, Volume 178, Issue 1, pp 219–230 | Cite as

Invasive earthworms interact with abiotic conditions to influence the invasion of common buckthorn (Rhamnus cathartica)

  • Alexander M. RothEmail author
  • Timothy J. S. Whitfeld
  • Alexandra G. Lodge
  • Nico Eisenhauer
  • Lee E. Frelich
  • Peter B. Reich
Plant-microbe-animal interactions - Original research


Common buckthorn (Rhamnus cathartica L.) is one of the most abundant and ecologically harmful non-native plants in forests of the Upper Midwest United States. At the same time, European earthworms are invading previously glaciated areas in this region, with largely anecdotal evidence suggesting they compound the negative effects of buckthorn and influence the invasibility of these forests. Germination and seedling establishment are important control points for colonization by any species, and manipulation of the conditions influencing these life history stages may provide insight into why invasive species are successful in some environments and not others. Using a greenhouse microcosm experiment, we examined the effects of important biotic and abiotic factors on the germination and seedling establishment of common buckthorn. We manipulated light levels, leaf litter depth and earthworm presence to investigate the independent and interactive effects of these treatments on buckthorn establishment. We found that light and leaf litter depth were significant predictors of buckthorn germination but that the presence of earthworms was the most important factor; earthworms interacted with light and leaf litter to increase the number and biomass of buckthorn across all treatments. Path analysis suggested both direct and moisture-mediated indirect mechanisms controlled these processes. The results suggest that the action of earthworms may provide a pathway through which buckthorn invades forests of the Upper Midwest United States. Hence, researchers and managers should consider co-invasion of plants and earthworms when investigating invasibility and creating preemptive or post-invasion management plans.


Light Leaf litter Invasibility Lumbricus terrestris Rhamnus cathartica 



We thank the staff at Warner Nature Center for allowing us to collect soil and leaf litter for the experiment. We thank Cindy Buschena and Susan Barrott for their help throughout the experiment. We also thank the undergraduate student workers in the Reich lab for help planting and harvesting the experiment. Funding for this project was provided by the Minnesota Environment and Natural Resources Trust Fund as recommended by the Legislative-Citizen Commission on Minnesota Resources (LCCMR). Support was also provided by the Integrative Graduate Education and Research Traineeship: Risk Analysis for Introduced Species and Genotypes (NSF DGE-0653827); University of Minnesota Graduate School; the Wilderness Research Foundation; and the Dayton Fund of the Bell Museum of Natural History. N. E. gratefully acknowledges funding by the Deutsche Forschungsgemeinschaft (Ei 862/1, Ei 862/2).

Supplementary material

442_2014_3175_MOESM1_ESM.docx (43 kb)
Supplementary material 1 (DOCX 42 kb)


  1. Arbuckle JL (2012) IMB SPSS Amos 19 user’s guide. Amos, CrawfordvilleGoogle Scholar
  2. Azcarate FM, Peco B (2006) Effects of seed predation by ants on Mediterranean grassland related to seed size. J Veg Sci 17:353–360CrossRefGoogle Scholar
  3. Baskin JM, Baskin CC (1992) Seed germination biology of the weedy biennial Alliaria petiolata. Nat Area J 12:191–197Google Scholar
  4. Bellard C, Thuiller W, Leroy B, Genovesi P, Bakkenes M, Courchamp F (2013) Will climate change promote future invasions? Glob Change Biol 19:3740–3748CrossRefGoogle Scholar
  5. Benton TG, Solan M, Travis JMJ, Sait SM (2007) Microcosm experiments can inform global ecological problems. Trends Ecol Evol 22:516–521CrossRefPubMedGoogle Scholar
  6. Bisikwa J (2005) Establishment and management of European buckthorn (Rhamnus cathartica L.). Dissertation, University of MinnesotaGoogle Scholar
  7. Bohlen PJ, Groffman PM, Fahey TJ, Fisk MC, Suarez E, Pelletier DM, Fahey RT (2004) Ecosystem consequences of exotic earthworm invasion of north temperate forests. Ecosystems 7:1–12CrossRefGoogle Scholar
  8. Carpenter SR (1996) Microcosm experiments have limited relevance for community and ecosystem ecology. Ecology 77:677–680CrossRefGoogle Scholar
  9. Cintra R (1997) Leaf litter effects on seed and seedling predation of the palm Astrocaryum murumuru and the legume tree Dipteryx micrantha in Amazonian forest. J Trop Ecol 13:709–725CrossRefGoogle Scholar
  10. Costello DM, Lamberti GA (2008) Biological and physical effects of non-native earthworms on nitrogen cycling in riparian soils. Soil Biol Biochem 41:2230–2235CrossRefGoogle Scholar
  11. Dávalos A, Nuzzo V, Stark J, Blossey B (2013) Unexpected earthworm effects on forest understory plants. BMC Ecol 13:48. doi: 10.1186/1472-6785-13-48 CrossRefPubMedCentralPubMedGoogle Scholar
  12. Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534CrossRefGoogle Scholar
  13. Davis MA, Thompson K, Grime JP (2005) Invasibility: the local mechanism driving community assembly and species diversity. Ecography 28:696–704CrossRefGoogle Scholar
  14. Drake JA, Huxel GR, Hewitt CL (1996) Microcosms as models for generating and testing community theory. Ecology 77:670–677CrossRefGoogle Scholar
  15. 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. App Soil Ecol 75:145–149CrossRefGoogle Scholar
  16. Eisenhauer N, Scheu S (2008) Invasibility of experimental grassland communities: the role of earthworms, plant functional group identity and seed size. Oikos 117:1026–1036. doi: 10.1111/j.2008.0030-1299.16812.x CrossRefGoogle Scholar
  17. 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 39:1099–1110CrossRefGoogle Scholar
  18. 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
  19. Eisenhauer N, Schlaghamersky J, Reich PB, Frelich LE (2011) The wave towards a new steady state: effects of earthworm invasion on soil microbial functions. Biol Invasions 13:2191–2196CrossRefGoogle Scholar
  20. Eisenhauer N, Fisichelli NA, Frelich LE, Reich PB (2012) Interactive effects of global warming and ‘global worming’ on the initial establishment of native and exotic herbaceous plant species. Oikos 121:1121–1133CrossRefGoogle Scholar
  21. Elton CS (1958) The ecology of invasions by animals and plants. Methuen, LondonCrossRefGoogle Scholar
  22. Eschtruth AK, Battles JJ (2009) Assessing the relative importance of disturbance, herbivory, diversity, and propagule pressure in exotic plant invasion. Ecol Monogr 79:265–280CrossRefGoogle Scholar
  23. Fagan M, Peart D (2004) Impact of the invasive shrub glossy buckthorn (Rhamnus frangula L.) on juvenile recruitment by canopy trees. For Ecol Manage 194:95–107. doi: 10.1016/j.foreco.2004.02.015 CrossRefGoogle Scholar
  24. Frelich L, Reich P (2009) Wilderness Conservation in an era of global warming and invasive species: a case study from Minnesota’s Boundary Waters Canoe Area Wilderness. Nat Area J 29:385–393CrossRefGoogle Scholar
  25. Frelich L, Hale C, Scheu S et al (2006) Earthworm invasion into previously earthworm-free temperate and boreal forests. Biol Invasions 8:1235–1245. doi: 10.1007/s10530-006-9019-3 CrossRefGoogle Scholar
  26. Frelich LE, Peterson RO, Dovciak M, Reich PB, Vucetich JA, Eisenhauer N (2012) Trophic cascades, invasive species and body-size hierarchies interactively modulate climate change responses of ecotonal temperate-boral forest. PNAS 367:2955–2961Google Scholar
  27. Fridley JD, Stachowicz JJ, Naeem S, Sax DF, Seabloom EW, Smith MD, Stohlgren TJ, Tilman DE, Von Holle B (2007) The invasion paradox: reconciling pattern and process in species invasions. Ecology 88:3–17CrossRefPubMedGoogle Scholar
  28. Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081CrossRefPubMedGoogle Scholar
  29. Gassman A, Tosevsky I (2014) Biological control of Rhamnus cathartica: is it feasible? A revies of work done in 2002–2012. J Appl Entomol 138:1–13CrossRefGoogle Scholar
  30. Gill D, Marks P (1991) Tree and shrub seedling colonization of old fields in central New York. Ecol Monogr 61:183–205CrossRefGoogle Scholar
  31. Gilliam FS (2006) Response of the herbaceous layer of forest ecosystems to excess nitrogen deposition. J Ecol 94:1176–1191CrossRefGoogle Scholar
  32. Gourley LC (1985) A study of the ecology and spread of Buckthorn (Rhamnus cathartica L.) with particular reference to the University of Wisconsin Arboretum. Dissertation, University of Wisconsin, MadisonGoogle Scholar
  33. Gourley LC, Howell E (1984) Factors in buckthorn invasion documented; control measures checked (Wisconsin). Restor Manage Notes 2:87Google Scholar
  34. Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  35. Griffith B, Turke M, Weisser WW, Eisenhauer N (2013) Herbivore behavior in the anecic earthworm species Lumbricus terrestris L.? Eur J Soil Biol 55:62–65CrossRefGoogle Scholar
  36. Groffman PM, Bohlen PJ, Fisk MC, Fahey TJ (2004) Exotic earthworm invasion and microbial biomass in temperate forest soils. Ecosystems 7:45–54CrossRefGoogle Scholar
  37. Grubb P, Lee W, Kollmann J, Wilson J (1996) Interaction of irradiance and soil nutrient supply on growth of seedlings of ten European tall-shrub species and Fagus sylvatica. J Ecol 84:827–840CrossRefGoogle Scholar
  38. Gundale MJ (2002) Influence of exotic earthworms on the soil organic horizon and the rare fern Botrychium mormo. Conserv Biol 16:1555–1561CrossRefGoogle Scholar
  39. Hale CM, Frelich LE, Reich PB (2005) Exotic European earthworm invasion dynamics in northern hardwood forests of Minnesota, USA. Ecol Appl 15:848–860CrossRefGoogle Scholar
  40. Hale CM, Frelich LE, Reich PB (2006) Changes in hardwood forest understory plant communities in response to European earthworm invasion. Ecology 87:1637–1649CrossRefPubMedGoogle Scholar
  41. Hale CM, Frelich LE, Reich PB (2008) Exotic earthworm effects on hardwood forest floor, nutrient availability and native plants: a mesocosm study. Oecologia 155:509–518CrossRefPubMedGoogle Scholar
  42. Hartman KM, McCarthy BC (2004) Restoration of a forest understory after the removal of an invasive shrub, amur honeysuckle (Lonicera maackii). Restor Ecol 12:154–165. doi: 10.1111/j.1061-2971.2004.00368.x CrossRefGoogle Scholar
  43. Heimpel GE, Frelich LE, Landis DA et al (2010) European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biol Invasions 12:2913–2931. doi: 10.1007/s10530-010-9736-5 CrossRefGoogle Scholar
  44. Heneghan L, Clay C, Brundage C (2002) Rapid decomposition of buckthorn litter may change soil nutrient levels. Ecol Restor 20:108–111CrossRefGoogle Scholar
  45. Heneghan L, Rauschenberg C, Fatemi F, Workman M (2004) European buckthorn and its effects on some ecosystem properties in an urban woodland. Ecol Restor 22:275–280CrossRefGoogle Scholar
  46. Heneghan L, Fatemi F, Umek L et al (2006) The invasive shrub European buckthorn (Rhamnus cathartica L.) alters soil properties in Midwestern U.S. woodlands. Appl Soil Ecol 32:142–148. doi: 10.1016/j.apsoil.2005.03.009 CrossRefGoogle Scholar
  47. 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. doi: 10.1016/j.pedobi.2006.10.002 CrossRefGoogle Scholar
  48. Holdsworth AR, Frelich LE, Reich PB (2007) Effects of earthworm invasion on plant species richness in northern hardwood forests. Conserv Biol 21:997–1008CrossRefPubMedGoogle Scholar
  49. Holdsworth A, Frelich L, Reich P (2008) Litter decomposition in earthworm-invaded northern hardwood forests: role of invasion degree and litter chemistry. Ecoscience 15:536–544. doi: 10.2980/15-4-3151 CrossRefGoogle Scholar
  50. Holdsworth AR, Frelich LE, Reich PB (2012) Leaf litter disappearance in earthworm-invaded northern hardwood forests: role of tree species and the chemistry and diversity of litter. Ecosys 15:913–926CrossRefGoogle Scholar
  51. Huenneke LF, Hamburg SP, Koide R, Mooney HA, Vitousek PM (1990) Effects of soil resources on plant invasion and community structure in Californian serpentine grassland. Ecology 71:478–491CrossRefGoogle Scholar
  52. Invasive Species Program (2012) Invasive species of aquatic plants and wild animals in Minnesota: annual report for 2012. Minnesota Department of Natural Resources, St PaulGoogle Scholar
  53. Kennedy TA, Naeem S, Howe KM, Knops JMH, Tilman D, Reich P (2002) Biodiversity as a barrier to ecological invasion. Nature 417:636–638CrossRefPubMedGoogle Scholar
  54. Klionsky SM, Amatangelo KL, Waller DM (2011) Above- and belowground impacts of european buckthorn (Rhamnus cathartica) on four native forbs. Restor Ecol 19:728–737. doi: 10.1111/j.1526-100X.2010.00727.x CrossRefGoogle Scholar
  55. Knight KS (2006) Factors that influence invasion success of two woody invaders of forest understories. Dissertation, University of MinnesotaGoogle Scholar
  56. Knight KS, Kurylo JS, Endress AG et al (2007) Ecology and ecosystem impacts of common buckthorn (Rhamnus cathartica): a review. Biol Invasions 9:925–937. doi: 10.1007/s10530-007-9091-3 CrossRefGoogle Scholar
  57. Kollman J, Grubb PJ (1999) Recruitment of fleshy-fruited species under different shrub species: control by under-canopy environment. Ecol Res 14:9–21CrossRefGoogle Scholar
  58. Kurylo J, Endress A (2012) Rhamnus cathartica: notes on Its early history in North America. Northeast Nat 19:601–610CrossRefGoogle Scholar
  59. Kurylo J, Knight K (2007) Rhamnus cathartica: native and naturalized distribution and habitat preferences. J Torrey Bot Soc 134:420–430CrossRefGoogle Scholar
  60. Larson ER, Kipfmueller KF, Hale CM, Frelich LE, Reich PB (2010) Tree rings detect earthworm invasions and their effects in northern hardwood forests. Biol Invasion 12:1053–1066CrossRefGoogle Scholar
  61. Lawrence B, Fisk MC, Fahey TJ, Suarez ER (2003) Influence of nonnative earthworms on mycorrhizal colonization of sugar maple (Acer saccharum). New Phytol 157:145–153CrossRefGoogle Scholar
  62. Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989CrossRefGoogle Scholar
  63. Lodge DM (1993) Biological invasions—lessons for ecology. Trends Ecol Evol 8:133–137CrossRefPubMedGoogle Scholar
  64. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol App 10:689–710CrossRefGoogle Scholar
  65. McCormick MK, Parker KL, Szlavecz K, Whigham DF (2013) Native and exotic earthworms affect orchid seed loss. AoB Plant. doi: 10.1093/aobpla/plt018 Google Scholar
  66. McKinney AM, Goodell K (2010) Shading by invasive shrub reduces seed production and pollinator services in a native herb. Biol Invasions 12:2751–2763. doi: 10.1007/s10530-009-9680-4 CrossRefGoogle Scholar
  67. Milcu A, Schumacher J, Scheu S (2006) Earthworms (Lumbricus terrestris) affects plant seedling recruitment and microhabitat heterogeneity. Funct Ecol 20:261–268CrossRefGoogle Scholar
  68. Murphy GEP, Romanuk TN (2014) A meta-analysis of declines in local species richness from human disturbances. Ecol Evol 4:91–103CrossRefPubMedCentralPubMedGoogle Scholar
  69. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288CrossRefGoogle Scholar
  70. Polgar C, Gallinat A, Primack RB (2014) Drivers of leaf-out phenology and their implications for species invasions: insights from Thoreau’s Concord. New Phytol 202:106–115CrossRefPubMedGoogle Scholar
  71. Prati D, Bossdorf O (2004) Allelopathic inhibition of germination by Alliaria petiolata (Brassicaceae). Am J Bot 91:285–288CrossRefPubMedGoogle Scholar
  72. Regnier E, Harrison SK, Liu J et al (2008) Impact of an exotic earthworm on seed dispersal of an indigenous US weed. J Appl Ecol 45:1621–1629CrossRefGoogle Scholar
  73. Richardson DM, Pysek P, Rejmanek M, Barbour MG, Panetta FD, West CJ (2000) Naturalization and invasion of alien plants: concepts and definitions. Divers Distrib 6:93–107CrossRefGoogle Scholar
  74. Sacerdote AB, King RB (2014) Direct effects of an invasive European buckthorn metabolite on embryo survival and development in Xenopus laevis and Pseudacris triseriata. J Herpetol 48:51–58CrossRefGoogle Scholar
  75. Sackett TE, Smith SM, Basiliko N (2013) Indirect and direct effects of exotic earthworms on soil nutrient and carbon pools in North American temperate forests. Siol Biol Biochem 57:459–476CrossRefGoogle Scholar
  76. Schindler DW (1998) Replication versus realism: the need for ecosystem-scale experiments. Ecosystems 1:323–334CrossRefGoogle Scholar
  77. Schmidt K, Whelan C (1999) Effects of exotic Lonicera and Rhamnus on songbird nest predation. Conserv Biol 13:1502–1506CrossRefGoogle Scholar
  78. Schramm JW, Ehrenfeld JG (2010) Leaf litter and understory canopy shade limit the establishment, growth and reproduction of Microstegium vimineum. Biol Invasion 12:3195–3204CrossRefGoogle Scholar
  79. Seltzner S, Eddy TL (2003) Allelopathy in Rhamnus cathartica, European Buckthorn. Mich Bot 42:51–61Google Scholar
  80. Stewart JR, Graves WR (2004) Photosynthesis and growth of Rhamnus caroliniana during drought and flooding : comparisons to the invasive Rhamnus cathartica. HortScience 39:1280–1284Google Scholar
  81. Stinson KA, Campbell SA, Powell JR, Wolfe BR, Callaway RM, Thelen GC, Hallett SG, Prati D, Klironomos JN (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol. doi: 10.1371/journal.pbio.0040140 PubMedCentralPubMedGoogle Scholar
  82. Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176:256–273CrossRefPubMedGoogle Scholar
  83. Traba J, Azcarate FM, Peco B (2004) From what depth do seeds emerge? A soil seed bank experiment with Mediterranean grassland species. Seed Sci Res 14:297–303CrossRefGoogle Scholar
  84. USDA, NRCS (2014) The PLANTS database ( National Plant Data Team, Greensboro
  85. Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478Google Scholar
  86. Warren RJ, Bahn V, Bradford MA (2012) The interaction between propagule pressure, habitat suitability and density-dependent reproduction in species invasion. Oikos 121:874–881CrossRefGoogle Scholar
  87. Whitfeld TJS, Lodge AG, Roth AM, Reich PB (2014a) Community phylogenetic diversity and abiotic site characteristics influence abundance of the invasive plant Rhamnus cathartica L. J Plant Ecol 7:202–209CrossRefGoogle Scholar
  88. Whitfeld TJS, Roth AM, Lodge AG, Eisenhauer N, Frelich LE, Reich PB (2014b) Resident plant diversity and introduced earthworms have contrasting effects on the success of invasive plants. Biol Invasion. doi: 10.1007/s10530-014-0657-6 Google Scholar
  89. Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666CrossRefGoogle Scholar
  90. Wyckoff PH, Jansen R, Patten R (2005) The European buckthorn (Rhamnus cathartica) invasion in west central Minnesota. USDA Forest Service, St. Paul. Report no. FHTET-2005-09Google Scholar
  91. Wyckoff PH, Greiman R, Krueger A, Luce L (2012) Forest dynamics at Minnesota’s prairie-forest border driven by invasive buckthorn (Rhamnus cathartica) and native bur oak (Quercus macrocarpa). J Torrey Bot Soc 139:311–322CrossRefGoogle Scholar
  92. Yeo HHT, Chong KY, Yee ATK, Giam X, Corlett RT, Tan HTW (2014) Leaf litter depth as an important factor inhibiting seedlings establishment of an exotic palm in tropical secondary forest patches. Biol Invasion 16:381–392CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Alexander M. Roth
    • 1
    Email author
  • Timothy J. S. Whitfeld
    • 1
    • 2
  • Alexandra G. Lodge
    • 1
  • Nico Eisenhauer
    • 3
    • 4
    • 5
  • Lee E. Frelich
    • 1
  • Peter B. Reich
    • 1
    • 6
  1. 1.Department of Forest ResourcesUniversity of MinnesotaSt PaulUSA
  2. 2.Department of Ecology and Evolutionary BiologyBrown UniversityProvidenceUSA
  3. 3.Institute of EcologyFriedrich-Schiller-University JenaJenaGermany
  4. 4.German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-LeipzigLeipzigGermany
  5. 5.Institute for BiologyUniversity of LeipzigLeipzigGermany
  6. 6.Hawkesbury Institute for the EnvironmentUniversity of Western SydneyPenrithAustralia

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