Biological Invasions

, Volume 21, Issue 1, pp 111–122 | Cite as

No evidence of co-facilitation between a non-native Asian earthworm (Amynthas tokioensis) and invasive common buckthorn (Rhamnus cathartica) in experimental mesocosms

  • Carly ZiterEmail author
  • Monica G. Turner
Original Paper


Non-native invasive earthworms are known drivers of forest change in north temperate forests. Much understanding of earthworm invasion is based on species of European origin, but concern about Asian pheretimoid earthworms (e.g. Asian jumping worms, Amynthas spp.) is increasing. Some effects of Amynthas spp. on soil properties and biota have been studied, but little is known about interaction of Amynthas spp. with plants. Potential interaction between Amynthas spp. and invasive buckthorn (Rhamnus cathartica) is of particular interest given hypothesized co-facilitation between R. cathartica and European earthworms—cited by some as components of an “invasional meltdown”. We used reciprocal mesocosm experiments in Wisconsin, USA, to test for co-facilitation between Amynthas tokioensis and R. cathartica. We asked: (1) Are jumping worms more successful in environments invaded by buckthorn? (2) Does jumping worm activity increase buckthorn germination and establishment? Counter to expectations, co-facilitation was not supported, and we found evidence to the contrary. There was no increase in litter loss (indicative of consumption by jumping worms) or jumping worm fecundity in buckthorn-invaded environments, and buckthorn germination was unaffected by increased jumping worm densities. Counter to our hypothesis, jumping worm fecundity was greater in buckthorn-free soils than in buckthorn-invaded soils. Our results show no experimental evidence of co-facilitation by either of these invasive species, and highlight potential differences in ecological impact of non-native invasive earthworm taxa that vary in life-history and functional dynamics.


Asian jumping worm Amynthas tokioensis Earthworms Rhamnus cathartica Wisconsin 



We thank Kristin Braziunas, Rose Graves, Winslow Hansen, and especially Daniela Robledo for field assistance, and Chris Kucharik, Claudio Gratton, Ellen Damschen, Steve Carpenter, Jiangxiao Qiu and Katie Laushman for helpful comments on development of these ideas. Thanks to Eric Pedersen for field assistance and statistical advice. Two anonymous reviewers also provided constructive comments on this manuscript. We appreciate logistical support from Susan Carpenter and Bradley Herrick, and thank the University of Wisconsin–Madison Arboretum for providing the field facility. Thanks to Marie Johnston for technical expertise with earthworm identification and cocoon processing, as well as arboretum volunteers for cocoon processing assistance. We acknowledge funding from the US National Science Foundation, especially the Long-term Ecological Research (DEB-1440297) and Water, Sustainability and Climate (DEB-1038759) Programs, and support to MGT from the University of Wisconsin-Madison Vilas Trust. CZ acknowledges support from a Natural Science and Engineering Research Council of Canada doctoral fellowship, National Geographic Young Explorer Grant (Grant Number 9857-16), and PEO Scholar Award. CZ and MGT conceived the ideas and designed methodology; CZ collected and analyzed the data and led the writing of the manuscript. Both authors contributed critically to all drafts and gave final approval for publication.

Supplementary material

10530_2018_1808_MOESM1_ESM.pdf (722 kb)
Supplementary material 1 (PDF 721 kb)


  1. Asshoff R, Scheu S, Eisenhauer N (2010) Different earthworm ecological groups interactively impact seedling establishment. Eur J Soil Biol 46:330–334CrossRefGoogle Scholar
  2. Bahlai CA, Sikkema S, Hallett RH, Newman J, Schaafsma AW (2010) Modeling distribution and abundance of soybean aphid in soybean fields using measurements from the surrounding landscape. Environ Entomol 39:50–56CrossRefGoogle Scholar
  3. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using LME4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  4. Bezemer TM, van Dam NM (2005) Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol Evolu 20:617–624CrossRefGoogle Scholar
  5. Blouin M, Hodson ME, Delgado EA, Baker G, Brussaard L, Butt KR, Dai J, Dendooven L, Peres G, Tondoh JE, Cluzeau D, Brun JJ (2013) A review of earthworm impact on soil function and ecosystem services. Eur J Soil Sci 64:161–182CrossRefGoogle Scholar
  6. Bohlen PJ, Scheu S, Hale CM, McLean MA, Migge S, Groffman PM, Parkinson D (2004) Non-native invasive earthworms as agents of change in northern temperate forests. Front Ecol Environ 2:427–435CrossRefGoogle Scholar
  7. Brooker RW, Maestre FT, Callaway RM, Lortie CL, Cavieres LA, Kunstler G, Liancourt P, Tielborger K, Travis JMJ, Anthelme F, Armas C, Coll L, Corcket E, Delzon S, Forey E, Kikvidze Z, Olofsson J, Pugnaire F, Quiroz CL, Saccone P, Schiffers K, Seifan M, Touzard B, Michalet R (2008) Facilitation in plant communities: the past, the present, and the future. J Ecol 96:18–34CrossRefGoogle Scholar
  8. 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 9:197–202CrossRefGoogle Scholar
  9. 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 47:466–470CrossRefGoogle Scholar
  10. Cassin CM, Kotanen PM (2016) Invasive earthworms as seed predators of temperate forest plants. Biol Invasions 18:1567–1580CrossRefGoogle Scholar
  11. Chang C-H, Snyder BA, Szlavecz K (2016a) Asian pheretimoid earthworms in North America north of Mexico: an illustrated key to the genera Amynthas, Metaphire, Pithemera, and Polypheretima (Clitellata: Megascolecidae). Zootaxa 4179:495–529CrossRefGoogle Scholar
  12. Chang C-H, Szlavecz K, Filley T, Buyer JS, Bernard MJ, Pitz SL (2016b) Belowground competition among invading detritivores. Ecology 97:160–170CrossRefGoogle Scholar
  13. Chang C-H, Szlavecz K, Buyer JS (2016c) Species-specific effects of earthworms on microbial communities and the fate of litter-derived carbon. Soil Biol Biochem 100:129–139CrossRefGoogle Scholar
  14. Chang C-H, Johnston MR, Görres JH, Dávalos A, McHugh D, Szlavecz K (2017a) Co-invasion of three Asian earthworms, Metaphire hilgendorfi, Amynthas agrestis and Amynthas tokioensis in the USA. Biol Invasions 4:843–848Google Scholar
  15. Chang C-H, Szlavecz K, Buyer JS (2017b) Amynthas agrestis invasion increases microbial biomass in Mid-Atlantic deciduous forests. Soil Biol Biochem 114:189–199CrossRefGoogle Scholar
  16. Eisenhauer N, Butenschoen O, Radsick S, Scheu S (2010) Earthworms as seedling predators: importance of seeds and seedlings for earthworm nutrition. Soil Biol Biochem 42:1245–1252CrossRefGoogle Scholar
  17. Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand Oaks CAGoogle Scholar
  18. Frelich LE, Hale CM, Scheu S, Holdsworth AR, Heneghan L, Bohlen PJ, Reich PB (2006) Earthworm invasion into previously earthworm-free temperate and boreal forests. Biol Invasions 8:1235–1245CrossRefGoogle Scholar
  19. Gates GE (1982) Farewell to North American megadriles. Megadrilogica 4:12–77Google Scholar
  20. Gorsuch JP, Owen PC (2014) Potential edaphic and aquatic predators of a nonindigenous Asian Earthworm (Amynthas agrestis) in the eastern United States. Northeast Nat 21:652–661CrossRefGoogle Scholar
  21. Greiner HG, Costello DM, Tiegs SD (2010) Allometric estimation of earthworm ash-free dry mass from diameters and lengths of select megascolecid and lumbricid species. Pedobiologia 53:247–252CrossRefGoogle Scholar
  22. 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 14:2017–2027CrossRefGoogle Scholar
  23. Hale CM, Frelich LE, Reich PB (2006) Changes in hardwood forest understory plant communities in response to European earthworm invasions. Ecology 87:1637–1649CrossRefGoogle Scholar
  24. Heimpel GE, Frelich LE, Landis DA, Hopper KR, Hoelmer KA, Sezen Z, Asplen MK, Wu K (2010) European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biol Invasions 12:2913–2931CrossRefGoogle Scholar
  25. Hendrix PF, Bohlen PJ (2002) Exotic Earthworm invasions in North America: ecological and policy implications. Bioscience 52:801–811CrossRefGoogle Scholar
  26. Heneghan L (2003) And when they got together… impacts of Eurasian earthworm and invasive shrubs on Chicago woodland ecosystems. Chic Wilderness J 1:27–31Google Scholar
  27. Heneghan L, Clay C, Brundage C (2002) Rapid decomposition of buckthorn litter may change soil nutrient levels. Ecol Restor 20:108–111CrossRefGoogle Scholar
  28. Heneghan L, Fatemi F, Umek L, Grady K, Fagen K, Workman M (2006) The invasive shrub European buckthorn (Rhamnus cathartica, L.) alters soil properties in Midwestern U.S. woodlands. Appl Soil Ecol 32:142–148CrossRefGoogle Scholar
  29. 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 50:543–551CrossRefGoogle Scholar
  30. Iannone BV III, 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 52:78–88CrossRefGoogle Scholar
  31. Ikeda H, Callaham MA, O’Brien JJ, Hornsby BS, Wenk E (2015) Can the invasive earthworm, Amynthas agrestis, be controlled with prescribed fire? Soil Biol Biochem 82:21–27CrossRefGoogle Scholar
  32. Knight KS, Kurylo JS, Endress AG, Stewart JR, Reich PB (2007) Ecology and ecosystem impacts of common buckthorn (Rhamnus cathartica): a review. Biol Invasions 9:925–937CrossRefGoogle Scholar
  33. Kurylo JS, Knight KS, Stewart JR, Endress AG (2007) Rhamnus cathartica: native and naturalized distribution and habitat preferences. J Torrey Bot Soc 134:420–430CrossRefGoogle Scholar
  34. Lacasella F, Marta S, Singh A, Stack Whitney K, Hamilton K, Townsend P, Kucharik CJ, Meehan TD, Gratton C (2017) From pest data to abundance-based risk maps combining eco-physiological knowledge, weather, and habitat variability. Ecol Appl 27:575–588CrossRefGoogle Scholar
  35. 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(7):1671–1685CrossRefGoogle Scholar
  36. Lawrence AP, Bowers MA (2002) A test of the `hot’ mustard extraction method of sampling earthworms. Soil Biol Biochem 34:549–552CrossRefGoogle Scholar
  37. Levine JM, Vila M, Antonio CMD, Dukes JS, Grigulis K, Lavorel S (2003) Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc Lond B Biol Sci 270:775–781CrossRefGoogle Scholar
  38. Madritch MD, Lindroth RL (2009) Removal of invasive shrubs reduces exotic earthworm populations. Biol Invasions 11:663–671CrossRefGoogle Scholar
  39. Mascaro J, Schnitzer SA (2007) Rhamnus cathartica L. (common buckthorn) as an ecosystem dominant in southern Wisconsin forests. Northeast Nat 14:387–402CrossRefGoogle Scholar
  40. Mascaro J, Schnitzer SA (2011) Dominance by the introduced tree Rhamnus cathartica (common buckthorn) may limit aboveground carbon storage in Southern Wisconsin forests. Forest Ecol Manag 261:545–550CrossRefGoogle Scholar
  41. Mueller KE, Lodge AG, Roth AM, Whitfeld TJS, Hobbie SE, Reich PB (2018) A tale of two studies: detection and attribution of the impacts of invasive plants in observational surveys. J Appl Ecol 147:60Google Scholar
  42. Qiu J, Turner MG (2016) Effects of non-native Asian earthworm invasionon temperate forest and prairie soils in the Midwestern US. Biol Invasions 19:73–88CrossRefGoogle Scholar
  43. Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmanek M (2000) Plant invasions-the role of mutualisms. Biol Rev Camb Philos Soc 75:65–93CrossRefGoogle Scholar
  44. Roth AM, Whitfeld TJS, Lodge AG, Eisenhauer N, Frelich LE, Reich PB (2015) Invasive earthworms interact with abiotic conditions to influence the invasion of common buckthorn (Rhamnus cathartica). Oecologia 178:219–230CrossRefGoogle Scholar
  45. Scheu S (2003) Effects of earthworms on plant growth: patterns and perspectives. Pedobiologia 47:846–856Google Scholar
  46. Schult N, Pittenger K, Davalos S, McHugh D (2016) Phylogeographic analysis of invasive Asian earthworms (Amynthas) in the northeast United States. Invertebr Biol 135:314–327CrossRefGoogle Scholar
  47. Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9:912–919CrossRefGoogle Scholar
  48. Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32CrossRefGoogle Scholar
  49. 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 13:349–358CrossRefGoogle Scholar
  50. 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 57:212–216CrossRefGoogle Scholar
  51. Stewart JR, Graves WR (2005) Seed germination of Rhamnus caroliniana: implications for ecology and horticulture. HortScience 40:767–770Google Scholar
  52. Vitousek PM (1990) Biological invasions and ecosystem processes—towards an integration of population biology and ecosystem studies. Oikos 57:7–13CrossRefGoogle Scholar
  53. Wyckoff PH, Shaffer A, Hucka B, Bombyk M, Wipf A (2014) No evidence of facilitation between invasive Rhamnus cathartica (European buckthorn) and invasive earthworms in west central Minnesota. Pedobiologia J Soil Ecol 57:311–317CrossRefGoogle Scholar
  54. Zhang W, Hendrix PF, Snyder BA, Molina M, Li J, Rao X, Siemann E, Fu S (2010) Dietary flexibility aids Asian earthworm invasion in North American forests. Ecology 91:2070–2079CrossRefGoogle Scholar
  55. Ziemba JL, Cameron AC, Peterson K, Hickerson CM, Anthony CD (2015) Invasive Asian earthworms of the genus Amynthas alter microhabitat use by terrestrial salamanders. Can J Zool 93:805–811CrossRefGoogle Scholar
  56. Ziemba JL, Hickerson C-AM, Anthony CD (2016) Invasive Asian earthworms negatively impact keystone terrestrial salamanders. PLoS ONE 11:e0151591CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Department of ZoologyUniversity of Wisconsin-MadisonMadisonUSA

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