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Spatial variability of an invasive earthworm (Amynthas agrestis) population and potential impacts on soil characteristics and millipedes in the Great Smoky Mountains National Park, USA

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Abstract

European and Asian earthworm invasions are widespread in North America. European earthworms especially are well-known to cause dramatic changes in ecosystems in northern, formerly glaciated portions of the continent, but less is known about the impacts of earthworm invasions in unglaciated areas inhabited by indigenous earthworms. We monitored fluctuations in the spatial extent of an Amynthas agrestis (Megascolecidae) population in the Great Smoky Mountains National Park in eastern Tennessee, USA. Two years of monthly growing-season observations revealed that the distribution of the earthworm population was dynamic, but overall distribution was closely linked to temperature and moisture with dramatic reductions of earthworm numbers associated with very dry conditions. In plots where A. agrestis were more often detected, we measured increased A-horizon soil aggregation and decreased thickness of the Oe/Oa-horizon. However, A. agrestis was not related to A-horizon microbial biomass, A-horizon C:N, Oi-horizon (litter) thickness, or mass of forest floor (O-horizon). Reductions in millipede species richness and density were associated with frequency of A. agrestis presence, possibly due to direct competition for food resources (Oe/Oa material). This evidence for potentially negative interactions between millipedes and A. agrestis suggests that expansion of the non-native earthworm into new habitats in the Park may alter soil physical properties and could pose a threat to native millipede diversity.

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References

  • Baltz DM, Moyle PB (1993) Invasion resistance to introduced species by a native assemblage of California stream fishes. Ecol Apps 3:246–255

    Article  Google Scholar 

  • Bohlen PJ, Scheu S, Hale CM, McLean MA, Migge S, Groffman PM, Parkinson D (2004a) Non-native invasive earthworms as agents of change in northern temperate forests. Front Ecol Environ 2:427–435

    Article  Google Scholar 

  • Bohlen PJ, Groffman PM, Fahey TJ, Fisk MC, Suárez E, Pelletier D, Fahey R (2004b) Ecosystem consequences of exotic earthworm invasion of north temperate forests. Ecosystems 7:1–12

    Article  Google Scholar 

  • Bossuyt H, Six J, Hendrix PF (2006) Interactive effects of functionally different earthworm species on aggregation and incorporation and decomposition of newly added residue carbon. Geoderma 130:14–25

    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 9:197–201

    Article  Google Scholar 

  • Callaham MA Jr, Hendrix PF, Phillips RJ (2003) Occurrence of an exotic earthworm (Amynthas agrestis) in undisturbed soils of the southern Appalachian Mountains, USA. Pedobiologia 47:466–470

    Google Scholar 

  • Callaham MA Jr, González G, Hale CM, Heneghan L, Lachnicht SL, Zou X (2006) Policy and management responses to earthworm invasions in North America. Biol Inv 8:1317–1329

    Article  Google Scholar 

  • Carlsson NOL, Sarnelle O, Strayer DL (2009) Native predators and exotic prey–an acquired taste? Front Ecol Environ 7:525–532

    Article  Google Scholar 

  • Coleman DC, Crossley DA Jr, Hendrix PF (2004) Fundamentals of soil ecology. Academic Press, San Diego

    Google Scholar 

  • Fragoso C, Kanyonyo J, Moreno A, Senapati BK, Blanchart E, Rodriguez C (1999) A survey of tropical earthworms: taxonomy, biogeography and environmental plasticity. In: Lavelle P, Brussaard L, Hendrix P (eds) Earthworm management in tropical agroecosystems. CABI, New York, pp 1–26

    Google Scholar 

  • Garman H (1888) On the anatomy and histology of a new earthworm (Diplocardia communis, gen. et sp. nov.). Bull Ill State Lab Nat Hist 3:47–77

    Google Scholar 

  • Gates GE (1937) The genus Pheretima in North America. Bull Mus Comp Zool, Harvard 80:339–373

    Google Scholar 

  • Gates GE (1956) Reproductive organ polymorphism in earth-worms of the Oriental Megascolecine genus Pheretima Kinberg 1867. Evolution 10:213–227

    Article  Google Scholar 

  • Gates GE (1958) On some species of the oriental earthworm genus Pheretima Kinberg, 1867, with a key to species reported from the Americas. Am Mus Novit 1888:1–33

    Google Scholar 

  • Gates GE (1982) Farewell to North American Megadriles. Megadrilogica 4:12–77

    Google Scholar 

  • Hale CM, Frelich LE, Reich PB (2005) Exotic European earthworm invasion dynamics in Northern Hardwood Forests of Minnesota, USA. Ecol Apps 15:848–860

    Article  Google Scholar 

  • Haynes RJ, Fraser PM, Piercy JE, Tregurtha RJ (2003) Casts of Aporrectodea caliginosa (Savigny) and Lumbricus rubellus (Hoffmeister) differ in microbial activity, nutrient availability and aggregate stability. Pedobiologia 47:882–887

    Google Scholar 

  • Hendrix PF (ed) (2006) Biological invasions belowground: earthworms as invasive species. Springer, Amsterdam

    Google Scholar 

  • Hendrix PF, Baker GH, Callaham MA Jr, Damoff GA, Fragoso C, González G, James SW, Lachnicht SL, Winsome T, Zou X (2006) Invasion of exotic earthworms into ecosystems inhabited by native earthworms. Biol Inv 8:1287–1300

    Article  Google Scholar 

  • Hendrix PF, Callaham MA Jr, Drake J, 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 S 29:571–592

    Google Scholar 

  • Hopkin SP, Read HJ (1992) The biology of millipedes. Oxford University Press, Oxford

    Google Scholar 

  • Lake PS, O’Dowd DJ (1991) Red crabs in rain forest, Christmas Island: biotic resistance to invasion by an exotic snail. Oikos 62:25–29

    Article  Google Scholar 

  • Maerz JC, Karuzas JM, Madison DM, Blossey B (2005) Introduced invertebrates are important prey for a generalist predator. Divers Distrib 11:83–90

    Article  Google Scholar 

  • McLean MA, Parkinson D (1997) Changes in structure, organic matter and microbial activity in pine forest soil following the introduction of Dendrobaena octaedra (Oligochaeta, Lumbricidae). Soil Biol Biochem 29:537–540

    Article  CAS  Google Scholar 

  • National Museum of Natural History (2008) Invertebrate zoology collections search. Url: http://acsmith.si.edu/emuwebizweb/pages/nmnh/iz/Query.php. Accessed 25 Feb 2008

  • Reynolds JW (1978) The earthworms of Tennessee (Oligochaeta). IV. Megascolecidae, with notes on distribution, biology and a key to the species in the state. Megadrilogica 3:117–129

    Google Scholar 

  • Reynolds JW, Wetzel MJ (2004) Terrestrial Oligochaeta (Annelida: Clitellata) in North America north of Mexico. Megadrilogica 9:71–98

    Google Scholar 

  • Richardson R, Snyder BA, Hendrix PF (2009) Soil moisture and temperature; tolerances and optima for a non-native earthworm species, Amynthas agrestis (Oligochaeta: Opisthopora: Megascolecidae). Southeast Nat 8:325–334

    Article  Google Scholar 

  • Schmidt O (2001) Appraisal of the electrical octet method for estimating earthworm populations in arable land. Ann Appl Biol 138:231–241

    Article  Google Scholar 

  • Six J, Paustian K, Elliott ET, Combrink C (2000) Soil structure and organic matter: I. Distribution of aggregate-size classes and aggregate-associated carbon. Soil Sci Soc Am J 64:681–689

    Article  CAS  Google Scholar 

  • Snyder BA (2008a) Invasion by the non-native earthworm Amynthas agrestis (Oligochaeta: Megascolecidae): dynamics, impacts, and competition with millipedes. Ph.D. Dissertation, University of Georgia, Athens, GA

  • Snyder BA (2008b) A preliminary checklist of the millipedes (Diplopoda) of the Great Smoky Mountains National Park, USA. Zootaxa 1856:16–32

    Google Scholar 

  • Snyder BA, Draney ML, Sierwald P (2006) Development of an optimal sampling protocol for millipedes (Diplopoda). J Insect Conserv 10:277–288

    Article  Google Scholar 

  • Snyder BA, Boots B, Hendrix PF (2009) Competition between invasive earthworms (Amynthas corticis, Megascolecidae) and native North American millipedes (Pseudopolydesmus erasus, Polydesmidae): effects on carbon cycling and soil structure. Soil Biol Biochem 41:1442–1449

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Suárez ER, Fahey TJ, Yavitt JB, Groffman PM, Bohlen PM (2006) Patterns of litter disappearance in a northern hardwood forest invaded by exotic earthworms. Ecol Apps 16:154–165

    Article  Google Scholar 

  • Torchin ME, Lafferty KD, Dobson AP, Mckenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630

    Article  CAS  PubMed  Google Scholar 

  • USDA (2007) Soil survey of Great Smoky Mountains National Park, Tennessee and North Carolina. United States Department of Agriculture, Natural Resources Conservation Service, and United States Department of the Interior, National Park Service, Sevierville, TN, USA

    Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • Weyers SL, Schomberg HH, Hendrix PF, Spokas KA, Endale DM (2008) Construction of an electrical device for sampling earthworm populations in the field. Appl Eng Agric 24:391–397

    Google Scholar 

  • Whittaker RH (1956) Vegetation of the Great Smoky Mountains. Ecol Monogr 26:1–80

    Article  Google Scholar 

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Acknowledgments

Amynthas invasions in GSMNP were first reported to us by K. Langdon and B. Nichols (National Park Service Inventory & Monitoring) to whom we are grateful for logistical and intellectual support throughout this study. We also acknowledge: NPS volunteer B. Lochbaum for GPS location of our plot arrays; C. Lawson (Western Carolina University, WCU) for surveying plot elevations; J. Craft and S. Ferrell (WCU) for vegetation surveys; T. Maddox and the Odum School of Ecology Analytical Lab for chemical analysis; and the staff of the Great Smoky Mountains National Park and Great Smoky Mountains Institute at Tremont for their enthusiastic assistance. J. Blackmon, W. Duncan, K. Jacobsen, and two anonymous reviewers provided helpful comments on the manuscript. Field collecting would not have been possible without the help of many, many field assistants, who could not all be named here. This research was permitted under study number GRSM-00337 and supported by National Science Foundation grant number 0236276 to the University of Georgia Research Foundation, Inc.

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Authors and Affiliations

  1. Odum School of Ecology, University of Georgia, Athens, GA, 30602, USA

    Bruce A. Snyder & Paul F. Hendrix

  2. Division of Biology, Kansas State University, Manhattan, KS, 66506, USA

    Bruce A. Snyder

  3. Center for Forest Disturbance Science, Southern Research Station, USDA Forest Service, Athens, GA, 30602, USA

    Mac A. Callaham Jr.

  4. Department of Crop & Soil Science, University of Georgia, Athens, GA, 30602, USA

    Paul F. Hendrix

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  1. Bruce A. Snyder
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  2. Mac A. Callaham Jr.
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Correspondence to Bruce A. Snyder.

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Snyder, B.A., Callaham, M.A. & Hendrix, P.F. Spatial variability of an invasive earthworm (Amynthas agrestis) population and potential impacts on soil characteristics and millipedes in the Great Smoky Mountains National Park, USA. Biol Invasions 13, 349–358 (2011). https://doi.org/10.1007/s10530-010-9826-4

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  • DOI: https://doi.org/10.1007/s10530-010-9826-4

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