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Amynthas spp. impacts on seedlings and forest soils are tree species-dependent

Abstract

Asian jumping worms (Amynthas spp.) are recent invaders of Upper Midwest forests. Research has highlighted the impacts of Amynthas earthworms on soil biogeochemistry and structure, and field observations suggest that Amynthas spp. decrease litter horizon depth and alter plant communities. However, the extent to which Amynthas spp. effects vary among forest types and with worm density and the mechanisms driving these effects are unknown. We conducted a 3-month tree seedling study to evaluate the effects of Amynthas spp. on tree seedling growth and a mesocosm field experiment to evaluate Amynthas spp. effects on soil carbon and nutrient cycling, soil structure, and leaf litter decomposition rates across forest types. In the seedling study, Amynthas spp. enhanced the growth of sugar maple and European buckthorn seedlings and decreased the growth of white oak seedlings. These effects were due to Amynthas spp.-induced changes in soil properties. In the mesocosm study, as Amynthas spp. density increased, carbon mineralization and carbon, nitrogen, and phosphorus availability increased in white oak forest soils and decreased in sugar maple forest soils, while decomposition rates of European buckthorn litter increased as Amynthas spp. density increased. Amynthas spp. altered soil structure similarly across all forest soil types. Taken together, our results suggest that Amynthas spp. have the potential to alter forest ecosystem dynamics via feedbacks among tree species, seedlings, and soil biogeochemistry. However, Amynthas spp. effects on tree seedlings and forest soils are largely context-dependent, and the direction and magnitude of these effects are mediated by tree species.

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References

  1. Averill C, Dietze MC, Bhatnagar JM (2018) Continental-scale nitrogen pollution is shifting forest mycorrhizal associations and soil carbon stocks. Glob Chang Biol 24:4544–4553. https://doi.org/10.1111/gcb.14368

    Article  PubMed  Google Scholar 

  2. Barbosa JZ, Demetrio WC, Silva CM, Dionísio JA (2017) Earthworms (Amynthas spp.) increase common bean growth, microbial biomass, and soil respiration. Semin Agrar 38:2887–2898. https://doi.org/10.5433/1679-0359.2017v38n5p2887

    Article  Google Scholar 

  3. BassiriRad H, Lussenhop JF, Sehtiya HL, Borden KK (2015) Nitrogen deposition potentially contributes to oak regeneration failure in the Midwestern temperate forests of the USA. Oecologia 177:53–63. https://doi.org/10.1007/s00442-014-3119-z

    Article  PubMed  Google Scholar 

  4. Beck T, Joergensen RG, Kandeler E et al (1997) An inter-laboratory comparison of ten different ways of measuring soil microbial biomass C. Soil Biol Biochem 29:1023–1032. https://doi.org/10.1016/S0038-0717(97)00030-8

    Article  CAS  Google Scholar 

  5. Bohlen PJ, Scheu S, Hale CM et al (2004) Non-native invasive earthworms as agents of change in northern temperate forests. Front Ecol Environ 2:427–435. https://doi.org/10.1890/1540-9295(2004)002

    Article  Google Scholar 

  6. Bottinelli N, Zhou H, Capowiez Y et al (2017) Earthworm burrowing activity of two non-Lumbricidae earthworm species incubated in soils with contrasting organic carbon content (Vertisol vs. Ultisol). Biol Fertil Soils 53:951–955. https://doi.org/10.1007/s00374-017-1235-8

    Article  CAS  Google Scholar 

  7. 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 

  8. Callaham MA, 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. https://doi.org/10.1078/0031-4056-00214

    Article  Google Scholar 

  9. Chang C-H, Szlavecz K, Buyer JS (2016a) Species-specific effects of earthworms on microbial communities and the fate of litter-derived carbon. Soil Biol Biochem 100:129–139. https://doi.org/10.1016/j.soilbio.2016.06.004

    Article  CAS  Google Scholar 

  10. Chang CH, Snyder BA, Szlavecz K (2016b) Asian pheretimoid earthworms in North America north of Mexico: an illustrated key to the genera Amynthas, Metaphire, Pithemera, and Polypheretima (Clitellata: Megascolecidae). Zootaxa 4179:495–529. https://doi.org/10.11646/zootaxa.4179.3.7

    Article  PubMed  Google Scholar 

  11. Chang CH, Szlavecz K, Buyer JS (2017) Amynthas agrestis invasion increases microbial biomass in Mid-Atlantic deciduous forests. Soil Biol Biochem 114:189–199. https://doi.org/10.1016/j.soilbio.2017.07.018

    Article  CAS  Google Scholar 

  12. Frelich LE, Hale CM, Reich PB et al (2006) Earthworm invasion into previously earthworm-free temperate and boreal forests. Biol Invasions 8:1235–1245. https://doi.org/10.1007/978-1-4020-5429-7_5

    Article  Google Scholar 

  13. Frelich LE, Blossey B, Cameron EK et al (2019) Side-swiped: ecological cascades emanating from earthworm invasions. Front Ecol Environ 17:502–510. https://doi.org/10.1002/fee.2099

    Article  PubMed  PubMed Central  Google Scholar 

  14. Frouz J (2018) Effects of soil macro- and mesofauna on litter decomposition and soil organic matter stabilization. Geoderma 332:161–172. https://doi.org/10.1016/j.geoderma.2017.08.039

    Article  CAS  Google Scholar 

  15. Görres JH, Melnichuk RDS (2012) Asian invasive earthworms of the genus Amynthas Kinberg in Vermont. Northeast Nat 19:313–322. https://doi.org/10.1656/045.019.0212

    Article  Google Scholar 

  16. Görres JH, Bellitürk K, Melnichuk RDS (2016) Temperature and moisture variables affecting the earthworms of genus Amynthas Kinberg, 1867 (Oligachaeta: Megascolecidae) in a hardwood forest in the Champlain Valley, Vermont, USA. Appl Soil Ecol 104:111–115. https://doi.org/10.1016/j.apsoil.2015.10.001

    Article  Google Scholar 

  17. Greiner HG, Kashian DR, Tiegs SD (2012) Impacts of invasive Asian (Amynthas hilgendorfi) and European (Lumbricus rubellus) earthworms in a North American temperate deciduous forest. Biol Invasions 14:2017–2027. https://doi.org/10.1007/s10530-012-0208-y

    Article  Google Scholar 

  18. Hale CM, Frelich LE, Reich PB (2006) 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 

  19. 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 

  20. Hedley MJ, Stewart JWB (1982) Method to measure microbial phosphate in soils. Soil Biol Biochem 14:377–385. https://doi.org/10.1016/0038-0717(82)90009-8

    Article  CAS  Google Scholar 

  21. 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 50:543–551. https://doi.org/10.1016/j.pedobi.2006.10.002

    Article  Google Scholar 

  22. Hobbie SE, Reich PB, Oleksyn J et al (2006) Tree species effects on decomposition and forest floor dynamics in a common garden. Ecology 87:2288–2297. https://doi.org/10.1890/0012-9658(2006)87[2288:TSEODA]2.0.CO;2

    Article  PubMed  Google Scholar 

  23. Hood-Nowotny R, Hinko-Najera Umana N, Inselbacher E et al (2010) Alternative methods for measuring inorganic, organic, and total dissolved nitrogen in soil. Soil Sci Soc Am J 74:1018–1027. https://doi.org/10.2136/sssaj2009.0389

    Article  CAS  Google Scholar 

  24. Iannone BV, Heneghan L, Rijal D, Wise DH (2015) Below-ground causes and consequences of woodland shrub invasions: a novel paired-point framework reveals new insights. J Appl Ecol 52:78–88. https://doi.org/10.1111/1365-2664.12354

    Article  CAS  Google Scholar 

  25. Kuebbing SE, Maynard DS, Bradford MA (2018) Linking functional diversity and ecosystem processes: a framework for using functional diversity metrics to predict the ecosystem impact of functionally unique species. J Ecol 106:687–698. https://doi.org/10.1111/1365-2745.12835

    Article  Google Scholar 

  26. Kuo S (1996) Phosphorus. In: Bartels JM, Bigham JM (eds) Methods of Soil Analysis, 3. Soil Science Society of America, Madison, Chemical Methods, pp 869–919

    Google Scholar 

  27. Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26. https://doi.org/10.18637/jss.v082.i13

    Article  Google Scholar 

  28. Laushman KM, Hotchkiss SC, Herrick BM (2018) Tracking an invasion: community changes in hardwood forests following the arrival of Amynthas agrestis and Amynthas tokioensis in Wisconsin. Biol Invasions 20:1671–1685. https://doi.org/10.1007/s10530-017-1653-4

    Article  Google Scholar 

  29. Lavelle P, Bignell D, Lepage M et al (1997) Soil function in a changing world: the role of invertebrate ecosystem engineers. Eur J Soil Biol 33:159–193

    CAS  Google Scholar 

  30. Lee MR, Bernhardt ES, van Bodegom PM et al (2017) Invasive species’ leaf traits and dissimilarity from natives shape their impact on nitrogen cycling: a meta-analysis. New Phytol 213:128–139. https://doi.org/10.1111/nph.14115

    Article  PubMed  CAS  Google Scholar 

  31. Lenth RV (2016) Least-squares means: the R package lsmeans. J Stat Softw 69:1–33. https://doi.org/10.18637/jss.v069.i01

  32. Liese R, Lübbe T, Albers NW, Meier IC (2018) The mycorrhizal type governs root exudation and nitrogen uptake of temperate tree species. Tree Physiol 38:83–95. https://doi.org/10.1093/treephys/tpx131

    Article  PubMed  CAS  Google Scholar 

  33. Loftis DL, McGee CE (eds) (1992) Oak regeneration: serious problems, practical recommendations. Southeastern Forest Experimental Station, Asheville, NC

    Google Scholar 

  34. Lovett GM, Weathers KC, Arthur MA, Schultz JC (2004) Nitrogen cycling in a northern hardwood forest: do species matter? Biogeochemistry 67:289–308. https://doi.org/10.1023/B:BIOG.0000015786.65466.f5

    Article  CAS  Google Scholar 

  35. Midgley MG, Phillips RP (2016) Resource stoichiometry and the biogeochemical consequences of nitrogen deposition in a mixed deciduous forest. Ecology 97:3369–3377. https://doi.org/10.1002/ecy.1595

    Article  PubMed  Google Scholar 

  36. Moore J-D, Görres JH, Reynolds JW (2018) Exotic Asian pheretimoid earthworms (Amynthas spp., Metaphire spp.): potzential for colonisation of south-eastern Canada and effects on forest ecosystems. Environ Rev 26:113–120. https://doi.org/10.1139/er-2017-0066

    Article  Google Scholar 

  37. Nowak DJ, Hoehn RE, Bodine AR et al (2014) Urban trees and forests of the Chicago Region. Chicago’s urban trees and forests: assessments, effects and values. Newtown Square, PA, pp 1–162

    Google Scholar 

  38. Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests. New Phytol 199:41–51. https://doi.org/10.1111/nph.12221

    Article  PubMed  CAS  Google Scholar 

  39. Qiu J, Turner MG (2017) Effects of non-native Asian earthworm invasion on temperate forest and prairie soils in the Midwestern US. Biol Invasions 19:73–88. https://doi.org/10.1007/s10530-016-1264-5

    Article  Google Scholar 

  40. R Core Development Team (2019) A language and environment for statistical computing. R Foundation for Statistical Computing

  41. 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 

  42. Richardson DR, 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. https://doi.org/10.1656/058.008.0211

    Article  Google Scholar 

  43. Richardson JB, Görres 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Rowland AP, Haygarth PM (1997) Determination of total dissolved phosphorus in soil solutions. J Environ Qual 26:410–415. https://doi.org/10.2134/jeq1997.00472425002600020011x

    Article  CAS  Google Scholar 

  45. 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 

  46. Shaw AN, DeForest JL (2013) The cycling of readily available phosphorus in response to elevated phosphate in acidic temperate deciduous forests. Appl Soil Ecol 63:88–93. https://doi.org/10.1016/j.apsoil.2012.09.008

    Article  Google Scholar 

  47. Sims GK, Ellsworth TR, Mulvaney RL (1995) Microscale determination of inorganic nitrogen in water and soil extracts. Commun Soil Sci Plant Anal 26:303–316. https://doi.org/10.1080/00103629509369298

    Article  CAS  Google Scholar 

  48. Snyder BA, Callaham MA, Hendrix PF (2011) 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. https://doi.org/10.1007/s10530-010-9826-4

    Article  Google Scholar 

  49. Snyder BA, Callaham MA, Lowe CN, Hendrix PF (2013) Earthworm invasion in North America: food resource competition affects native millipede survival and invasive earthworm reproduction. Soil Biol Biochem 57: 212–216. https://doi.org/10.1016/j.soilbio.2012.08.022

    Article  CAS  Google Scholar 

  50. 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 

  51. Talbot JM, Allison SD, Treseder KK (2008) Decomposers in disguise: Mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct Ecol 22:955–963. https://doi.org/10.1111/j.1365-2435.2008.01402.x

    Article  Google Scholar 

  52. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707. https://doi.org/10.1016/0038-0717(87)90052-6

    Article  CAS  Google Scholar 

  53. Zhang W, Hendrix PF, Snyder BA et al (2010) Dietary flexibility aids Asian earthworm invasion in North American forests. Ecology 91:2070–2079. https://doi.org/10.1890/09-0979.1

    Article  PubMed  Google Scholar 

  54. Ziter C, Turner MG (2019) No evidence of co-facilitation between a non-native Asian earthworm (Amynthas tokioensis) and invasive common buckthorn (Rhamnus cathartica) in experimental mesocosms. Biol Invasions 21:111–122. https://doi.org/10.1007/s10530-018-1808-y

    Article  Google Scholar 

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Acknowledgements

We thank Michelle Catania, Brendan Brown, Jeremiah Donovan, and the Soil Ecology Laboratory volunteers for their assistance in preparing materials and processing soil and seedling samples; Tom Olsen and the Natural Areas volunteer crew for their assistance in extracting eighty forest soil cores during a very hot summer day; and the members of Community Access Naperville for their assistance with mulching and watering the soil cores. Susan Lewis and Linda Williams graciously provided us with European buckthorn and white pine leaf litter. We thank Bradley Herrick and Marie Johnston at the University of Wisconsin-Madison Arboretum for their assistance in procuring soil for the tree seedling experiment and in Amynthas species identification. Additionally, we thank Kurt Dreisilker for allowing the field experiment to be established on The Morton Arboretum grounds. We also thank Wes Beaulieu for his statistical consultations. Jennifer Fraterrigo, Piper Hodson and Renee Gracon provided critical feedback on our experimental design, analyses, and interpretations. This project was funded and supported by the Center for Tree Science at The Morton Arboretum.

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Bethke, P.G., Midgley, M.G. Amynthas spp. impacts on seedlings and forest soils are tree species-dependent. Biol Invasions 22, 3145–3162 (2020). https://doi.org/10.1007/s10530-020-02315-4

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Keywords

  • Amynthas agrestis
  • Amynthas tokioensis
  • Asian jumping worm
  • Earthworm
  • Forest soil
  • Illinois
  • Seedlings