Unexpected earthworm effects on forest understory plants

BMC Ecology

Volumn 13, Issue , 2013, Pages

  Dávalos, Andrea ^a   Nuzzo, Victoria ^b   Stark, Jordan ^a,c   Blossey, Bernd ^a  

^a Cornell University ^*  (United States)

^b Natural Area Consultants   (United States)

^c SKIDMORE COLLEGE   (United States)

Author keywords

Earthworm invasion; Forest understory; Lumbricus terrestris; Mesocosm; Plant community; Sedge

Indexed keywords

COMMUNITY RESPONSE; EARTHWORM; ECOLOGICAL IMPACT; FOREST ECOSYSTEM; INTRODUCED SPECIES; MESOCOSM; SEDGE; UNDERSTORY;

NORTH AMERICA;

CAREX; CAREX RADIATA; CAREX RETROFLEXA; LUMBRICUS TERRESTRIS;

ANIMAL; ARTICLE; BIOMASS; CYPERACEAE; ECOSYSTEM; INTRODUCED SPECIES; OLIGOCHAETA; PHYSIOLOGY; TREE; UNITED STATES;

ANIMALS; BIOMASS; CAREX PLANT; ECOSYSTEM; INTRODUCED SPECIES; NEW YORK; OLIGOCHAETA; TREES;

EID: 84889014588     PISSN: None     EISSN: 14726785     Source Type: Journal    
DOI: 10.1186/1472-6785-13-48     Document Type: Article

References (48)

1. Frelich LE, Hale CM, Scheu S, Holdsworth AR, Heneghan L, Bohlen PJ, Reich PB. Earthworm invasion into previously earthworm-free temperate and boreal forests. Biol Invasions 2006, 8(6):1235-1245.
2. Bohlen PJ, Groffman PM, Fahey TJ, Fisk MC, Suarez E, Pelletier DM, Fahey RT. Ecosystem consequences of exotic earthworm invasion of north temperate forests. Ecosystems 2004, 7(1):1-12.
3. Hale CM, Frelich LE, Reich PB. Changes in hardwood forest understory plant communities in response to European earthworm invasions. Ecology 2006, 87(7):1637-1649. 10.1890/0012-9658(2006)87[1637:CIHFUP]2.0.CO;2, 16922315.
4. Suarez ER, Pelletier DM, Fahey TJ, Groffman PM, Bohlen PJ, Fisk MC. Effects of exotic earthworms on soil phosphorus cycling in two broadleaf temperate forests. Ecosystems 2004, 7(1):28-44.
5. Suarez ER, Fahey TJ, Yavitt JB, Groffman PM, Bohlen PJ. Patterns of litter disappearance in a northern hardwood forest invaded by exotic earthworms. Ecol Appl 2006, 16(1):154-165. 10.1890/04-0788, 16705969.
6. Maerz JC, Nuzzo VA, Blossey B. Declines in woodland salamander abundance associated with non-native earthworm and plant invasions. Conserv Biol 2009, 23(4):975-981. 10.1111/j.1523-1739.2009.01167.x, 19236449.
7. Nuzzo VA, Maerz JC, Blossey B. Earthworm invasion as the driving force behind plant invasion and community change in northeastern North American forests. Conserv Biol 2009, 23(4):966-974. 10.1111/j.1523-1739.2009.01168.x, 19236448.
8. Asshoff R, Scheu S, Eisenhauer N. Different earthworm ecological groups interactively impact seedling establishment. Eur J Soil Biol 2010, 46(5):330-334.
9. Eisenhauer N, Butenschoen O, Radsick S, Scheu S. Earthworms as seedling predators: importance of seeds and seedlings for earthworm nutrition. Soil Biol Biochem 2010, 42:1245-1253.
10. Hale CM, Frelich LE, Reich PB, Pastor J. Exotic earthworm effects on hardwood forest floor, nutrient availability and native plants: a mesocosm study. Oecologia 2008, 155(3):509-518. 10.1007/s00442-007-0925-6, 18066602.
11. Hopfensperger KN, Leighton GM, Fahey TJ. Influence of invasive earthworms on above and belowground vegetation in a northern hardwood forest. Am Midl Nat 2011, 166(1):53-62.
12. Holdsworth AR, Frelich LE, Reich PB. Regional extent of an ecosystem engineer: earthworm invasion in northern hardwood forests. Ecol Appl 2007, 17(6):1666-1677. 10.1890/05-2003.1, 17913131.
13. Eisenhauer N, Partsch S, Parkinson D, Scheu S. Invasion of a deciduous forest by earthworms: changes in soil chemistry, microflora, microarthropods and vegetation. Soil Biol Biochem 2007, 39(5):1099-1110.
14. Eisenhauer N, Scheu S. Earthworms as drivers of the competition between grasses and legumes. Soil Biol Biochem 2008, 40(10):2650-2659.
15. Straube D, Johnson EA, Parkinson D, Scheu S, Eisenhauer N. Nonlinearity of effects of invasive ecosystem engineers on abiotic soil properties and soil biota. Oikos 2009, 118(6):885-896.
16. Eisenhauer N, Straube D, Johnson EA, Parkinson D, Scheu S. Exotic ecosystem engineers change the emergence of plants from the seed bank of a deciduous forest. Ecosystems 2009, 12(6):1008-1016.
17. Nieminen M, Ketoja E, Mikola J, Terhivuo J, Sirén T, Nuutinen V. Local land use effects and regional environmental limits on earthworm communities in Finnish arable landscapes. Ecol Appl 2011, 21(8):3162-3177.
18. Ransom TS. Earthworms, as ecosystem engineers, influence multiple aspects of a salamander's ecology. Oecologia 2011, 165:745-754. 10.1007/s00442-010-1775-1, 20848134.
19. Karberg NJ, Lilleskov EA. White-tailed deer (Odocoileus virginianus) fecal pellet decomposition is accelerated by the invasive earthworm Lumbricus terrestris. Biol Invasions 2009, 11(3):761-767.
20. Skelly D, JM K. Venue and outcome in ecological experiments: manipulations of larval anurans. Oikos 2001, 94:198-208.
21. Drake JM AMK. Mechanistic analogy: how microcosms explain nature. Theor Ecol 2012, 5:433-444.
22. Eisenhauer N, Schuy M, Butenschoen O, Scheu S. Direct and indirect effects of endogeic earthworms on plant seeds. Pedobiol 2009, 52:151-162.
23. Eisenhauer N, Fisichelli NA, Frelich LE, Reich PB. Interactive effects of global warming and 'global worming' on the initial establishment of native and exotic herbaceous plant species. Oikos 2012, 121:1121-1133.
24. Northeast Regional Climate Center http://www.nrcc.cornell.edu/climate/ithaca/normal.html, Northeast Regional Climate Center.
25. Boodley J, Sheldrake R. Cornell peat-lite mixes for commercial plant growing. Cornell Univ Coop Ext Div Info Bull, Volume 43, 8 1977, Ithaca, NY: Cornell University.
26. OECD Test No. 207: Earthworm, Acute Toxicity Tests, OECD Guidelines for the Testing of Chemicals, Section 2 1984, Paris, France: OECD Publishing, OECD.
27. Lev SM, Matthies N, Snodgrass JW, Casey RE, Ownby DR. Effects of Zinc exposure on earthworms, Lumbricus terrestris, in an artificial soil. Bull Environ Contam Toxicol 2010, 84:687-691. 10.1007/s00128-010-0002-4, 20431863.
28. Svendsen TS, Hansen PE, Sommer C, Martinussen T, Grønvold J, Holter P. Life history characteristics of Lumbricus terrestris and effects of the veterinary antiparasitic compounds ivermectin and fenbendazole. Soil Biol Biochem 2005, 37:927-936.
29. R Core Team R: A language and environment for statistical computing 2012, Vienna, Austria: R Foundation for Statistical Computing, R Core Team.
30. Bates D, Maechler M, Bolker B. Linear mixed-effects models using S4 classes 2011, R package version 0.999375-42.
31. Royo AA, Ristau TE. Stochastic and deterministic processes regulate spatio-temporal variation in seed bank diversity. J Veg Sci 2012, DOI: 10.1111/jvs.12011.
32. Schiffman PM, Johnson WC. Sparse buried seed bank in a southern Appalachian oak forest: implications for succession. Am Midl Nat 1992, 127(2):258-267.
33. Bossuyt B, Honnay O. Can the seed bank be used for ecological restoration? An overview of seed bank characteristics in European communities. J Veg Sci 2008, 19(6):875-884.
34. Forey E, Barot S, Decaens T, Langlois E, Laossi KR, Margerie P, Scheu S, Eisenhauer N. Importance of earthworm-seed interactions for the composition and structure of plant communities: a review. Acta Oecologica-Int J Ecol 2011, 37(6):594-603.
35. Laossi K-R, Noguera DC, Barot S. Earthworm-mediated maternal effects on seed germination and seedling growth in three annual plants. Soil Biol Biochem 2010, 42:319-323.
36. Bartlett MD, Harris JA, James IT, Ritz K. Inefficiency of mustard extraction technique for assessing size and structure of earthworm communities in UK pasture. Soil Biol Biochem 2006, 38:2990-2992.
37. Pelosi C, Bertrand M, Capowiez Y, Boizard H, Roger-Estrade J. Earthworm collection from agricultural fields: comparisons of selected expellants in presence/absence of hand-sorting. Eur J Soil Biol 2009, 45:176-183.
38. Holdsworth A, Frelich L, Reich P. Leaf litter disappearance in earthworm-invaded northern hardwood forests: Role of tree species and the chemistry and diversity of litter. Ecosystems 2012, 15(6):913-926.
39. Eisenhauer N, Milcu A, Sabais ACW, Bessler H, Weigelt A, Engels C, Scheu S. Plant community impacts on the structure of earthworm communities depend on season and change with time. Soil Biol Biochem 2009, 41(12):2430-2443.
40. Corio K, Wolf A, Draney M, Fewless G. Exotic earthworms of Great Lakes forests: a search for indicator plant species in maple forests. For Ecol Manag 2009, 258(7):1059-1066.
41. Holdsworth AR, Frelich LE, Reich PB. Effects of earthworm invasion on plant species richness in northern hardwood forests. Conserv Biol 2007, 21(4):997-1008. 10.1111/j.1523-1739.2007.00740.x, 17650250.
42. Loss SR, Blair RB. Reduced density and nest survival of ground-nesting songbirds relative to earthworm invasions in northern hardwood forests. Conserv Biol 2011, 25(5):983-992. 10.1111/j.1523-1739.2011.01719.x, 21797927.
43. Zaller JG, Heigl F, Grabmaier A, Lichtenegger C, Piller K, Allabashi R, Frank T, Drapela T. Earthworm-mycorrhiza interactions can affect the diversity, structure and functioning of establishing model grassland communities. Plos One 2011, 6(12):e29293. 10.1371/journal.pone.0029293, 3247237, 22216236.
44. Miller RM, Smith CI, Jastrow JD, Bever JD. Mycorrhizal status of the genus Carex (Cyperaceae). Am J Bot 1999, 86(4):547-553. 10.2307/2656816, 10205075.
45. Muthukumar T, Udaiyan K, Shanmughavel P. Mycorrhiza in sedges - an overview. Mycorrhiza 2004, 14(2):65-77. 10.1007/s00572-004-0296-3, 14999550.
46. Johnson SN, Staley JT, McLeod FAL, Hartley SE. Plant-mediated effects of soil invertebrates and summer drought on above-ground multitrophic interactions. J Ecol 2011, 99(1):57-65.
47. Eisenhauer N, Marhan S, Scheu S. Assessment of anecic behavior in selected earthworm species: Effects on wheat seed burial, seedling establishment, wheat growth and litter incorporation. Appl Soil Ecol 2008, 38(1):79-82.
48. Szlavecz K, McCormick M, Xia LJ, Saunders J, Morcol T, Whigham D, Filley T, Csuzdi C. Ecosystem effects of non-native earthworms in Mid-Atlantic deciduous forests. Biol Invasions 2011, 13(5):1165-1182.