Ecosystems

, Volume 7, Issue 1, pp 1–12 | Cite as

Ecosystem Consequences of Exotic Earthworm Invasion of North Temperate Forests

  • Patrick J. Bohlen
  • Peter M. Groffman
  • Timothy J. Fahey
  • Melany C. Fisk
  • Esteban Suarez
  • Derek M. Pelletier
  • Robert T. Fahey
Article

Abstract

The invasion of north temperate forests by exotic species of earthworms is an important issue that has been overlooked in the study and management of these forests. We initiated research to address the hypothesis that earthworm invasion will have large consequences for nutrient retention and uptake in these ecosystems. In this special feature of Ecosystems, we present five papers describing results from our experiment. In this paper, we (a) introduce our experimental approach and conceptual model of how earthworms influence forest ecosystem processes, (b) describe the characteristics of the study areas and earthworm communities at our two study locations, and (c) provide a brief overview and synthesis of the main findings. The most dramatic effect of earthworm invasion was the loss of the forest floor at an undisturbed forest site, which altered the location and nature of nutrient cycling activity in the soil profile. Invasion changed soil total carbon (C) and phosphorus (P) pools, carbon–nitrogen (C:N) ratios, the loss and distribution of different soil P fractions, and the distribution and function of roots and microbes. Response to invasion varied with site characteristics and earthworm species. Our results suggest that exotic earthworm invasion is a significant factor that will influence the structure and function of northern temperate forest ecosystems over the next few decades. Regional evaluations of these forests will need to consider the presence or absence of earthworms along with other important ecosystem drivers, such as pollution, climate, and underlying soil characteristics.

Keywords

exotic species invasions carbon nitrogen phosphorus roots nutrient cycling forests 

References

  1. 1.
    Aber, JD, Nadelhoffer, KJ, Steudler, P, Melillo, JM 1989Nitrogen saturation in northern forest ecosystems.BioScience3937886Google Scholar
  2. 2.
    Aber, JD, Neilson, RP, McNulty, S, Lenihan, JM, Bachelet, D, Drapek, RJ 2001Forest processes and global environmental change; predicting the effects of individual and multiple stressors.BioScience5173551Google Scholar
  3. 3.
    Alban, DH, Berry, E 1994Effects of earthworm invasion on morphology, carbon, and nitrogen of a forest soils.Appl Soil Ecol12469CrossRefGoogle Scholar
  4. 4.
    Binkley, D 1986Forest nutrition and management.WileyNew YorkGoogle Scholar
  5. 5.
    Bohlen PJ, Groffman PM, Fahey TJ, Fisk MC. 2004. Influence of earthworm invasion on redistribution and retention of soil carbon and nitrogen in northern temperate forests. Ecosystems 7:Google Scholar
  6. 6.
    Bormann, FH, Likens, GE 1979Pattern and process in a forested ecosystem.Springer-VerlagNew YorkGoogle Scholar
  7. 7.
    Bradley, RL, Fyles, JW 1996Interactions between tree seedling roots and humus forms in the control of soil C and N cylcing.Biol Fertil Soils23709CrossRefGoogle Scholar
  8. 8.
    Brussaard L, Behan-Pelletier VM, Bignell DE, Brown VK, Didden W, Folgarait P, Fragoso C, Freckman DW, Gupta VVSR, Hattori T, and others. 1997. Biodiversity and ecosystem functioning in soil. Ambio 26:563–70.Google Scholar
  9. 9.
    Burtelow, AE, Bohlen, PJ, Groffman, PM 1997Influence of exotic earthworm invasion on soil organic matter, microbial biomass and denitrification potential in forest soils of the northeastern United States.Appl Soil Ecol9197202CrossRefGoogle Scholar
  10. 10.
    Canfield, R 1941Applications of the line intercept method in sampling range vegetation.J For3938894Google Scholar
  11. 11.
    Carlyle, JC 1986Nitrogen cycling in forested ecosystems.For Abstr4730836Google Scholar
  12. 12.
    Compton, JE, Boone, RD 2000Long-term impacts of agriculture on soil carbon and nitrogen in New England forests.Ecology81231430Google Scholar
  13. 13.
    Covington, WW 1981Changes in forest floor organic matter and nutrient content following clear cutting in northern hardwoods.Ecology62418Google Scholar
  14. 14.
    Davidson, EA 1995

    Linkages between carbon and nitrogen cycling and their implications for storage of carbon in terrestrial ecosystems.

    Woodwell, GMMackenzie, FT eds. Biotic feedbacks in the global climatic system: will the warming feed the warming?Oxford University PressNew York21932
    Google Scholar
  15. 15.
    Davidson, EA, Ackerman, I 1993Changes in soil carbon inventories following cultivation of previously untilled soils.Biogeochemistry2016193Google Scholar
  16. 16.
    Day, GM 1950Influence of earthworms on soil microorganisms.Soil Sci6917584Google Scholar
  17. 17.
    Dominguez J, Bohlen PJ, Parmelee RW. Effects of earthworms on movement of nitrogen into groundwater in agroecosystems. Ecosystems. Forthcoming.Google Scholar
  18. 18.
    Drake, JA, Mooney, HA 1989Biological invasions: a global perspective.WileyChichester: (UK)Google Scholar
  19. 19.
    Edwards, CA, Bohlen, PJ 1996Biology and ecology of earthworms.Chapman & HallLondon426Google Scholar
  20. 20.
    Ehrenfeld, JG, Kourtev, P, Huang, WZ 2001Changes in soil functions following invasions of exotic understory plants in deciduous forests.Ecol Appl111287300PubMedGoogle Scholar
  21. 21.
    Elliot, ET, Knight, D, Anderson, JM 1990Denitrification in eartworm casts and soil from pasture under different fertilizer and drainage regimes.Soil Biol Biochem226015CrossRefGoogle Scholar
  22. 22.
    Fahey, TJ 1998Recent changes in an upland forest in south-central New York.J Torrey Bot Soc125519Google Scholar
  23. 23.
    Fahey, TJ, Hughes, JW 1994Fine root dynamics in a northern hardwood forest ecosystem at Hubbard Brook Experimental Forest, NH.J Ecol8253348Google Scholar
  24. 24.
    Fahey, TJ, Battles, JJ, Wilson, GF 1997Response of early successional northern hardwood forests to changes in nutrient availability.Ecol Monogr68183212Google Scholar
  25. 25.
    Fain, JJ, Volk, TA, Fahey, TJ 1994Fifty years of change in an upland forest in south-central New York: general patterns.Bull Torrey Bot Club1211309Google Scholar
  26. 26.
    Fisk MC, Fahey TJ, Groffman PM, Bohlen PJ. 2004. Earthworm invasion, fine root distributions, and soil respiration in north temperate forests. Ecosystems 7:Google Scholar
  27. 27.
    Finzi, AC, van Breemen, N, Canham, CC 1998Canopy tree–soil interactions within temperate forests: species effects on soil carbon and nitrogen.Ecol Appl84406Google Scholar
  28. 28.
    Foster, D, Motzkin, G, Slater, B 1998Land-use history as long-term broad-scale disturbance: regional forest dynamics in central New England.Ecosystems196119CrossRefGoogle Scholar
  29. 29.
    Groffman, PM, Bohlen, PJ 1999Soil and sediment biodiversity: cross-system comparisons and large scale effects.BioScience4913948Google Scholar
  30. 30.
    Groffman PM, Bohlen PJ, Fisk MC, Fahey TJ. 2004. Exotic earthworm invasion and microbial biomass in temperate forest soils. Ecosystems 7:Google Scholar
  31. 31.
    Haimi, J, Boucelham, M 1991Influence of a litter feeding earthworm, Lumbricus rubellus, on soil processes in a simulated forest floor.Pedobiologia3524756Google Scholar
  32. 32.
    Haimi, J, Huhta, V 1990Effects of earthworms on decomposition processes in raw humus forest soil: a microcosm study.Biol Fertil Soils1017883Google Scholar
  33. 33.
    Hamburg, SP 1984

    Effects of forest growth on soil nitrogen and organic matter pools following release from subsistence agriculture.

    Stone, EL eds. Forest soils and treatment impacts. Proceedings of the Sixth North American Forest Soils Conference.University of TennesseeKnoxville (TH)14558
    Google Scholar
  34. 34.
    Hansen, A, Dale, V 2001Biodiversity in US forests under global climate change.Ecosystems41613CrossRefGoogle Scholar
  35. 35.
    Hansen, AJ, Neilson, RP, Dale, VH, Flather, CH, Iverson, LR, Currie, DJ, Shafer, S, Cook, R, Bartlein, PJ 2001Global change in forests: responses of species, communities, and biomes.BioScience5176579Google Scholar
  36. 36.
    Harrison, RB, Gessel, SP, Zabowski, D, Henry, CL, Xue, D, Cole, DW, Compton, JE 1996Mechanisms of negative impacts of three forest treatments on nutrient availability.Soil Sci Soc Am J60162228Google Scholar
  37. 37.
    Hendrick, RL, Pregitzer, KS 1992The demography of fine roots in a northern hardwood forest.Ecology731094104Google Scholar
  38. 38.
    Hooper DU, Bignel DE, Brown VK, Brussaard L, Dangerfield JM, Wall DH, Wardle DA, Coleman DC, Giller KE, Lavelle P, and others. 2000. Interactions between aboveground and belowground biodiversity in terrestrial ecosystems: patterns, mechanisms, and feedbacks. BioScience 50:1049–61.Google Scholar
  39. 39.
    Houghton, RA 1991The worldwide extent of land-use change.BioScience4430513Google Scholar
  40. 40.
    Ingestad, T, Agren, GI 1992Theories and methods on plant nutrition and growth.Plant Physiol8417784CrossRefGoogle Scholar
  41. 41.
    Iverson, LR, Prasad, AM 2001Potential changes in tree species richness and forest community types following climate change.Ecosystems418699CrossRefGoogle Scholar
  42. 42.
    James, SW 1995

    Systematics, biogeography, and ecology of nearctic earthworms from eastern, central, southern and southwestern United States.

    Hendrix, PF eds. Earthworm ecology and biogeography in North America.LewisBoca Raton (FL)2952
    Google Scholar
  43. 43.
    Jordan, D, Hubbard, VC, Ponder, R Jr, Berry, EC 2000The influence of soil compaction and the removal of organic matter on two native earthworms and soil properties in an oak–hickory forest.Biol Fertil Soils313238PubMedGoogle Scholar
  44. 44.
    Keyser, AR, Kimball, JS, Nemani, RR, Running, SW 2000Simulating the effects of climate change on the carbon balance of North American high-latitude forests.Global Change Biol618595CrossRefGoogle Scholar
  45. 45.
    Knight, D, Elliot, PW, Anderson, JM, Scholefield, P 1992The role of earthworms in managed, permanent pastures in Devon, England.Soil Biol Biochem24151117CrossRefGoogle Scholar
  46. 46.
    Langmaid, KK 1964Some effects of earthworm invasion in virgin podzols.Can J Soil Sci44347Google Scholar
  47. 47.
    Lavelle, P, Martin, A 1992Small-scale and large-scale effects of endogeic earthworms on soil organic matter dynamics in soils of the humid tropics.Soil Biol Biochem2414918CrossRefGoogle Scholar
  48. 48.
    Lawrence, B, Fisk, MC, Fahey, TJ, Suarez, ER 2003Influence of non-native earthworms on mycorrhizal colonization of sugar maple (Acer saccharum Marsh).New Phytol.157145153CrossRefGoogle Scholar
  49. 49.
    Lawrence, GB, Lovett, GM, Baevsky, YH 2000Atmospheric deposition and watershed nitrogen export along an elevational gradient in the Catskill Mountains, New York.Biogeochemistry502143CrossRefGoogle Scholar
  50. 50.
    Lopez-Hernandez, D, Burnham, CP 1974The effect of pH on phosphate adsorption in soils.J Soil Sci2520116Google Scholar
  51. 51.
    Lovett, GM, Rueth, H 1999Potential nitrogen mineralization and nitrification in american beech and sugar maple stands along a nitrogen deposition gradient in the northeastern U.S.Ecol Appl9133044Google Scholar
  52. 52.
    Lunt, HA, Jacobson, GM 1944The chemical composition of earthworm casts.Soil Sci58367375Google Scholar
  53. 53.
    Mack, RN, Simberloff, D, Bazaz, FA 2000Biotic invasions: causes, epidemiology, global consequences, and control.Ecol Appl10689710Google Scholar
  54. 54.
    Martin, A 1991Short- and long-term effects of the endogeic earthworm Millsonia anomala (Omodeo) (Megascolescidae, Oligochaeta) of tropical savannas, on soil organic matter.Biol Fertil Soils112348Google Scholar
  55. 55.
    Mugasha, AG, McDonald, SE, Pluth, DJ 1996Needle litter responses of peatland tamarack and black spruce to fertilization of minerotrophic peatland sites.For Ecol Manage8725764CrossRefGoogle Scholar
  56. 56.
    Neilson, GE, Hole, FE 1964Earthworms and the development of coprogenous A1 horizons in forest soils of Wisconsin.Soil Sci Soc Am Proc2842630Google Scholar
  57. 57.
    Papadopol, CS 2000Impacts of climate warming on forests in Ontario: options for adaptation and mitigation.For Chron7613949Google Scholar
  58. 58.
    Paré, D, Bernier, B 1989aOrigin of the phosphorus deficiency observed in declining sugar maple stands in the Quebec Appalachians.Can J For Res192434Google Scholar
  59. 59.
    Paré, D, Bernier, B 1989bPhosphorus-fixing potential of Ah and H horizons subjected to acidification.Can J For Res191324Google Scholar
  60. 60.
    Paré, D, Bernier, B 1989cChanges in phosphorus nutrition of sugar maple along a topographic gradient in the Quebec Appalachians.Can J For Res191357Google Scholar
  61. 61.
    Parle, JN 1963A microbiological study of earthworm casts.J Gen Microbiol31135Google Scholar
  62. 62.
    Pastor, J, Aber, JB, McClaugherty, CA, Melillo, JM 1984Aboveground production and N and P cycling along a nitrogen mineralization gradient on Blackhawk Island, Wisconsin.Ecology6525668Google Scholar
  63. 63.
    Pastor, J, Dewey, B, Naiman, RJ, MacInnes, PF, Cohen, Y 1993Moose browsing and soil fertility in the boreal forests of Isle Royale National Park.Ecology7446780Google Scholar
  64. 64.
    Raw, F 1959Estimating earthworm populations by using formalin.Nature18416611662Google Scholar
  65. 65.
    Reynolds, JW 1994The distribution of the earthworms (Oligochaeta) of Indiana: a case for the Post Quaternary Introduction Theory for megadrile migration in North America.Megadrilogica51332Google Scholar
  66. 66.
    Robinson, CH, Ineson, P, Piearce, TG, Rowland, AP 1992Nitrogen mobilization by earthworms in limed peat soils under Picea sitchensis.J Appl Ecol2922637Google Scholar
  67. 67.
    Ryan, DF, Bormann, FH 1982Nutrient resorption in northern hardwood forests.BioScience322932Google Scholar
  68. 68.
    Satchell, JE 1967

    Lumbricidae.

    Burgess, ARaw, F eds. Soil biology.Academic PressLondon259322
    Google Scholar
  69. 69.
    Scheu, S, Parkinson, D 1994aEffects of earthworms on nutrient dynamics, carbon turnover and microorganisms in soils from cool temperate forests of the Canadian Rocky Mountains—laboratory studies.Appl Soil Ecol111325CrossRefGoogle Scholar
  70. 70.
    Scheu, S, Parkinson, D 1994bEffects of invasion of an aspen forest (Canada) by Dendrobaena octaedra (Lumbricidae) on plant growth.Ecology75234861Google Scholar
  71. 71.
    Scheu, S, Wolters, V 1991Influence of fragmentation and bioturbation on the decomposition of 14C-labeled beech leaf litter.Soil Biol Biochem23102934CrossRefGoogle Scholar
  72. 72.
    Schlesinger, WH 1995

    Soil respiration and changes in soil carbon stocks.

    Woodwell, GMMackenzie, FT eds. Biotic feedbacks in the global climatic system: will the warming feed the warming?Oxford University PressNew York15968
    Google Scholar
  73. 73.
    Shipitalo, MJ, Edwards, WM, Redmond, CE 1994Comparison of water movement and quality in earthworm burrows and pan lysimeters.J Environ Qual2334551Google Scholar
  74. 74.
    Steinberg, DA, Pouyat, RV, Parmelee, RW, Groffman, PM 1996Earthworm abundance and nitrogen mineralization rates along an urban-rural land use gradient.Soil Biol Biochem2942730CrossRefGoogle Scholar
  75. 75.
    Suarez ER, Fahey TJ, Groffman PM, Bohlen PJ, Fisk MC. 2004. Effects of exotic earthworms on soil phosphorus cycling in two broadleaf temperate forests Ecosystems 7:Google Scholar
  76. 76.
    Subler, S, Baranski, CM, Edwards, CA 1997Earthworm additions increased short-term nitrogen availability and leaching in two grain-crop agroecosystems.Soil Biol Biochem2941321Google Scholar
  77. 77.
    Svensson, BH, Bostrom, U, Klemedtson, L 1986Potential for higher rates of denitrification in earthworm casts than in the surrounding soil.Biol Fertil Soils21479Google Scholar
  78. 78.
    Tomlin, AD, Shipitalo, MJ, Edwards, WM, Protz, R 1995

    Earthworms and their influence on soil structure and infiltration.

    Hendrix, PF eds. Earthworm ecology and biogeography in North America.LewisBoca Raton (FL)15984
    Google Scholar
  79. 79.
    Vitousek, PM 1994Beyond global warming: ecology and global change.Ecology75186176Google Scholar
  80. 80.
    Vitousek, PM, D’Antonio, CM, Loope, LL, Rejmanek, M, Westbrooks, R 1997Introduced species: a significant component of human-caused global change.NZ J Ecol21116Google Scholar
  81. 81.
    Volk, TA, Fahey, TJ 1994Fifty-three years of change in an upland forest in south-central New York: growth, mortality and recruitment.Bull Torrey Bot Soc1211407Google Scholar
  82. 82.
    Walbridge, M, Richardson, CJ, Swank, WT 1991Vertical distribution of biological and geochemical phosphorus sub-cycles in two southern Appalachian forest soils.Biogeochemistry136185Google Scholar
  83. 83.
    Waring, RH, Pitman, GB 1985Modifying lodgepole pine stands to change susceptibility to mountain pine beetle attack.Ecology6688997Google Scholar
  84. 84.
    Wienand, KT, Stock, WD 1995Long-term phosphorous fertilization effects on the litter dynamics of an age sequence of Pinus elliottic plantations in the southern Cape of South Africa.For Ecol Manage7513546CrossRefGoogle Scholar
  85. 85.
    Williams, M 1990

    Deforestation.

    Turner, BClark, WKates, RRichards, JMathews, JMeyer, W eds. The earth as transformed by human action.Cambridge University PressCambridge (UK)179201
    Google Scholar
  86. 86.
    Wood, T, Bormann, FH, Voigt, GK 1984Phosphorus cycling in a northern hardwood forest: biological and chemical controls.Science273913Google Scholar
  87. 87.
    Yanai, RD 1992Phosphorous budget of a 70-yr-old northern hardwood forest.Biogeochemistry17122Google Scholar
  88. 88.
    Zak, DR, Host, GE, Pregitzer, KS 1989Regional variability in nitrogen mineralization, nitrification and overstory biomass in northern Lower Michigan.Can J For Res1915216Google Scholar
  89. 89.
    Zhou, L, Shabanov, NV, Myneni, RB, Tucker, CJ, Kaufmann, RK, Slayback, D 2001Variations in northern vegetation activity inferred from satellite data of vegetation index during 1981 to 1999.J Geophys Res – Atmos1062006983CrossRefGoogle Scholar

Copyright information

© Springer-Verlag New York, Inc. 2004

Authors and Affiliations

  • Patrick J. Bohlen
    • 1
  • Peter M. Groffman
    • 2
  • Timothy J. Fahey
    • 3
  • Melany C. Fisk
    • 3
    • 4
  • Esteban Suarez
    • 3
  • Derek M. Pelletier
    • 3
  • Robert T. Fahey
    • 3
  1. 1.Archbold Biological Station, Lake Placid, Florida 33852USA
  2. 2.Institute of Ecosystem Studies, Box AB, Millbrook, New York 12545USA
  3. 3.Department of Natural ResourcesCornell University, Ithaca, New York 14853USA
  4. 4.Department of Biology, Appalachian State University, Boone, North Carolina 28608-2027USA

Personalised recommendations