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Tree rings detect earthworm invasions and their effects in northern Hardwood forests

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Abstract

Invasions of European earthworms into the forests of northern North America are causing dramatic changes in forest floor structure, vegetation communities, biogeochemical cycling, and site hydrology. However, long-term studies on the effects of invasive earthworms are limited because little data exist on the timing and rate of earthworm invasion at specific sites. We successfully used tree rings to identify the timing of earthworm invasions and the effects of earthworm activity on the Acer saccharum overstory of two recently invaded sites in northern Minnesota, thereby establishing a method to date earthworm invasions at other sites. In addition to identifying a tree-ring signature related to earthworm invasion, we found trees growing in invaded conditions were more sensitive to drought than trees growing in earthworm-free conditions. Increased drought sensitivity by A. saccharum has important implications for possible range shifts under climate change scenarios that include increasing drought frequency and severity.

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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 

  • Alley WM (1984) The palmer drought severity index: limitations and assumptions. J Appl Meteor 23:1100–1109

    Article  Google Scholar 

  • Asshof R, Schweingruber FH, Wermelinger B (1999) Influence of a gypsy moth (Lymantria dispar L.) outbreak on radial growth and wood-anatomy of Spanish chestnut (Castanea sativa Mill.) in Ticino (Switzerland). Dendrochronologia 16–17:133–145

    Google Scholar 

  • Auclair AND, Lill JT, Revenga C (1996) The role of climate variability and global warming in the dieback of Northern Hardwoods. Water Air Soil Pollut 91:163–186

    Article  CAS  Google Scholar 

  • Baker WL, Veblen TT (1990) Spruce beetles and fires in the nineteenth-century subalpine forests of western Colorado. USA Arct Alp Res 22:65–80

    Article  Google Scholar 

  • Bergeron Y (2000) Species and stand dynamics in the mixed woods of Quebec’s southern boreal forest. Ecology 81:1500–1516

    Article  Google Scholar 

  • Blais JR (1958) Effects of defoliation by spruce budworm on radial growth at breast height of balsam fir and white spruce. For Chron 34:39–47

    Google Scholar 

  • Bohlen PJ, Groffman PM, Fahey TJ et al (2004a) Ecosystem consequences of exotic earthworm invasion of north temperate forests. Ecosystems 7:1–12

    Article  Google Scholar 

  • Bohlen PJ, Pelletier DM, Groffman PM et al (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 et al (2004c) Non-native invasive earthworms as agents of change in northern temperate forests. Front Ecol Environ 2:427–435

    Article  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 

  • Consulting Voortech (2005) Measure J2X v3.2.1: the tree ring measurement program. Voortech Consulting, Holderness

    Google Scholar 

  • Cook ER (1985) ARSTAN v6.05: chronology development and statistical analysis software. Tree-Ring Laboratory, Lamont-Doherty Earth Observatory of Columbia University, Palisades, NY

    Google Scholar 

  • Cook ER, Peters K (1981) The smoothing spline: a new approach to standardizing forest interior tree-ring width series for dendroclimatic studies. Tree-Ring Bull 41:45–53

    Google Scholar 

  • Duncan DP, Hodson AC (1958) Influence of the forest tent caterpillar upon the aspen forests of Minnesota. For Sci 4:71–93

    Google Scholar 

  • Easterling DR, Karl TR, Mason EH et al (1996) United States Historical Climatology Network (U.S. HCN) monthly temperature and precipitation data. ORNL/CDIAC-87, NDP-019/R3. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. DoE, Oak Ridge, TN

  • Fisk MG, Fahey TJ, Groffman PM et al (2004) Earthworm invasion, fine-root distributions, and soil respiration in north temperate forests. Ecosystems 7:55–62

    Article  Google Scholar 

  • Foster DR (1988) Disturbance history, community organization and vegetation dynamics of the old-growth Pisgah Forest, southwestern New Hampshire, USA. J Ecol 76:105–134

    Article  Google Scholar 

  • Francis GS, Fraser PM (1998) The effects of three earthworm species on soil macroporosity and hydraulic conductivity. Appl Soil Ecol 10:11–19

    Article  Google Scholar 

  • Fraver S, White AS (2005) Disturbance dynamics of old-growth Picea rubens forests of northern Maine. J Veg Sci 16:597–610

    Google Scholar 

  • Frelich LE (2002) Forest dynamics and disturbance regimes. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Frelich LE, Hale CM, Scheu S et al (2006) Earthworm invasion into previously earthworm-free temperate and boreal forests. Biol Inv 8:1235–1245

    Article  Google Scholar 

  • Fritts HC (1976) Tree rings and climate. Academic Press, New York

    Google Scholar 

  • Fritts HC, Swetnam TW (1989) Dendroecology—a tool for evaluating variations in past and present forest environments. Adv Ecol Res 19:111–188

    Article  Google Scholar 

  • Graumlich LJ (1993) Response of tree growth to climatic variation in the mixed conifer and deciduous forests of the Upper Great-Lakes Region. Can J For Res 23:133–143

    Article  Google Scholar 

  • Grissino-Mayer HD (2001) Evaluating crossdating accuracy: a manual and tutorial for the computer program COFECHA. Tree-Ring Res 57:205–221

    Google Scholar 

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

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

    Article  Google Scholar 

  • Hale CM, Frelich LE, Reich PB et al (2005b) 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

    Article  PubMed  Google Scholar 

  • Hale CM, Frelich LE, Reich PB et al (2008) Exotic earthworm effects on hardwood forest floor, nutrient availability and native plants: a mesocosm study. Oecologia 155:509–518

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Holmes RL (1983) Computer-assisted quality control in tree-ring dating and measurement. Tree-Ring Bull 43:69–78

    Google Scholar 

  • Holmes RL (1999) User’s manual for program EDRM v6.00P. Laboratory of Tree-Ring Research, The University of Arizona, Tucson

    Google Scholar 

  • Hook DD (1984) Waterlogging tolerance of lowland tree species of the south. South J Appl For 8:136–149

    Google Scholar 

  • Iverson LR, Prasad AM, Matthews SN et al (2008) Estimating potential habitat for 134 eastern US tree species under six climate scenarios. For Ecol Manag 254:390–406

    Article  Google Scholar 

  • Kalnay EM, Kanamitsu R, Kistler W et al (1996) The NCEP/NCAR 40-year reanalysis project. Bull Amer Meteor Soc 77:437–470

    Article  Google Scholar 

  • Karl TR, Koscielny AJ (1982) Drought in the United States—1895–1981. J Climatology 2:313–329

    Article  Google Scholar 

  • Kimmins JP (2003) Forest ecology, 3rd edn. Prentice Hall, New York

    Google Scholar 

  • Kipfmueller KF, Swetnam TW (2001) Using dendrochronology to reconstruct the history of forest and woodland ecosystems. In: Egan D, Howell EA (eds) The historical ecology handbook: a restorationist’s guide to reference ecosystems. Island Press, Washington, DC, pp 199–228

    Google Scholar 

  • Koenig WD, Liebhold AM (2003) Regional impacts of periodical cicadas on oak radial increment. Can J For Res 33:1084–1089

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lee KE (1985) Earthworms, their ecology and relationships with soils and land use. Academic Press, Sydney

    Google Scholar 

  • Lorimer CG, Frelich LE (1989) A methodology for estimating canopy disturbance frequency and intensity in dense temperate forests. Can J For Res 19:651–663

    Article  Google Scholar 

  • Lorimer CG, Frelich LE, Nordheim EV (1988) Estimating gap origin probabilities for canopy trees. Ecology 69:778–785

    Article  Google Scholar 

  • Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102

    CAS  Google Scholar 

  • Morin H, Laprise D, Bergeron Y (1993) Chronology of spruce budworm outbreaks near Lake Duparquet, Abitibi Region, Quebec. Can J For Res 23:1497–1506

    Article  Google Scholar 

  • Nadelhoffer KJ, Aber JD, Melillo JM (1985) Fine roots, net primary production, and soil-nitrogen availability—a new hypothesis. Ecology 66:1377–1390

    Article  Google Scholar 

  • Orwig DA, Abrams MD (1997) Variation in radial growth responses to drought among species, site, and canopy strata. Trees Struct Funct 11:474–484

    Google Scholar 

  • Payette S, Fortin MJ, Morneau C (1996) The recent sugar maple decline in southern Quebec: probable causes deduced from tree rings. Can J For Res 26:1069–1078

    Article  Google Scholar 

  • Perkins DL, Swetnam TW (1996) A dendroecological assessment of whitebark pine in the Sawtooth-Salmon River region, Idaho. Can J For Res 26:2123–2133

    Article  Google Scholar 

  • Ponge JF, Delhaye L (1995) The heterogeneity of humus profiles and earthworm communities in a virgin beech forest. Biol Fert Soil 20:24–32

    Article  Google Scholar 

  • Runkle JR (1981) Gap regeneration in some old-growth forests of the eastern United States. Ecology 62:1041–1051

    Article  Google Scholar 

  • Scheu S, Parkinson D (1994a) Effects of earthworms on nutrient dynamics, carbon turnover and microorganisms in soils from cool temperate forests of the Canadian Rocky Mountains—laboratory studies. App Soil Ecol 1:113–125

    Article  Google Scholar 

  • Scheu S, Parkinson D (1994b) Effects of invasion of an aspen forest (Canada) by Dendrobaena-Octaedra (Lumbricidae) on plant-growth. Ecology 75:2348–2361

    Article  Google Scholar 

  • Schweingruber FH (1996) Tree rings and environment—dendroecology. Swiss Federal Institute for Forest, Snow and Landscape Research, Paul Haupt

    Google Scholar 

  • Speer JH, Swetnam TW, Wickman BE et al (2001) Changes in Pandora moth outbreak dynamics during the past 622 years. Ecology 82:679–697

    Article  Google Scholar 

  • Steinberg DA, Pouyat RV, Parmelee RW et al (1997) Earthworm abundance and nitrogen mineralization rates along an urban–rural land use gradient. Soil Biol Biochem 29:427–430

    Article  CAS  Google Scholar 

  • Stokes MA, Smiley TL (1996) An Introduction to tree-ring dating. University of Arizona Press, Tucson

    Google Scholar 

  • Suarez ER, Pelletier DM, Fahey TJ et al (2004) Effects of exotic earthworms on soil phosphorus cycling in two broadleaf temperate forests. Ecosystems 7:28–44

    Article  CAS  Google Scholar 

  • Swetnam TW, Lynch AM (1993) Multicentury, regional-scale patterns of western spruce budworm outbreaks. Ecol Monogr 63:399–424

    Article  Google Scholar 

  • Szlavecz K, Placella SA, Pouyat RV et al (2006) Invasive earthworm species and nitrogen cycling in remnant forest patches. Appl Soil Ecol 32:54–62

    Article  Google Scholar 

  • Tardif J, Brisson J, Bergeron Y (2001) Dendroclimatic analysis of Acer saccharum, Fagus grandifolia, and Tsuga canadensis from an old-growth forest, southwestern Quebec. Can J For Res 31:1491–1501

    Article  Google Scholar 

  • Tebaldi C, Hayhoe K, Arblaster JM et al (2006) Going to the extremes—an intercomparison of model-simulated historical and future changes in extreme events. Clim Change 79:185–211

    Article  Google Scholar 

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

    Article  Google Scholar 

  • USDA (1997) Soil survey of Cass County, Minnesota. National Cooperative Soil Survey, US Department of Agriculture and Minnesota Natural Resources Conservation Service, Washington, DC

    Google Scholar 

  • Veblen TT, Hadley KS, Reid MS et al (1991) Methods of detecting past spruce beetle outbreaks in Rocky Mountain subalpine forests. Can J For Res 21:242–254

    Article  Google Scholar 

  • Wood T, Bormann FH, Voigt GK (1984) Phosphorus cycling in a northern hardwood forest—biological and chemical control. Science 223:391–393

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi DK (1990) A simple method for cross-dating increment cores from living trees. Can J For Res 21:414–416

    Article  Google Scholar 

Download references

Acknowledgments

We thank Ian Aldrich, Ruth Baker, Chaïna Bapikee, Ryan Hueffmeier, Danny Margoles, and Julia Sawa for their assistance in the field, and Kenny Blumenfeld for his insightful comments on the most recent climate predictions for Minnesota. The comments of two anonymous reviewers and Daniel Simberloff improved this manuscript.

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  1. Evan R. Larson

    Present address: Department of Social Sciences/Geography, University of Wisconsin-Platteville, 1 University Plaza, Platteville, WI, 53818, USA

Authors and Affiliations

  1. Minnesota Dendroecology Laboratory, Department of Geography, University of Minnesota—Twin Cities, 414 Social Sciences Tower, 267—19th Avenue South, Minneapolis, MN, 55455, USA

    Evan R. Larson & Kurt F. Kipfmueller

  2. The Natural Resources Research Institute, Center for Water and the Environment, University of Minnesota Duluth, 5013 Miller Trunk Highway, Duluth, MN, 55811, USA

    Cindy M. Hale

  3. Department of Forest Resources, University of Minnesota—Twin Cities, 1530 North Cleveland Avenue, Saint Paul, MN, 55108, USA

    Lee E. Frelich & Peter B. Reich

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  1. Evan R. Larson
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Correspondence to Evan R. Larson.

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Larson, E.R., Kipfmueller, K.F., Hale, C.M. et al. Tree rings detect earthworm invasions and their effects in northern Hardwood forests. Biol Invasions 12, 1053–1066 (2010). https://doi.org/10.1007/s10530-009-9523-3

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