Invasive earthworms change nutrient availability and uptake by forest understory plants

Abstract

Background and aims

Assess whether invasive earthworms alter nutrient dynamics in habitats they colonize.

Methods

We investigated nutrient dynamics of forest soils and three native plant species (Acer saccharum, Polygonatum pubescens, Polystichum acrostichoides) along four earthworm invasion gradients in central New York.

Results

Earthworm biomass (a proxy for earthworm impact) was related to distribution and concentration of soil and plant nutrients. At shallower depths, earthworms were associated with lower total and exchangeable P, but higher Ca, K, Mg and Mn. Earthworm-invaded plots showed higher soil Ca and higher foliar Ca in A. saccharum and P. acrostichoides, and lower soil P with lower foliar P in P. pubescens. Presence of earthworms substantially decreased rooting volume in the A horizon, co-occurring with a build up of exchangeable nutrient concentrations and pools.

Conclusions

Overall, earthworm biomass was a better predictor of foliar nutrient concentrations than either exchangeable or total nutrient concentrations and pools. Earthworms may create stressful rooting conditions, limiting rooting of native plants in the A horizon. The resulting plant-accessible nutrient pool that builds up in the A horizon of earthworm-invaded soils could provide a mechanism for the invasive success of non-indigenous plants that have an evolutionary association with earthworms in the native range and that follow earthworm invasions.

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References

  1. Asshoff R, Scheu S, Eisenhauer N (2010) Different earthworm ecological groups interactively impact seedling establishment. Eur J Soil Biol 46:330–334. https://doi.org/10.1016/j.ejsobi.2010.06.005

    Article  Google Scholar 

  2. Bal TL, Storer AJ, Jurgensen MF (2017) Evidence of damage from exotic invasive earthworm activity was highly correlated to sugar maple dieback in the Upper Great Lakes region. Biol Invasions. https://doi.org/10.1007/s10530-017-1523-0

  3. Bard GE (1949) The mineral nutrient content of the annual parts of herbaceous species growing on 3 New York soil types varying in limestone content. Ecology 30:384–389

    Article  Google Scholar 

  4. Berch SM, Kendrick B (1982) Vesicular-arbuscular mycorrhizae of southern Ontario ferns and fern-allies. Mycologia 74:769–776

    Article  Google Scholar 

  5. Bernier B, Paré D, Brazeau M (1989) Natural stresses, nutrient imbalances and forest decline in southeastern Quebec. Water, Air, Soil Polution 48:239–250

    CAS  Google Scholar 

  6. Bityutskii NP, Lapshina IN, Lukina EI et al (2002) Role of earthworms in mineralization of organic nitrogen compounds in soil. Eurasian Soil Sci 35:1100–1107

    Google Scholar 

  7. Boerner REJ (1986) Seasonal nutrient dynamics, nutrient resorption, and mycorrhizal infection intensity of two perennial forest herbs. Am J Bot 73:1249–1257

    Article  Google Scholar 

  8. Bohlen PJ, Groffman PM, Fahey TJ et al (2004a) Ecosystem consequences of exotic earthworm invasion of north temperate forests. Ecosystems 7:1–12. https://doi.org/10.1007/s10021-003-0126-z

    Article  Google Scholar 

  9. Bohlen PJ, Pelletier DM, Groffman PM et al (2004b) Influence of earthworm invasion on redistribution and retention of soil carbon and nitrogen in northern temperate forests. Ecosystems 7:13–27. https://doi.org/10.1007/s10021-003-0127-y

    CAS  Article  Google Scholar 

  10. Bohlen PJ, Scheu S, Hale CM et al (2004c) Non-native invasive earthworms as agents of change in northern temperate forests. Front Ecol Environ 2:427

    Article  Google Scholar 

  11. Brady NC, Weil RR (2008) Calcium, Magnesium and trace elements. In: The nature and properties of soils, 14th edn. Pearson, Prentice Hall, Upper Saddle River, pp 639–677

    Google Scholar 

  12. Brundrett MC, Kendrick B (1988) The mycorrhizal status, root anatomy, and phenology of plants in a sugar maple forest. Can J Bot 66:1153–1173. https://doi.org/10.1139/b88-166

    Article  Google Scholar 

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

    Article  Google Scholar 

  14. Burton AJ, Pregitzer KS, Macdonald NW (1993) Foliar nutrients in sugar maple forests along a regional pollution-climate gradient. Soil Sci Soc Am J 57:1619–1628. https://doi.org/10.2136/sssaj1993.03615995005700060036x

    CAS  Article  Google Scholar 

  15. Chapman HD (1965) Cation-exchange capacity 1. In: Norman AG (ed) Methods of soil analysis. Part 2. Chemical and microbiological properties. American Society of Agronomy, Soil Science Society of America, Madison, pp 891–901

    Google Scholar 

  16. Chapuis-Lardy L, Le Bayon R-C, Brossard M et al (2011) Phosphorus in action. Soil Biol 26:295–316. https://doi.org/10.1007/978-3-642-15271-9

    Article  Google Scholar 

  17. Ciesielski H, Sterckeman T, Santerne M, Willery J (1997) A comparison between three methods for the determination of cation exchange capacity and exchangeable cations in soils. Agronomie 17:9–16

    Article  Google Scholar 

  18. Clair SS, Lynch J (2005) Base cation stimulation of mycorrhization and photosynthesis of sugar maple on acid soils are coupled by foliar nutrient dynamics. New Phytol 165:581–590. https://doi.org/10.1111/j.1469-8137.2004.01249.x

    Article  Google Scholar 

  19. Corio K, Wolf A, Draney M, Fewless G (2009) Exotic earthworms of Greak Lakes forests: A search for indicator plant species in maple forests. For Ecol Manag 258:1059–1066. https://doi.org/10.1016/j.foreco.2009.05.013

    Article  Google Scholar 

  20. Côté B, Halloran IO, Hendershot WH, Spankie H (1995) Possible interference of fertilization in the natural recovery of a declining sugar maple stand in southern Quebec. 471–480

  21. Coulis M, Bernard L, Gérard F et al (2014) Endogeic earthworms modify soil phosphorus, plant growth and interactions in a legume-cereal intercrop. Plant Soil 379:149–160. https://doi.org/10.1007/s11104-014-2046-4

    CAS  Article  Google Scholar 

  22. Cronan CS, Grigal DF (1995) Use of calcium aluminum ratios as indicators of stress in forest ecosystems. J Environ Qual 24:209–226

    CAS  Article  Google Scholar 

  23. Daniel O (1990) Life cycle and population dynamics of the earthworm Lumbricus terrestris L. Swiss Federal Institute of Technology Zurich

  24. De Vleeschauwer D, Lal R (1981) Properties of worm casts under secondary tropical forest regrowth (Nigeria). Soil Sci 132:175–181

    Article  Google Scholar 

  25. Deleporte S (2001) Changes in the earthworm community of an acidophilous lowland beech forest during a stand rotation. Eur J Soil Biol 37:1–7. https://doi.org/10.1016/S1164-5563(01)01065-2

    Article  Google Scholar 

  26. Dobson A, Blossey B (2015) Earthworm invasion, white-tailed deer and seedling establishment in deciduous forests of north-eastern North America. J Ecol 103:153–164. https://doi.org/10.1111/1365-2745.12350

    Article  Google Scholar 

  27. Dorning M, Cipollini D (2006) Leaf and root extracts of the invasive shrub, Lonicera maackii, inhibit seed germination of three herbs with no autotoxic effects. Plant Ecol 184:287–296. https://doi.org/10.1007/s11258-005-9073-4

    Article  Google Scholar 

  28. Doust JL, Cavers PB (1982) Sex and gender dynamics in Jack-in-the-Pulpit, Arisaema triphyllum (Araceae). Ecology 63:797–808

    Article  Google Scholar 

  29. Drouin M, Bradley R, Lapointe L (2016) Forest ecology and management linkage between exotic earthworms, understory vegetation and soil properties in sugar maple forests. For Ecol Manag 364:113–121

    Article  Google Scholar 

  30. Drouin M, Bradley R, Lapointe L, Whalen J (2014) Non-native anecic earthworms (Lumbricus terrestris L.) reduce seed germination and seedling survival of temperate and boreal trees species. Appl Soil Ecol 75:145–149. https://doi.org/10.1016/j.apsoil.2013.11.006

    Article  Google Scholar 

  31. Edwards CA (2004) Earthworm ecology, 2nd edn. CRC Press, Boca Raton

    Google Scholar 

  32. Edwards CA, Bohlen PJ (1996) Biology and ecology of earthworms. Chapman & Hall, London

    Google Scholar 

  33. Eisenhauer N, Partsch S, Parkinson D, Scheu S (2007) Invasion of a deciduous forest by earthworms: changes in soil chemistry, microflora, microarthropods and vegetation. Soil Biol Biochem 39:1099–1110. https://doi.org/10.1016/j.soilbio.2006.12.019

    CAS  Article  Google Scholar 

  34. Elliott HL (2009) Evaluating the influences of soil calcium and aluminum availability on ecosystem processes in northern hardwood forest. University of Vermont

  35. Ellsworth DS, Liu X (1994) Photosynthesis and canopy nutrition of four sugar maple forests on acid soils in northern Vermont. Can J For Res 24:2119–2127

    Article  Google Scholar 

  36. Filley TR, McCormick MK, Crow SE et al (2008) Comparison of the chemical alteration trajectory of Liriodendron tulipifera L. leaf litter among forests with different earthworm abundance. J Geophys Res 113:G01027–G01027. https://doi.org/10.1029/2007JG000542

    Google Scholar 

  37. Fisk MG, Fahey TJ, Groffman PM, Bohlen PJ (2004) Earthworm invasion, fine-root distributions, and soil respiration in North temperate forests. Ecosystems 7:55–62. https://doi.org/10.1007/s10021-003-0130-3

    Article  Google Scholar 

  38. Frelich LE, Hale CM, Scheu S et al (2006) Earthworm invasion into previously earthworm-free temperate and boreal forests. Biol Invasions 8:1235–1245. https://doi.org/10.1007/s10530-006-9019-3

    Article  Google Scholar 

  39. Giehl RFH, von Wiren N (2014) Root nutrient foraging. Plant Physiol 166:509–517. https://doi.org/10.1104/pp.114.245225

    Article  PubMed  PubMed Central  Google Scholar 

  40. Gilbert KJ, Fahey TJ, Maerz JC et al (2014) Exploring carbon flow through the root channel in a temperate forest soil food web. Soil Biol Biochem 76:45–52. https://doi.org/10.1016/j.soilbio.2014.05.005

    CAS  Article  Google Scholar 

  41. Gilliam FS (2014) The herbaceous layer in forests of eastern North America, 2nd edn. Oxford University Press, New York

    Google Scholar 

  42. Gilliam FS, Adams MB (1995) Plant and soil nutrients in young versus mature central Appalachian hardwood stands. Proc 10th Cent Hardwood For Conf 109–118

  43. Gundale MJ (2002) Influence of exotic earthworms on the soil organic horizon and the rare fern Botrychium mormo. Conserv Biol 16:1555–1561. https://doi.org/10.1046/j.1523-1739.2002.01229.x

    Article  Google Scholar 

  44. Hale C, Frelich L, Reich P, Pastor J (2005) Effects of European earthworm invasion on soil characteristics in northern hardwood forests of Minnesota, USA. Ecosystems 8:911–927. https://doi.org/10.1007/s10021-005-0066-x

    CAS  Article  Google Scholar 

  45. Hale CM, Frelich LE, Reich PB (2006a) Changes in cold-temperate hardwood forest understory plant communities in response to invasion by European earthworms. Ecology 87:1637–1649. https://doi.org/10.1890/0012-9658(2006)87[1637:CIHFUP]2.0.CO;2

    Article  PubMed  Google Scholar 

  46. Hale CM, Frelich LE, Reich PB (2006b) Changes in hardwood forest understory plant communities in response to European earthworm invasions. Ecology 87:1637–1649. https://doi.org/10.1890/0012-9658(2006)87[1637:CIHFUP]2.0.CO;2

    Article  PubMed  Google Scholar 

  47. Hale CM, Frelich LE, Reich PB, Pastor J (2008) Exotic earthworm effects on hardwood forest floor, nutrient availability and native plants: A mesocosm study. Oecologia 155:509–518. https://doi.org/10.1007/s00442-007-0925-6

    Article  PubMed  Google Scholar 

  48. Hawkesford M, Horst W, Kichey T et al (2011) Functions of macronutrients. In: Marschner H (ed) Marschner’s mineral nutrition of higher plants, 3rd edn. Academic Press, London, pp 135–189

    Google Scholar 

  49. Hendrix P, Bohlen P (2002) Exotic earthworm invasions in North America: ecological and policy implications. Bioscience 52:801–811. https://doi.org/10.1641/0006-3568(2002)052[0801:EEIINA]2.0.CO;2

    Article  Google Scholar 

  50. Heneghan L, Steffen J, Fagen K (2007) Interactions of an introduced shrub and introduced earthworms in an Illinois urban woodland: Impact on leaf litter decomposition. Pedobiologia (Jena) 50:543–551. https://doi.org/10.1016/j.pedobi.2006.10.002

    Article  Google Scholar 

  51. Holdsworth AR, Frelich LE, Reich PB (2007a) Effects of earthworm invasion on plant species richness in northern hardwood forests. Conserv Biol 21:997–1008. https://doi.org/10.1111/j.1523-1739.2007.00740.x

    Article  PubMed  Google Scholar 

  52. Holdsworth AR, Frelich LE, Reich PB (2007b) Regional extent of an ecosystem engineer: Earthworm invasion in northern hardwood forests. Ecol Appl 17:1666–1677. https://doi.org/10.1890/05-2003.1

    Article  PubMed  Google Scholar 

  53. Horsley SB, Long RP, Bailey SW et al (2000) Factors associated with the decline disease of sugar maple on the Allegheny Plateau. Can J For Res 30:1365–1378. https://doi.org/10.1139/x00-057

    CAS  Article  Google Scholar 

  54. Horsley SB, Long RP, Bailey SW et al (2002) Health of eastern North American sugar maple forests and factors affecting decline. North J Appl For 19:34–44

    Google Scholar 

  55. Huenneke LF, Hamburg SP, Koide R et al (1990) Effects of soil resources on plant invasion and community structure in Californian serpentine grassland. Ecology 71:478–491

    Article  Google Scholar 

  56. Hunter MD, Watt AD, Docherty M (1991) Outbreaks of the winter moth on Sitka Spruce in Scotland are not influenced by nutrient deficiencies of trees, tree budburst, or pupal predation. Oecologia 86:62–69

    CAS  Article  PubMed  Google Scholar 

  57. Huntington TG, Hooper RP, Johnson CE et al (2000) Calcium depletion in a southeastern United States forest ecosystem. Soil Sci Soc Am J 64:1845. https://doi.org/10.2136/sssaj2000.6451845x

    CAS  Article  Google Scholar 

  58. James SW (1995) Systematics, biogeography, and ecology of nearctic earthworms from eastern, central, southern and southwestern United States. In: Hendrix PF (ed) Earthworm ecology and biogeography in North America. Lewis, pp 29–52

  59. Jenkins J, Roy K, Driscoll C, Buerkett C (2005) Acid rain and the Adirondacks : a research summary. Ray Brook, New York

    Google Scholar 

  60. Joern A, Provin T, Behmer ST (2012) Not just the usual suspects: Insect herbivore populations and communities are associated with multiple plant nutrients. Ecology 93:1002–1015. https://doi.org/10.1890/11-1142.1

    Article  PubMed  Google Scholar 

  61. Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647. https://doi.org/10.1111/j.1469-8137.2009.03110.x

    CAS  Article  PubMed  Google Scholar 

  62. Juice SM, Fahey TJ, Siccama TG et al (2006) Response of sugar maple to calcium addition to northern hardwood forest. Ecology 87:1267–1280. https://doi.org/10.1890/0012-9658(2006)87[1267:ROSMTC]2.0.CO;2

    Article  PubMed  Google Scholar 

  63. Kery M, Gregg KB (2004) Demographic analysis of dormancy and survival in the terrestrial orchid Cypripedium reginae. J Ecol 92:686–695. https://doi.org/10.1111/j.0022-0477.2004.00885.x

    Article  Google Scholar 

  64. Knowles ME, Ross DS, Josef HG (2016) Effect of the endogeic earthworm Aporrectodea tuberculata on aggregation and carbon redistribution in uninvaded forest soil columns. Soil Biol Biochem 100:192–200. https://doi.org/10.1016/j.soilbio.2016.06.016

    CAS  Article  Google Scholar 

  65. Kobe RK, Likens GE, Eagar C (2002) Tree seedling growth and mortality responses to manipulations of calcium and aluminum in a northern hardwood forest. Can J For Res 32:954–966. https://doi.org/10.1139/x02-018

    CAS  Article  Google Scholar 

  66. Kolb T, McCormick L (1993) Etiology of sugar maple decline in four Pennsylvania stands. Can J For Res 23:2395–2402

    Article  Google Scholar 

  67. Kuczak CN, Fernandes ECM, Lehmann J et al (2006) Inorganic and organic phosphorus pools in earthworm casts (Glossoscolecidae) and a Brazilian rainforest Oxisol. Soil Biol Biochem 38:553–560. https://doi.org/10.1016/j.soilbio.2005.06.007

    CAS  Article  Google Scholar 

  68. Laossi K-R, Decaëns T, Jouquet P, Barot S (2010a) Can we predict how earthworm effects on plant growth vary with soil properties? Appl Environ Soil Sci. https://doi.org/10.1155/2010/784342

  69. Laossi KR, Ginot A, Noguera DC et al (2010b) Earthworm effects on plant growth do not necessarily decrease with soil fertility. Plant Soil 328:109–118. https://doi.org/10.1007/s11104-009-0086-y

    CAS  Article  Google Scholar 

  70. Larson ER, Kipfmueller KF, Hale CM et al (2010) Tree rings detect earthworm invasions and their effects in northern Hardwood forests. Biol Invasions 12:1053–1066. https://doi.org/10.1007/s10530-009-9523-3

    Article  Google Scholar 

  71. Lawrence AP, Bowers MA (2002) A test of the “hot” mustard extraction method of sampling earthworms. Soil Biol Biochem 34:549–552. https://doi.org/10.1016/S0038-0717(01)00211-5

    CAS  Article  Google Scholar 

  72. Lawrence B, Fisk MC, Fahey TJ, Suarez ER (2003) Influence of nonnative earthworms on mycorrhizal colonization of sugar maple (Acer saccharum). New Phytol 157:145–153. https://doi.org/10.1046/j.1469-8137.2003.00649.x

    Article  Google Scholar 

  73. Le Bayon RC, Binet F (2006) Earthworms change the distribution and availability of phosphorous in organic substrates. Soil Biol Biochem 38:235–246. https://doi.org/10.1016/j.soilbio.2005.05.013

    Article  Google Scholar 

  74. Leonard JA, Field JB (2004) Distributions of cations in the regolith and vegetation. In: Roach I (ed) Regiolith: Proceedings of the CRC LEME Regional Regolith Symposia 2004. CRC LEME, Bentley, pp 215–219

    Google Scholar 

  75. Long RP, Horsley SB, Lilja PR (1997) Impact of forest liming on growth and crown vigor of sugar maple and associated hardwoods. Can J For Res 1573:1560–1573

    Article  Google Scholar 

  76. Madritch MD, Lindroth RL (2009) Removal of invasive shrubs reduces exotic earthworm populations. Biol Invasions 11:663–671. https://doi.org/10.1007/s10530-008-9281-7

    Article  Google Scholar 

  77. McLean MA, Migge-Kleian S, Parkinson D (2006) Earthworm invasions of ecosystems devoid of earthworms: Effects on soil microbes. Biol Invasions 8:1257–1273. https://doi.org/10.1007/978-1-4020-5429-7_7

    Article  Google Scholar 

  78. Newell CL, Peet RK (1998) Vegetation of Linville Gorge Wilderness, North Carolina. Castanea 63:275–322

    Google Scholar 

  79. Nuzzo VA, Maerz JC, Blossey B (2009) Earthworm invasion as the driving force behind plant invasion and community change in northeastern North American forests. Conserv Biol 23:966–974. https://doi.org/10.1111/j.1523-1739.2009.01168.x

    Article  PubMed  Google Scholar 

  80. Paré D, Bernier B (1989) Origin of the phosphorus deficiency observed in declining sugar maple stands in the Quebec Appalachians. Can J For Res 19:24–34

    Article  Google Scholar 

  81. R Core Team (2014) R: A language and environment for statistical computing. 3.0.1

  82. Reich PB, Oleksyn J, Modrzynski J et al (2005) Linking litter calcium, earthworms and soil properties: a common garden test with 14 tree species. Ecol Lett 8:811–818. https://doi.org/10.1111/j.1461-0248.2005.00779.x

    Article  Google Scholar 

  83. Resner K, Yoo K, Sebestyen SD et al (2015) Invasive earthworms deplete key soil inorganic nutrients (Ca, Mg, K, and P) in a northern hardwood forest. Ecosystems 18:89–102. https://doi.org/10.1007/s10021-014-9814-0

    CAS  Article  Google Scholar 

  84. Richardson JB, Görres JH, Friedland AJ (2016) Forest floor decomposition, metal exchangeability, and metal bioaccumulation by exotic earthworms: Amynthas agrestis and Lumbricus rubellus. Environ Sci Pollut Res 23:18253–18266. https://doi.org/10.1007/s11356-016-6994-5

    CAS  Article  Google Scholar 

  85. Richardson JB, Gorres JH, Jackson BP, Friedland AJ (2015) Trace metals and metalloids in forest soils and exotic earthworms in northern New England, USA. Soil Biol Biochem 85:190–198. https://doi.org/10.1016/j.soilbio.2015.03.001

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  86. Royo AA, Carson WP (2008) Direct and indirect effects of a dense understory on tree seedling recruitment in temperate forests: habitat-mediated predation versus competition. Can J For Res 38:1634–1645. https://doi.org/10.1139/X07-247

    Article  Google Scholar 

  87. Schaberg PG, Tilley JW, Hawley GJ et al (2006) Associations of calcium and aluminum with the growth and health of sugar maple trees in Vermont. For Ecol Manag 223:159–169. https://doi.org/10.1016/j.foreco.2005.10.067

    Article  Google Scholar 

  88. Schelfhout S, Mertens J, Verheyen K et al (2017) Tree species identity shapes earthworm communities. Forests 8:85. https://doi.org/10.3390/f8030085

    Article  Google Scholar 

  89. Scheu S (1994) There is an earthworm mobilizable nitrogen pool in soil. Pedobiologia (Jena) 38:243–249

    Google Scholar 

  90. Scheu S, Parkinson D (1994) Effects 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 1:113–125

    Article  Google Scholar 

  91. Siccama T, Bormann F, Likens G (1970) The Hubbard Brook Ecosystem study: productivity, nutrients, and phytosociology of the herbaceous layer. Ecol Monogr 40:389–402

    Article  Google Scholar 

  92. St. Clair S, Lynch JP (2005) Element accumulation patterns of deciduous and evergreen tree seedlings on acid soils: Implications for sensitivity to manganese toxicity. Tree Physiol 25:85–92. https://doi.org/10.1093/treephys/25.1.85

    CAS  Article  PubMed  Google Scholar 

  93. Suarez ER, Fahey TJ, Yavitt JB et al (2006a) Patterns of litter disappearance in a northern hardwood forest invaded by exotic earthworms. Ecol Appl 16:154–165. https://doi.org/10.1890/04-0788

    Article  PubMed  Google Scholar 

  94. Suarez ER, Pelletier DM, Fahey TJ et al (2004) Effects of exotic earthworms on soil phosphorus cycling in two broadleaf temperate forests. Ecosystems 7:28–44. https://doi.org/10.1007/s10021-003-0128-x

    CAS  Article  Google Scholar 

  95. Suárez ER, Pelletier DM, Fahey TJ et al (2004) Effects of exotic earthworms on soil phosphorus cycling in two broadleaf temperate forests. Ecosystems 7:28–44. https://doi.org/10.1007/s10021-003-0128-x

    Article  Google Scholar 

  96. Suarez ER, Tierney GL, Fahey TJ, Fahey R (2006b) Exploring patterns of exotic earthworm distribution in a temperate hardwood forest in south-central New York, USA. Landsc Ecol 21:297–306. https://doi.org/10.1007/s10980-005-1785-2

    Article  Google Scholar 

  97. Szlavecz K, McCormick M, Xia L et al (2011) Ecosystem effects of non-native earthworms in Mid-Atlantic deciduous forests. Biol Invasions 13:1165–1182. https://doi.org/10.1007/s10530-011-9959-0

    Article  Google Scholar 

  98. Szlavecz K, Placella SA, Pouyat RV et al (2006) Invasive earthworm species and nitrogen cycling in remnant forest patches. Appl Soil Ecol 32:54–62. https://doi.org/10.1016/j.apsoil.2005.01.006

    Article  Google Scholar 

  99. Thornton FC, Schaedle M, Raynal DJ (1986) Effect of aluminum on growth of sugar maple in solution culture. Can J For Res 16:892–896

    CAS  Article  Google Scholar 

  100. Umarov MM, Striganova BR, Kostin NV (2008) Specific features of nitrogen transformation in the gut and coprolites of earthworms. Biol Bull 35:643–652. https://doi.org/10.1134/S1062359008060125

    CAS  Article  Google Scholar 

  101. Vos HMJ, Ros MBH, Koopmans GF, van Groenigen JW (2014) Do earthworms affect phosphorus availability to grass? A pot experiment. Soil Biol Biochem 79:34–42. https://doi.org/10.1016/j.soilbio.2014.08.018

    CAS  Article  Google Scholar 

  102. Weihua D, Xiuqin Y (2007) Transformation of carbon and nitrogen by earthworms in the decomposition processes of broad-reaved litters. Chinese Geogr Sci 17:166–172. https://doi.org/10.1007/s11769-007-0166-y

    Article  Google Scholar 

  103. West B, Brandt J, Holstien K et al (2009) Fern-associated arbuscular mycorrhizal fungi are represented by multiple Glomus spp.: Do environmental factors influence partner identity? Mycorrhiza 19:295–304. https://doi.org/10.1007/s00572-009-0234-5

    Article  PubMed  Google Scholar 

  104. Whitfeld TS, Roth A, Lodge A et al (2014) Resident plant diversity and introduced earthworms have contrasting effects on the success of invasive plants. Biol Invasions 16:2181–2193. https://doi.org/10.1007/s10530-014-0657-6

    Article  Google Scholar 

  105. Wironen M, Moore TR (2006) Exotic earthworm invasion increases soil carbon and nitrogen in an old-growth forest in southern Quebec. Can J For Res Can Rech For 36:845–854. https://doi.org/10.1139/X06-016

    Article  Google Scholar 

  106. Wood T, Bormann FH, Voigt GK (1984) Phosphorus cycling in a northern hardwood forest: biological and chemical control. Science 223(80):391–393

    CAS  Article  PubMed  Google Scholar 

  107. Yanai RD (1992) Phosphorus budget of a 70-year-old northern hardwood forest. Biogeochemistry 17:1–22

    CAS  Article  Google Scholar 

  108. Zhang BG, Li GT, Shen TS et al (2000) Changes in microbial biomass C, N, and P and enzyme activities in soil incubated with the earthworms Metaphire guillelmi or Eisenia fetida. Soil Biol Biochem 32:2055–2062. https://doi.org/10.1016/S0038-0717(00)00111-5

    CAS  Article  Google Scholar 

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Acknowledgements

We thank Tim Fahey, Francoise Vermeylen and Andrea Dávalos for their input in interpreting results and improving data analysis. Juan Pablo Jordan and Wade Simmons helped immensely in field collection, and we are grateful to Gregg McElwee for his help in lab analysis. We would like to thank the New York State Department of Environmental Conservation, Cornell Natural Areas, and Victoria Nuzzo for long-term use of their land for this experiment. This study was conducted through TRP #6673, and we are grateful for funding received through the Mellon Foundation and a Hatch Grant.

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Correspondence to Annise M. Dobson.

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Dobson, A.M., Blossey, B. & Richardson, J.B. Invasive earthworms change nutrient availability and uptake by forest understory plants. Plant Soil 421, 175–190 (2017). https://doi.org/10.1007/s11104-017-3412-9

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Keywords

  • Macronutrients
  • Calcium
  • Phosphorus
  • Foliar tissue
  • Root tissue
  • European earthworms