Skip to main content

Advertisement

Log in

Do non-native earthworms in Southeast Alaska use streams as invasional corridors in watersheds harvested for timber?

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Exotic earthworms from Europe and Asia have invaded previously earthworm-free areas of North America where they consume leaf litter, mix soil horizons, and alter nutrient cycling. Primarily, earthworm introductions occur through human activities; we hypothesized that the combination of logging (i.e., road construction and soil disturbance) and stream transport (i.e., hydrochory) allows earthworms to invade new ecosystems and spread within watersheds. On Prince of Wales Island, AK, we surveyed riparian zones in 11 watersheds with varying timber harvest intensity for terrestrial oligochaetes. Additionally, common invasive earthworms were experimentally submerged in a local stream to test for tolerance to prolonged immersion: all taxa survived immersion for at least 6 days. Using principal components analysis, watershed and harvest variables describing the watersheds upstream of our sampled riparian areas were reduced to two principal components describing harvest intensity (PC1) and harvest style (PC2). Logistic models successfully predicted earthworm abundance (r 2 = 0.70) from PC1, which indicated that watersheds with older, intense upstream timber harvest contained larger earthworm populations. Earthworm species richness was best predicted by PC2 (r 2 = 0.39), which suggested that earthworm communities in watersheds containing large clear-cut stands were more species-rich. Collectively, these results suggest that (1) invasive earthworms may use streams for dispersal and (2) upstream introductions via timber harvest can initiate downstream earthworm invasions. Hydrochory would allow invasive earthworms to spread at rates (tens of km d−1) that are much greater than previously reported rates of terrestrial spread (5–10 m y−1). Effective control of exotic earthworms in riparian zones will require watershed-level management and surveillance.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bardgett RD, Anderson JM, Behan-Pelletier V, Brussaard L, Coleman DC, Ettema C, Moldenke A, Schimel JP, Wall DH (2001) The influence of soil biodiversity on hydrological pathways and the transfer of materials between terrestrial and aquatic ecosystems. Ecosystems 4:421–429. doi:10.1007/s10021-001-0020-5

    Article  Google Scholar 

  • Blair JM, Parmelee RW, Lavelle P (1995) Influences of earthworms on biogeochemistry. In: Hendrix PF (ed) Earthworm ecology and biogeography in North America. CRC Press, Boca Raton, FL, pp 127–158

    Google Scholar 

  • Bohlen PJ, Pelletier DM, Groffman PM, Fahey TJ, Fisk MC (2004a) Influence of earthworm invasion on redistribution and retention of soil carbon and nitrogen in northern temperate forests. Ecosystems 7:13–27. doi:10.1007/s10021-003-0127-y

    Article  CAS  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 2:427–435. doi:10.1890/1540-9295(2004)002[0427:NIEAAO]2.0.CO;2

    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. doi:10.1016/S0929-1393(98)00075-4

    Article  Google Scholar 

  • Callaham MA, González G, Hale CM, Heneghan L, Lachnicht SL, Zou X (2006) Policy and management responses to earthworm invasions in North America. Biol Invasions 8:1317–1329. doi:10.1007/s10530-006-9016-6

    Article  Google Scholar 

  • Cameron EK, Bayne EM, Coltman DW (2008) Genetic structure of invasive earthworms Dendrobaena octaedra in the boreal forest of Alberta: insights into introduction mechanism. Mol Ecol 17:1189–1197. doi:10.1111/j.1365-294X.2007.03603.x

    Article  CAS  PubMed  Google Scholar 

  • Costello DM, Lamberti GA (2008) Non-native earthworms in riparian soils increase nitrogen flux into adjacent aquatic ecosystems. Oecologia 158:499–510. doi:10.1007/s00442-008-1149-0

    Article  PubMed  Google Scholar 

  • Costello DM, Lamberti GA (2009) Biological and physical effects of non-native earthworms on nitrogen cycling in riparian soils. Soil Biol Biochem 41:2230–2235. doi:10.1016/j.soilbio.2009.08.007

    Article  CAS  Google Scholar 

  • Dash M (1990) Oligochaeta: Enchytraeidae. In: Dindal DL (ed) Soil biology guide. Wiley, New York, NY, pp 311–340

    Google Scholar 

  • Davis CA, Austin JE, Buhl DA (2006) Factors influencing soil invertebrate communities in riparian grasslands of the central Platte River floodplain. Wetlands 26:438–454. doi:10.1672/0277-5212(2006)26[438:FISICI]2.0.CO;2

    Article  Google Scholar 

  • Deal RL, Hennon PE, Orlikowska EH, D’Amore DV (2004) Stand dynamics of mixed red alder—conifer forests of southeast Alaska. Can J Forest Res 34:969–980. doi:10.1139/X04-002

    Article  Google Scholar 

  • Dymond P, Scheu S, Parkinson D (1997) Density and distribution of Dendrobaena octaedra (Lumbricidae) in aspen and pine forests in the Canadian Rocky Mountains (Alberta). Soil Biol Biochem 29:265–273. doi:10.1016/S0038-0717(96)00052-1

    Article  Google Scholar 

  • Edwards CA (2004) Earthworm ecology. CRC Press, Boca Raton, FL

    Book  Google Scholar 

  • Fender WM (1995) Native earthworms of the Pacific Northwest: an ecological overview. In: Hendrix PF (ed) Earthworm ecology and biogeography in North America. CRC Press, Boca Raton, FL, pp 53–66

    Google Scholar 

  • Fender WM, McKey-Fender D (1990) Oligochaeta: Megascolecidae and other earthworms from Western North America. In: Dindal DL (ed) Soil biology guide. Wiley, New York, NY, pp 357–386

    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 2006:1235–1245. doi:10.1007/s10530-006-9019-3

    Article  Google Scholar 

  • Greiner HG, Costello DM, Tiegs SD (2010) Allometric estimation of earthworm ash-free dry mass from diameters and lengths of select Megascolecid and Lumbricid species. Pedobiologia 53:247–252. doi:10.1016/j.pedobi.2009.12.004

    Article  Google Scholar 

  • Hale CM (2007) Earthworms of the great lakes. Kollath and Stensaas, Duluth, MN

    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. doi:10.1890/03-5345

    Article  Google Scholar 

  • Hale CM, Frelich LE, Reich PB, Pastor J (2005b) Effects of European earthworm invasion on soil characteristics in Northern hardwood forests of Minnesota, USA. Ecosystems 8:911–927. doi:10.1007/s10021-005-0066-x

    Article  CAS  Google Scholar 

  • Hendrix PF, Callaham MA, Drake JM, Huang C-Y, James SW, Snyder BA, Zhang W (2008) Pandora’s box contained bait: the global problem of introduced earthworms. Annu Rev Ecol Evol Syst 39:593–613. doi:10.1146/annurev.ecolsys.39.110707.173426

    Article  Google Scholar 

  • Kalisz PJ, Dotson DB (1989) Land-use history and the occurrence of exotic earthworms in the mountains of Eastern Kentucky. Am Midl Nat 122:288–297. doi:10.1023/A:1010048909563

    Article  Google Scholar 

  • Keller RP, Cox AN, Van Loon C, Lodge DM, Herborg L-M, Rothlisberger J (2007) From bait shops to forest floor: earthworm use and disposal by anglers. Am Midl Nat 158:321–328. doi:10.1674/0003-0031(2007)158[321:FBSTTF]2.0.CO;2

    Article  Google Scholar 

  • Knollenberg WG, Merritt RW, Lawson DL (1985) Consumption of leaf litter by Lumbricus terrestris (Oligochaeta) on a Michigan woodland floodplain. Am Midl Nat 113:1–6. doi:10.2307/2425341

    Article  Google Scholar 

  • Lewis MA (1997) Variability, patchiness, and jump dispersal in the spread of an invading population. In: Tilman DG, Kareiva P (eds) Spatial ecology: the role of space in population dynamics and interspecific interactions. Princeton University Press, Princeton, NJ, USA, pp 46–69

    Google Scholar 

  • Marinissen JCY, van den Bosch F (1992) Colonization of new habitats by earthworms. Oecologia 91:371–376. doi:10.1007/BF00317626

    Article  Google Scholar 

  • McClain ME, Boyer EW, Dent CL, Gergel SE, Grimm NB, Groffman PM, Hart SC, Harvey JW, Johnston CA, Mayorga E, McDowell WH, Pinay G (2003) Biogeochemical hot spots and hot moments at the interface of terrestrial and aquatic ecosystems. Ecosystems 6:301–312. doi:10.1007/s10021-003-0161-9

    Article  CAS  Google Scholar 

  • Merritt DM, Wohl EE (2002) Processes governing hydrochloric along rivers: hydraulics, hydrology, and dispersal phenology. Ecol Appl 12:1071–1087. doi:10.1890/1051-0761(2002)012[1071:PGHARH]2.0.CO;2

    Article  Google Scholar 

  • Naiman RJ, Décamps H, McClain ME (2005) Riparia: ecology, conservation and management of streamside communities. Elsevier, Burlington, MA

    Google Scholar 

  • Nilsson C, Gardfjell M, Grelsson G (1991) Importance of hydrochloric in structuring plant communities along rivers. Can J Botany 69:2631–2633. doi:10.1139/b91-328

    Article  Google Scholar 

  • R Core Development Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Reynolds JW (1977) The earthworms (Lumbricidae and Sparganophilidae) of Ontario. Royal Ontario Museum, Toronto, CA

    Google Scholar 

  • Reynolds JW (1995) Status of exotic earthworm systematics and biogeography in North America. In: Hendrix PF (ed) Earthworm Ecology and Biogeography in North America. CRC Press, Boca Raton, FL, pp 1–28

    Google Scholar 

  • Reynolds JW, Wetzel MJ (2008) Terrestrial oligochaeta (Annelida: Clitellata) in North America, including Mexico, Puerto Rico, Hawaii, and Bermuda. Megadrilogica 12:157–210

    Google Scholar 

  • Roots BI (1956) The water relations of earthworms: II. Resistance to desiccation and immersion, and behaviour when submerged and when allowed choice of environment. J Exp Biol 33:29–44

    Google Scholar 

  • Rota E (2001) Oversized enchytraeids (Annelida, Clitellata): a comparative study with a revised rescription of Lumbricillus maximus (Michaelsen). Org Divers Evol 1:225–238. doi:10.1078/1439-6092-00019

    Article  Google Scholar 

  • Rota E, Brinkhurst RO (2000) Mesenchytraeus antaeus, a new giant enchytraeid (Annelida, Clitellata) from the temperate rainforest of British Columbia, Canada, with revised diagnosis of the genus Mesenchytraeus. J Zool 252:27–40. doi:10.1111/j.1469-7998.2000.tb00817.x

    Article  Google Scholar 

  • Schwert DP, Dance KW (1979) Earthworm cocoons as a drift component in a Southern Ontario stream. Can Field Nat 93:180–183

    Google Scholar 

  • Suomalainen E, Saura A, Lokki J (1987) Cytology and evolution in parthenogenesis. CRC Press, Boca Raton 216 pp

    Google Scholar 

  • Terhivuo J, Saura A (2006) Dispersal and clonal diversity of North-European parthenogenetic earthworms. Biol Invasions 8:1205–1218

    Article  Google Scholar 

  • Terhivuo J, Lundqvist E, Saura A (2002) Clone diversity of Eiseniella tetraedra (Oligochaeta: Lumbricidae) along regulated and free-flowing boreal rivers. Ecography 25:714–720. doi:10.1034/j.1600-0587.2002.250607.x

    Article  Google Scholar 

  • Tiegs SD, Chaloner DT, Levi PS, Rüegg J, Tank JL, Lamberti GA (2008) Timber harvest transforms ecological roles of salmon in southeast Alaska rain forest streams. Ecol Appl 18:4–11. doi:10.1890/07-0655.1

    Article  PubMed  Google Scholar 

  • Tomlin AD, Shipitalo MJ, Edwards WM, Protz R (1995) Earthworms and their influence on soil structure and infiltration. In: Hendrix PF (ed) Earthworm ecology and biogeography in North America. CRC Press, Boca Raton, FL, pp 159–184

    Google Scholar 

  • Turner JS (2000) The extended organism: the physiology of animal-built structures. Oxford University Press, Cambridge, MA

    Google Scholar 

  • U.S. Forest Service (1997) Tongass land management plan revision. Final environmental impact statement, region 10 (Alaska Region). U.S. Department of Agriculture, U.S. Forest Service, Juneau

    Google Scholar 

  • Ward JV (1976) Lumbricide earthworm populations in a Colorado mountain river. Southwest Nat 21:71–78. doi:10.2307/3670326

    Article  Google Scholar 

  • Zimmer M, Kautz G, Topp W (2005) Do woodlice and earthworms interact synergistically in leaf litter decomposition? Funct Ecol 19:7–16. doi:10.1111/j.0269-8463.2005.00926.x

    Article  Google Scholar 

  • Zorn MI, van Gestel CAM, Eijackers H (2005) Species-specific earthworm population responses in relation to flooding dynamics in a Dutch floodplain soil. Pedobiologia 49:189–198. doi:10.1016/j.pedobi.2004.08.004

    Article  Google Scholar 

  • Zorn MI, Van Gestel CAM, Morrien E, Wagenaar M, Eijackers H (2008) Flooding responses of three earthworm species, Allolobophora chlorotica, Aporrectodea caliginosa, and Lumbricus rubellus, in a laboratory-controlled environment. Soil Biol Biochem 40:587–593. doi:10.1016/j.soilbio.2007.06.028

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank J Rüegg for providing us with the GIS data, HG Greiner for assistance with the earthworm biomass estimates, DT Chaloner for providing the map of POW, and two anonymous reviewers for helpful comments on a previous version of the manuscript. J Rüegg, EY Campbell, AM Larquier, and PS Levi assisted with field collections, DV D’Amore assisted with soil classifications, and SZ Hebbeler and MA Brueseke provided logistical support. The Craig and Thorne Bay Ranger Districts (US Forest Service) graciously provided logistical support and assisted with access to sites. This research was funded by the USDA-CSREES National Research Initiative (Managed Ecosystems Program 2006-35101-16566) and a NSF Doctoral Dissertation Improvement Grant to DMC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David M. Costello.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 40 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Costello, D.M., Tiegs, S.D. & Lamberti, G.A. Do non-native earthworms in Southeast Alaska use streams as invasional corridors in watersheds harvested for timber?. Biol Invasions 13, 177–187 (2011). https://doi.org/10.1007/s10530-010-9800-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-010-9800-1

Keywords

Navigation