Invasive earthworms change nutrient availability and uptake by forest understory plants
- 396 Downloads
Background and aims
Assess whether invasive earthworms alter nutrient dynamics in habitats they colonize.
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.
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.
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.
KeywordsMacronutrients Calcium Phosphorus Foliar tissue Root tissue European earthworms
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.
- 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
- Bernier B, Paré D, Brazeau M (1989) Natural stresses, nutrient imbalances and forest decline in southeastern Quebec. Water, Air, Soil Polution 48:239–250Google Scholar
- Bityutskii NP, Lapshina IN, Lukina EI et al (2002) Role of earthworms in mineralization of organic nitrogen compounds in soil. Eurasian Soil Sci 35:1100–1107Google Scholar
- 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 639–677Google Scholar
- 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 CrossRefGoogle Scholar
- 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 891–901Google Scholar
- 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. 471–480Google Scholar
- Daniel O (1990) Life cycle and population dynamics of the earthworm Lumbricus terrestris L. Swiss Federal Institute of Technology ZurichGoogle Scholar
- Edwards CA, Bohlen PJ (1996) Biology and ecology of earthworms. Chapman & Hall, LondonGoogle Scholar
- Elliott HL (2009) Evaluating the influences of soil calcium and aluminum availability on ecosystem processes in northern hardwood forest. University of VermontGoogle Scholar
- Gilliam FS, Adams MB (1995) Plant and soil nutrients in young versus mature central Appalachian hardwood stands. Proc 10th Cent Hardwood For Conf 109–118Google Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 135–189Google Scholar
- 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 CrossRefGoogle Scholar
- 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 19:34–44Google Scholar
- 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 29–52Google Scholar
- Jenkins J, Roy K, Driscoll C, Buerkett C (2005) Acid rain and the Adirondacks : a research summary. Ray Brook, New YorkGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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
- 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 215–219Google Scholar
- Newell CL, Peet RK (1998) Vegetation of Linville Gorge Wilderness, North Carolina. Castanea 63:275–322Google Scholar
- R Core Team (2014) R: A language and environment for statistical computing. 3.0.1Google Scholar
- Scheu S (1994) There is an earthworm mobilizable nitrogen pool in soil. Pedobiologia (Jena) 38:243–249Google Scholar