. p.341-356.

  • Sollins P, Kramer M, Swantson C, Lajtha K, Filley T, Aufdenkampe A, Wagai R, Bowden R. 2009. Sequential density fractionation across soils of contrasting mineralogy: evidence for both microbial- and mineral-controlled soil organic matter stabilization. Biogeochemistry 96:209–31.

    Article  CAS  Google Scholar 

  • Torn MS, Trumbore SE, Chadwich OA, Vitousek PM, Hendricks MD. 1997. Mineral control of soil organic carbon storage and turnover. Nature 389:170–3.

    Article  CAS  Google Scholar 

  • Torresan M. 1987. The use of sodium polytungstate in heavy mineral separations. US Geological Survey Open-File Report. pp 87–590

  • von Lutzow M, Kögel-Knabner I, Ekschmitt K, Matzner E, Guggenberger G, Marschner B, Flessa H. 2006. Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions: a review. Eur J Soil Sci 57:426–45.

    Article  Google Scholar 

  • Wagai R, Mayer LM, Kitayama K. 2009. Extent and nature of organic coverage of soil mineral surfaces assessed by a gas sorption approach. Geoderma 149:152–60.

    Article  CAS  Google Scholar 

  • Webb PA, Orr C. 1997. Analytical methods in fine particle technology. Norcross (GA): Micromeritics Instrument Corp. p p301.

    Google Scholar 

  • Wironen M, Moore TR. 2006. Exotic earthworm invasion increases soil carbon and nitrogen in an old-growth forest in southern Quebec. Can J For Res 36:845–54.

    Article  Google Scholar 

Download references

Acknowledgements

This study was financially support by a USDA NRI Grant to K. Yoo, A.K. Aufdenkampe, and C.Hale. Yoo’s effort was partly covered by Hatch funding from Agricultural Experiment Station. We thank Cristina Fernandez, Jim Barott and Becky Knowles for their help in the field. We also appreciate detailed and constructive comments by our colleagues: Lee Frelich at the University of Minnesota, Don Ross at the University of Vermont and Kurt Smemo at the Holden Arboretum. We thank constructive comments from two anonymous reviewers.

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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

    Amy Lyttle, Kyungsoo Yoo & Kathryn Resner

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

    Cindy Hale

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

    Anthony Aufdenkampe

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

    Stephen D. Sebestyen

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

    Alex Blum

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  1. Amy Lyttle
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  4. Anthony Aufdenkampe
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Correspondence to Kyungsoo Yoo.

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Author contributions

A. Lyttle conducted part of laboratory analysis, analyzed data, and wrote the first draft. K. Yoo conceived and designed the study, led collaborative field and laboratory research, analyzed data, and wrote the paper. C. Hale supervised earthworm collection and identification. A. Aufdenkampe contributed to designing BET surface area analysis, study design, and sample collection. S. D. Sebestyen contributed to study design and writing. K. Resner contributed to laboratory analysis. A. Blum conducted quantitative mineralogical analysis.

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Lyttle, A., Yoo, K., Hale, C. et al. Impact of Exotic Earthworms on Organic Carbon Sorption on Mineral Surfaces and Soil Carbon Inventories in a Northern Hardwood Forest. Ecosystems 18, 16–29 (2015). https://doi.org/10.1007/s10021-014-9809-x

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