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Exotic Earthworm Invasion and Microbial Biomass in Temperate Forest Soils

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Abstract

Invasion of north temperate forest soils by exotic earthworms has the potential to alter microbial biomass and activity over large areas of North America. We measured the distribution and activity of microbial biomass in forest stands invaded by earthworms and in adjacent stands lacking earthworms in sugar maple-dominated forests in two locations in New York State, USA: one with a history of cultivation and thin organic surface soil horizons (forest floors) and the other with no history of cultivation and a thick (3–5 cm) forest floor. Earthworm invasion greatly reduced pools of microbial biomass in the forest floor and increased pools in the mineral soil. Enrichment of the mineral soil was much more marked at the site with thick forest floors. The increase in microbial biomass carbon (C) and nitrogen (N) in the mineral soil at this site was larger than the decrease in the forest floor, resulting in a net increase in total soil profile microbial biomass in the invaded plots. There was an increase in respiration in the mineral soil at both sites, which is consistent with a movement of organic matter and microbial biomass into the mineral soil. However, N-cycle processes (mineralization and nitrification) did not increase along with respiration. It is likely that the earthworm-induced input of C into the mineral soil created a microbial “sink” for N, preventing an increase in net mineralization and nitrification and conserving N in the soil profile.

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References

  1. DH Alban E Berry (1994) ArticleTitleEffects of earthworm invasion on morphology, carbon, and nitrogen of a forest soil. Appl Soil Ecol 1 243–9 Occurrence Handle10.1016/0929-1393(94)90015-9

    Article  Google Scholar 

  2. JM Anderson (2000) Food web functioning and ecosystem processes: problems and perceptions of scaling. DC Coleman PF Hendrix (Eds) Invertebrates as webmasters in ecosystems. CAB International Wallingford, (UK) 3–24

    Google Scholar 

  3. J Bauhus PK Khanna (1999) The significance of microbial biomass in forest soils N Rastin J Bauhus (Eds) Going underground: ecological studies in forest soils Research Signpost Trivandrum (India) 77–100

    Google Scholar 

  4. MH Beare RW Parmelee PF Hendrix W Cheng DC Coleman DA Crossley Jr (1992) ArticleTitleMicrobial and faunal interactions and effects on litter nitrogen and decomposition in agro-ecosystems. Ecol Monogr 62 569–91 Occurrence Handle1:STN:280:DC%2BD3c3hvVWktg%3D%3D Occurrence Handle10757248

    CAS  PubMed  Google Scholar 

  5. PJ Bohlen CA Edwards (1995) ArticleTitleEarthworm effects on N dynamics and soil respiration in microcosms receiving organic and inorganic nutrients. Soil Biol Biochem 27 341–8 Occurrence Handle10.1016/0038-0717(94)00184-3 Occurrence Handle1:CAS:528:DyaK2MXksVSrtLY%3D

    Article  CAS  Google Scholar 

  6. PJ Bohlen PM Groffman TJ Fahey CT Driscoll TG Siccama (2001) ArticleTitlePlant–soil–microbial interactions in a northern hardwood forest. Ecology 82 965–78

    Google Scholar 

  7. PJ Bohlen PM Groffman TJ Fahey MC Fisk (2004a) ArticleTitleEcosystem consequences of exotic earthworm invasion of north temperate forests. Ecosystems 7 .

    Google Scholar 

  8. PJ Bohlen PM Groffman TJ Fahey M Fisk (2004b) ArticleTitleInfluence of earthworm invasion on redistribution and retention of soil carbon and nitrogen in northern temperate forests. Ecosystem 7 .

    Google Scholar 

  9. PJ Bohlen RW Parmelee MF Allen QM Ketterings (1999) ArticleTitleDifferential effects of earthworms on nitrogen cycling from various nitrogen-15-labeled substrates. Soil Sci Soc Am J 63 882–90 Occurrence Handle1:CAS:528:DyaK1MXmsFCnsrY%3D

    CAS  Google Scholar 

  10. GG Brown I Barois P Lavelle (2000) ArticleTitleRegulation of soil organic matter dynamics and microbial activity in the drilosphere and the role of interactions with other edaphic functional domains. Eur J Soil Biol 3–4 177–98 Occurrence Handle10.1016/S1164-5563(00)01062-1

    Article  Google Scholar 

  11. 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.

  12. AE Burtelow PJ Bohlen PM Groffman (1998) ArticleTitleInfluence 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 Occurrence Handle10.1016/S0929-1393(98)00075-4

    Article  Google Scholar 

  13. MA Callaham JM Blair (1999) ArticleTitleInfluence of differing land management on the invasion of North American tallgrass prairie soils by European earthworms. Pedobiologia 43 507–12

    Google Scholar 

  14. MA Callaham JM Blair PF Hendrix (2001) ArticleTitleDifferent behavioral patterns of the earthworms Octolasion tyrtaeum and Diplocardia spp. in tallgrass prairie soils: potential influences on plant growth. Biol Fertil Soils 34 49–56

    Google Scholar 

  15. MA Callaham PF Hendrix (1998) ArticleTitleImpact of earthworms (Diplocardia: Megascolecidae) on cycling and uptake of nitrogen in coastal plain forest soils from northwest Florida, USA. Appl Soil Ecol 9 233–9 Occurrence Handle10.1016/S0929-1393(97)00048-6

    Article  Google Scholar 

  16. DC Coleman EP Odum DA Crossley Jr (1992) ArticleTitleSoil biology, soil ecology, and global change. Biol Fertil Soils 14 104–11

    Google Scholar 

  17. O Daniel JM Anderson (1992) ArticleTitleMicrobial biomass and activity in contrasting soil materials after passage through the gut of the earthworm Lumbricus rubellus Hoffmeister. Soil Biol Biochem 23 465–70 Occurrence Handle10.1016/0038-0717(92)90209-G

    Article  Google Scholar 

  18. W Devliegher W Verstraete (1995) ArticleTitle Lumbricus terrestris in a soil core experiment: nutrient-enrichment processes (NEP) and gut-associated processes (GAP) and their effect on microbial biomass and activity. Soil Biol Biochem 12 1573–80 Occurrence Handle10.1016/0038-0717(95)00090-2

    Article  Google Scholar 

  19. CA Edwards PJ. Bohlen (1996) Biology and ecology of earthworms. Chapman and Hall London 426

    Google Scholar 

  20. TJ Fahey (1998) ArticleTitleRecent changes in an upland forest in south-central New York. J Torrey Bot Soc 121 51–7

    Google Scholar 

  21. JJ Fain TA Volk TJ Fahey (1994) ArticleTitleFifty years of change in an upland forest in south-central New York: general patterns. Bull Torrey Bot Club 121 130–9

    Google Scholar 

  22. MC Fisk TJ Fahey PM Groffman PJ Bohlen (2004) ArticleTitleEarthworm invasion, fine root distributions and soil respiration in north temperate forests. Ecosystems 7 .

    Google Scholar 

  23. GE Gates (1976) ArticleTitleMore on earthworm distribution in North America. Proc Biol Soc Wash 89 467–76

    Google Scholar 

  24. JS Glitzenstein CD Canham MJ McDonnell DR Strong (1990) ArticleTitleEffects of environment and land-use history on upland forests of the Cary Arboretum. Bull Torrey Bot Club 117 106–22

    Google Scholar 

  25. JH Gorres MC Savin JA Amador (1997) ArticleTitleDynamics of carbon and nitrogen mineralization, microbial biomass, and nematode abundance within and outside the burrow walls of anecic earthworms (Lumbricus terrestris). Soil Sci 162 666–71 Occurrence Handle1:CAS:528:DyaK2sXmsV2rsLo%3D

    CAS  Google Scholar 

  26. PM Groffman PJ Bohlen (1999) ArticleTitleSoil and sediment biodiversity: cross-system comparisons and large-scale effects. Bioscience 49 139–48

    Google Scholar 

  27. PM Groffman CG. Jones (2000) Soil invertebrates in ecosystems: Do they matter to global change? DC Coleman PF Hendrix (Eds) Invertebrates as webmasters in ecosystems. CAB International Wallingford (UK) 316–26

    Google Scholar 

  28. J Haimi V Huhta (1990) ArticleTitleEffects of earthworms on decomposition processes in raw humus forest soil: a microcosm study. Biol Fertil Soils 10 178–83

    Google Scholar 

  29. SW James (1995) Systematics, biogeography, and ecology of neararctic earthworms from Eastern, Central, Southern, and Southwestern USA. PF Hendrix (Eds) Earthworm ecology and biogeography in North America. Lewis Boca Raton (FL) 29–51

    Google Scholar 

  30. DS Jenkinson DS Powlson (1976) ArticleTitleThe effects of biocidal treatments on metabolism in soil. V. A method for measuring soil biomass. Soil Biol Biochem 8 209–13 Occurrence Handle1:CAS:528:DyaE28Xkslens7c%3D

    CAS  Google Scholar 

  31. SL Lachnicht PF Hendrix (2001) ArticleTitleInteraction of the earthworm Diplocardia mississippiensis (Megascolecidae) with microbial and nutrient dynamics in a subtropical Spodosol. Soil Biol Biochem 33 1411–7 Occurrence Handle10.1016/S0038-0717(01)00049-9 Occurrence Handle1:CAS:528:DC%2BD3MXlt1Slt70%3D

    Article  CAS  Google Scholar 

  32. X Li MC Fisk TJ Fahey PJ Bohlen (2003) ArticleTitleInfluence of earthworm invasion on soil microbial biomass and activity in a northern hardwood forest. Soil Biol Biochem 34 1929–37 Occurrence Handle10.1016/S0038-0717(02)00210-9

    Article  Google Scholar 

  33. MA McLean D Parkinson (1997a) ArticleTitleChanges in structure, organic matter and microbial activity in pine forest soil following the introduction of Dendrobaena octaedra (Oligochaeta, Lumbricidae). Soil Biol Biochem 29 537–40 Occurrence Handle1:CAS:528:DyaK2sXktFCksb4%3D

    CAS  Google Scholar 

  34. MA McLean D Parkinson (1997b) ArticleTitleSoil impacts of the epigeic earthworm Dendrobaena octaedra on organic matter and microbial activity in lodgepole pine forest. Can J For Res 27 1907–13 Occurrence Handle10.1139/cjfr-27-12-1907

    Article  Google Scholar 

  35. MA McLean D Parkinson (2000) ArticleTitleField evidence of the effects of the epigeic earthworm Dendrobaena octaedra on the microfungal community in pine forest floor. Soil Biol Biochem 32 351–60 Occurrence Handle10.1016/S0038-0717(99)00161-3 Occurrence Handle1:CAS:528:DC%2BD3cXhs1Smt70%3D

    Article  CAS  Google Scholar 

  36. HA Mooney PM Vitousek PA Matson (1987) ArticleTitleExchange of materials between terrestrial ecosystems and the atmosphere. Science 238 926–32

    Google Scholar 

  37. JN Parle (1963) ArticleTitleA microbiological study of earthworm casts. J Gen Microbiol 31 13–5 Occurrence Handle1:CAS:528:DyaF3sXkt1emt78%3D

    CAS  Google Scholar 

  38. EA Paul FE Clark (1996) Soil microbiology and biochemistry, 2nd edition. Academic New York

    Google Scholar 

  39. P Saetre (1998) ArticleTitleDecomposition, microbial community structure, and earthworm effects along a birch–spruce soil gradient. Ecology 79 834–46 Occurrence Handle1:CAS:528:DyaK28XlvVCqt7Y%3D Occurrence Handle8804245

    CAS  PubMed  Google Scholar 

  40. InstitutionalAuthorNameSAS (1988) SAS/STAT user’s guide, Release 6.03. SAS Institute Incorporated Cary (NC)

    Google Scholar 

  41. S Scheu D Parkinson (1994a) ArticleTitleEffects of earthworms on nutrient dynamics, carbon turnover and microorganisms in soils from cool temperate forests of the Canadian Rocky Mountains: laboratory studies. Appl Soil Ecol 1 113–25 Occurrence Handle10.1016/0929-1393(94)90031-0

    Article  Google Scholar 

  42. S Scheu D Parkinson (1994b) ArticleTitleEffects of an invasion of an aspen woodland (Alberta, Canada) by Dendrobaena octaedra on plant growth. Ecology 75 2348–61

    Google Scholar 

  43. G Scholle V Wolters RG Joergensen (1992) ArticleTitleEffects of mesofauna exclusion on the microbial biomass in two model profiles. Biol Fertil Soils 12 253–60

    Google Scholar 

  44. Secor W, Koehler LR, Kinsman DF, Benson WE, Cline MG, Moran WJ, Leighty RG, Johnsgard GA, Marin IL, Donner HL, and others. 1955. Soil survey of Dutchess County, New York. Series 1939, No. 23. USDA Soil Conservation Service and Cornell University Agricultural Experiment Station. 178 p.

  45. C Shaw S Pawluk (1986) ArticleTitleFaecal microbiology of Octolasion tyrtaeum, Aporrectodea turgida and Lumbricus terrestris and its relation to the carbon budgets of three artificial soils. Pedobiologia 29 377–89

    Google Scholar 

  46. DA Steinberg RV Pouyat RW Parmelee PM Groffman (1997) ArticleTitleEarthworm abundance and nitrogen mineralization rates along an urban–rural land use gradient. Soil Biol Biochem 29 427–30 Occurrence Handle1:CAS:528:DyaK2sXktFCgu7g%3D

    CAS  Google Scholar 

  47. E Suàrez TJ Fahey PM Groffman PJ Bohlen MC Fisk (2004) ArticleTitleEffects of exotic earthworms on soil phosphorus cycling in two broadleaf temperate forests. Ecosystems 7 .

    Google Scholar 

  48. SC Tiwari RR Mishra (1993) ArticleTitleFungal abundance and diversity in earthworm casts and in uningested soil. Biol Fertil Soils 16 131–4

    Google Scholar 

  49. TA Volk TJ Fahey (1994) ArticleTitleFifty-three years of change in an upland forest in south-central New York: growth, mortality and recruitment. Bull Torrey Bot Soc 121 140–7

    Google Scholar 

  50. RP Voroney EA Paul (1984) ArticleTitleDetermination of kc and kn in situ for calibration of the chloroform fumigation–incubation method. Soil Biol Biochem 16 9–14 Occurrence Handle10.1016/0038-0717(84)90117-2 Occurrence Handle1:CAS:528:DyaL2cXksFeru7c%3D

    Article  CAS  Google Scholar 

  51. DH Wall JC Moore (1999) ArticleTitleInteractions underground: soil biodiversity, mutualism, and ecosystem processes. Bioscience 49 109–17

    Google Scholar 

  52. V Wolters RG Joergensen (1992) ArticleTitleMicrobial carbon turnover in beech forest soils worked by Aporrectodea caliginosa (Savigny) (Oligochaeta: Lumbricidae). Soil Biol Biochem 24 171–7 Occurrence Handle10.1016/0038-0717(92)90274-2

    Article  Google Scholar 

  53. DR Zak D Tilman R Parmenter CW Rice FM Fisher J Vose D Milchunas W Martin (1994) ArticleTitlePlant production and soil microorganisms in late-successional ecosystems: a continental-scale study. Ecology 75 2333–47

    Google Scholar 

  54. BG Zhang GT Li TS Shen JK Wang Z Sun (2000) ArticleTitleChanges in microbial biomass C, N, and P and enzyme activities in soil incubated with the earthworms Metaphire guillemi or Eisenia fetida. Soil Biol Biochem 32 2055–62 Occurrence Handle10.1016/S0038-0717(00)00111-5 Occurrence Handle1:CAS:528:DC%2BD3MXpvFSr

    Article  CAS  Google Scholar 

  55. QL Zhang PF Hendrix (1995) ArticleTitleEarthworm (Lumbricus rubellus and Aporrectodea caliginosa) effects on carbon flux in soil. Soil Sci Soc Am J 59 816–23 Occurrence Handle1:CAS:528:DyaK2MXlvFyqsLc%3D

    CAS  Google Scholar 

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Acknowledgements

We thank Isabella Fiorentino, Emilie Stander, and Abraham Parker for help with fieldwork and laboratory and data analysis. This research was supported by a grant from the National Science Foundation (DEB-9726869).

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Correspondence to Peter M. Groffman.

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Groffman, P., Bohlen, P., Fisk, M. et al. Exotic Earthworm Invasion and Microbial Biomass in Temperate Forest Soils . Ecosystems 7, 45–54 (2004). https://doi.org/10.1007/s10021-003-0129-9

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