Biological Invasions

, Volume 17, Issue 4, pp 1267–1281 | Cite as

Historical anthropogenic disturbances influence patterns of non-native earthworm and plant invasions in a temperate primary forest

  • Robin Beauséjour
  • I. Tanya Handa
  • Martin J. Lechowicz
  • Benjamin Gilbert
  • Mark Vellend
Original Paper

Abstract

Time lags are of potentially great importance during biological invasions. For example, significant delays can occur between the human activities permitting the arrival of an invader, the establishment of this new species, and the manifestation of its impacts. In this context, to assess the influence of anthropogenic disturbances, it may become necessary to include a historical perspective. In this study, we reconstructed the history of human activities in a temperate forest now protected as a nature reserve to evaluate the magnitude and duration of the impact of human disturbances (e.g. trails, old quarries), as well as environmental factors, in explaining the probability of occurrence and the intensity of invasion by non-native earthworms and plants. The present-day patterns of distribution and intensity of earthworms and plants were better explained by proximity to the oldest human disturbances (initiated more than a century ago) than by proximity to more recent disturbances or to all disturbances combined. We conclude that understanding present-day patterns of non-native species invasions may often require reconstructing the history of human disturbances that occurred decades or even centuries in the past.

Keywords

Human activities Ecological legacies Nature reserve Lumbricidae Taraxacum officinalis Historical ecology Time lag 

Supplementary material

10530_2014_794_MOESM1_ESM.docx (254 kb)
Supplementary material 1 (DOCX 253 kb)

References

  1. Addison JA (2009) Distribution and impacts of invasive earthworms in Canadian forest ecosystems. Biol Invasions 11:59–79CrossRefGoogle Scholar
  2. Bartuszevige AM, Hrenko RL, Gorchov DL (2007) Effects of leaf litter on establishment, growth and survival of invasive plant seedlings in a deciduous forest. Am Midl Nat 158:472–477CrossRefGoogle Scholar
  3. Belote RT, Jones RH (2009) Tree leaf litter composition and nonnative earthworms influence plant invasion in experimental forest floor mesocosms. Biol Invasions 11:1045–1052CrossRefGoogle Scholar
  4. Bennett JR, Vellend M, Lilley PL, Cornwell WK, Arcese P (2013) Abundance, rarity and invasion debt among exotic species in a patchy ecosystem. Biol Invasions 15:707–716CrossRefGoogle Scholar
  5. 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
  6. Brothers TS, Spingarn A (1992) Forest fragmentation and alien plant invasion of central Indiana old- growth forests. Conserv Biol 6:91–100CrossRefGoogle Scholar
  7. Brouillet L, Coursol F, Meades SJ, Favreau M, Anions M, Bélisle P, Desmet P (2010) VASCAN, the database of vascular plants of Canada. http://data.canadensys.net/vascan/. Accessed 02 Apr 2012
  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. Butt KR, Nuutinen V (1998) Reproduction of the earthworm Lumbricus terrestris Linné after the first mating. Can J Zool 76:104–109CrossRefGoogle Scholar
  10. Cameron EK, Bayne EM (2009) Road age and its importance in earthworm invasion of northern boreal forests. J Appl Ecol 46:28–36CrossRefGoogle Scholar
  11. Cameron EK, Bayne EM, Clapperton MJ (2007) Human-facilitated invasion of exotic earthworms into northern boreal forests. Ecoscience 14:482–490CrossRefGoogle Scholar
  12. Cameron EK, Bayne EM, Coltman DW (2008) Genetic structure of invasive earthworms Dendrobaena octaedra in the boreal forest of Alberta: insights into introduction mechanisms. Mol Ecol 17:1189–1197CrossRefPubMedGoogle Scholar
  13. Christensen RHB (2012) Ordinal-regression models for ordinal data R package version 2012-09-11. http://www.cran.r-project.org/package=ordinal/. Accessed 05 June 2012
  14. Crooks JA (2005) Lag times and exotic species: the ecology and management of biological invasions in slow-motion. Ecoscience 12:316–329CrossRefGoogle Scholar
  15. Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carre G, Marquez JRG, Gruber B, Lafourcade B, Leitao PJ, Munkemuller T, Mcclean C, Osborne PE, Reineking B, Schroder B, Skidmore AK, Zurell D, Lautenbach S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46CrossRefGoogle Scholar
  16. Dymond P, Scheu S, Parkinson D (1997) Density and distribution of Dendrobaena octaedra (Lumbricidae) in aspen and pine forests in the Canadian rocky mountain (Alberta). Soil Biol Biochem 29:265–273CrossRefGoogle Scholar
  17. 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
  18. Essl F, Mang T, Moser D (2012) Ancient and recent alien species in temperate forests: steady state and time lags. Biol Invasions 14:1331–1342CrossRefGoogle Scholar
  19. Flinn KM, Vellend M (2005) Recovery of forest plant communities in post-agricultural landscapes. Front Ecol Environ 3:243–250CrossRefGoogle Scholar
  20. Foster DR (2000) Conservation lessons and challenges from ecological history. Forest History Today Fall 2000: 2–11Google Scholar
  21. Frazer GW, Canham CD, Lertzman KP (2000) Gap light analyzer (GLA), version 20: image-processing software to analyze true-color, hemispherical canopy photographs. Bull Ecol Soc Am 81:191–197CrossRefGoogle Scholar
  22. 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
  23. Fridley JD (2011) Invasibility of communities and ecosystems. In: Simberloff D, Rejmanek M (eds) Encyclopedia of biological invasions. University of California Press, Oakland, pp 356–360Google Scholar
  24. Gavier-Pizarro GI, Radeloff VC, Stewart SI, Huebner CD, Keuler NS (2010) Rural housing is related to plant invasions in forests of southern Wisconsin, USA. Landsc Ecol 25:1505–1518CrossRefGoogle Scholar
  25. Gilbert B, Lechowicz MJ (2004) Neutrality, niches, and dispersal in a temperate forest understory. Proc Natl Acad Sci 101:7651–7656CrossRefPubMedCentralPubMedGoogle Scholar
  26. Gilbert B, Lechowicz MJ (2005) Invasibility and abiotic gradients: the positive correlation between native and exotic plant diversity. Ecology 86:1848–1855CrossRefGoogle Scholar
  27. Guisan A, Harrell FE (2000) Ordinal response regression models in ecology. J Veg Sci 11:617–626CrossRefGoogle Scholar
  28. Hale CM (2004) Allometric equations for estimation of ash-free dry mass from length measurements for selected European earthworm species (Lumbricidae) in the western Great Lakes region. Am Midl Nat 151:179–185CrossRefGoogle Scholar
  29. 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
  30. Harrell FE (2013) rms: regression modeling strategies. R package version 3.6-3. http://CRAN.R-project.org/package=rms. Accessed 06 May 2012
  31. Harrell FE, Margolis PA, Gove S, Mason KE, Mulholland EK, Lehmann D, Muhe L, Gatchalian S, Eichenwald HF (1998) Tutorial in biostatistics: development of a clinical prediction model for an ordinal outcome. Stat Med 17:909–944CrossRefPubMedGoogle Scholar
  32. 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
  33. Hendriksen NB (1990) Leaf litter selection by detritivore and geophagous earthworms. Biol Fertil Soils 10:17–21Google Scholar
  34. Hendrix PF, Bohlen PJ (2002) Exotic earthworm invasions in North America: ecological and policy implications. Bioscience 52:801–811CrossRefGoogle Scholar
  35. Hendrix PF, Callaham MA Jr, Drake JM, Huang C-, James SW, Snyder BA, Zhang W (2008) Pandora’s box contained bait: the global problem of introduced earthworms. Annu Rev Ecol Evol Syst 39:593–613CrossRefGoogle Scholar
  36. Hobbs RJ, Huenneke LF (1992) Disturbance, diversity, and invasion: implications for conservation. Conserv Biol 6:324–337CrossRefGoogle Scholar
  37. Holdsworth AR, Frelich LE, Reich PB (2007) Regional extent of an ecosystem engineer: earthworm invasion in northern hardwood forest. Ecol Appl 17:1666–1677CrossRefPubMedGoogle Scholar
  38. Jackson ST, Sax DF (2010) Balancing biodiversity in a changing environment: extinction debt, immigration credit and species turnover. Trends Ecol Evol 25:153–160CrossRefPubMedGoogle Scholar
  39. James SW, Hendrix PF (2004) Invasion of exotic earthworms into North America and other regions. In: Edwards CA (ed) Earthworm ecology. CRC Press, Boca Raton, pp 75–88Google Scholar
  40. Jodoin Y, Lavoie C, Villeneuve P, Theriault M, Beaulieu J, Belzile F (2008) Highways as corridors and habitats for the invasive common reed Phragmites australis in Quebec, Canada. J Appl Ecol 45:459–466CrossRefGoogle Scholar
  41. Josefsson T, Hörnberg G, Östlund L (2009) Long-term human impact and vegetation changes in a boreal forest reserve: implications for the use of protected areas as ecological references. Ecosystems 12:1017–1036CrossRefGoogle Scholar
  42. Kalisz PJ, Dotson DB (1989) Land-use history and the occurrence of exotic earthworms in the mountains of eastern Kentucky. Am Midl Nat 122:288–297CrossRefGoogle Scholar
  43. Kolanowska M (2013) Niche conservatism and the future potential range of Epipactis helleborine (Orchidaceae). PLoS ONE 8:e77352CrossRefPubMedCentralPubMedGoogle Scholar
  44. Koncz G, Török P, Papp M, Matus G, Tóthmérész B (2011) Penetration of weeds into the herbaceous understorey and soil seed bank of a Turkey oak-sessile oak forest in Hungary. Community Ecol 12:227–233CrossRefGoogle Scholar
  45. Kostel-Hughes F, Young TP, Carreiro MM (1998) Forest leaf litter quantity and seedling occurrence along an urban-rural gradient. Urban Ecosyst 2:263–278CrossRefGoogle Scholar
  46. Kourtev PS, Huang WZ, Ehrenfeld JG (1999) Differences in earthworm densities and nitrogen dynamics in soils under exotic and native plant species. Biol Invasions 1:237–245CrossRefGoogle Scholar
  47. Larson ER, Kipfmueller KF, Hale CM, Frelich LE, Reich PB (2010) Tree rings detect earthworm invasions and their effects in northern Hardwood forests. Biol Invasions 12:1053–1066CrossRefGoogle Scholar
  48. Lavoie C, Saint-Louis A, Guay G, Groeneveld E, Villeneuve P (2012) Naturalization of exotic plant species in north-eastern North America: trends and detection capacity. Divers Distrib 18:180–190CrossRefGoogle Scholar
  49. Leckie S, Vellend M, Bell G, Waterway MJ, Lechowicz MJ (2000) The seed bank in an old-growth, temperate deciduous forest. Can J Bot 78:181–192Google Scholar
  50. Lilley PL, Vellend M (2009) Negative native-exotic diversity relationship in oak savannas explained by human influence and climate. Oikos 118:1373–1382CrossRefGoogle Scholar
  51. MacDougall AS, Turkington R (2005) Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86:42–55CrossRefGoogle Scholar
  52. Magnuson JJ (1990) Long-term ecological research and the invisible present. Bioscience 40:495–501CrossRefGoogle Scholar
  53. Martin PH, Marks PL (2006) Intact forests provide only weak resistance to a shade-tolerant invasive Norway maple (Acer platanoides L.). J Ecol 94:1070–1079CrossRefGoogle Scholar
  54. Martin PH, Canham CD, Marks PL (2009) Why forests appear resistant to exotic plant invasions: intentional introductions, stand dynamics, and the role of shade tolerance. Front Ecol Environ 7:142–149CrossRefGoogle Scholar
  55. Mazerolle MJ (2013) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 1.27. http://CRAN.R-project.org/package=AICcmodavg. Accessed 08 May 2012
  56. Meunier G, Lavoie C (2012) Roads as corridors for invasive plant species: new evidence from smooth bedstraw (Galium mollugo). Invasive Plant Sci Manag 5:92–100CrossRefGoogle Scholar
  57. Natural Resources Research Institute (NRRI) (2011) Great lakes worm watch. http://http://www.nrri.umn.edu/worms/. Accessed 10 Apr 2012
  58. 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 23:966–974CrossRefPubMedGoogle Scholar
  59. Piqueray J, Cristofoli S, Bisteau E, Palm R, Mahy G (2011) Testing coexistence of extinction debt and colonization credit in fragmented calcareous grasslands with complex historical dynamics. Landsc Ecol 26:823–836CrossRefGoogle Scholar
  60. Pollnac F, Seipel T, Repath C, Rew LJ (2012) Plant invasion at landscape and local scales along roadways in the mountainous region of the Greater Yellowstone Ecosystem. Biol Invasions 14:1753–1763CrossRefGoogle Scholar
  61. Reich PB, Oleksyn J, Modrzynski J, Mrozinski P, Hobbie SE, Eissenstat DM, Chorover J, Chadwick OA, Hale CM, Tjoelker MG (2005) Linking litter calcium, earthworms and soil properties: a common garden test with 14 tree species. Ecol Lett 8:811–818CrossRefGoogle Scholar
  62. Rejmanek M (1989) Invasibility of plant communities. In: Drake JA (ed) Biological invasions: a global perspective. Wiley, Hoboken, pp 369–388Google Scholar
  63. Reynolds JW (1977) The earthworms (Lumbricidae and Sparganophilidae) of Ontario. Royal Ontario Museum, TorontoGoogle Scholar
  64. Sackett TE, Smith SM, Basiliko N (2012) Exotic earthworm distribution in a mixed-use northern temperate forest region: influence of disturbance type, development age, and soils. Can J Forest Res 42:375–381CrossRefGoogle Scholar
  65. Shartell LM, Lilleskov EA, Storer AJ (2013) Predicting exotic earthworm distribution in the northern Great Lakes region. Biol Invasions 15:1665–1675Google Scholar
  66. Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9:912–919CrossRefPubMedGoogle Scholar
  67. Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32CrossRefGoogle Scholar
  68. Stoscheck LM, Sherman RE, Suarez ER, Fahey TJ (2012) Exotic earthworm distributions did not expand over a decade in a hardwood forest in New York State. Appl Soil Ecol 62:124–130CrossRefGoogle Scholar
  69. Suarez ER, Tierney GL, Fahey TJ, Fahey R (2006) Exploring patterns of exotic earthworm distribution in a temperate hardwood forest in south-central New York, USA. Landsc Ecol 21:297–306CrossRefGoogle Scholar
  70. Sutherland WJ, Bardsley S, Bennun L, Clout M, Côté IM, Depledge MH, Dicks LV, Dobson AP, Fellman L, Fleishman E, Gibbons DW, Impey AJ, Lawton JH, Lickorish F, Lindenmayer DB, Lovejoy TE, Mac Nally R, Madgwick J, Peck LS, Pretty J, Prior SV, Redford KH, Scharlemann JPW, Spalding M, Watkinson AR (2011) Horizon scan of global conservation issues for 2011. Trends Ecol Evol 26:10–16CrossRefPubMedGoogle Scholar
  71. 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
  72. Tiunov AV, Hale CM, Holdsworth AR, Vsevolodova-Perel TS (2006) Invasion patterns of Lumbricidae into the previously earthworm-free areas of northeastern Europe and the western Great Lakes region of North America. Biol Invasions 8:1223–1234CrossRefGoogle Scholar
  73. Valckx J, Govers G, Hermy M, Muys B (2011) Optimizing earthworm sampling in ecosystems. In: Karaca E (ed) Biology of earthworms. Springer, New York, pp 19–38CrossRefGoogle Scholar
  74. Vallet J, Beaujouan V, Pithon J, Rozé F, Daniel H (2010) The effects of urban or rural landscape context and distance from the edge on native woodland plant communities. Biodivers Conserv 19:3375–3392CrossRefGoogle Scholar
  75. Vellend M, Brown CD, Kharouba HM, McCune JL, Myers-Smith IH (2013) Historical ecology: using unconventional data sources to test for effects of global environmental change. Am J Bot 100:1294–1305CrossRefPubMedGoogle Scholar
  76. Von Holle B, Delcourt HR, Simberloff D (2003) The importance of biological inertia in plant community resistance to invasion. J Veg Sci 14:425–432CrossRefGoogle Scholar
  77. Wironen M, Moore TR (2006) Exotic earthworm invasion increases soil carbon and nitrogen in an old-growth forest in southern Quebec. Can J Forest Res 36:845–854CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Robin Beauséjour
    • 1
  • I. Tanya Handa
    • 2
  • Martin J. Lechowicz
    • 3
  • Benjamin Gilbert
    • 4
  • Mark Vellend
    • 1
  1. 1.Département de biologieUniversité de SherbrookeSherbrookeCanada
  2. 2.Département de sciences biologiquesUniversité du Québec à MontréalMontrealCanada
  3. 3.Department of BiologyMcGill UniversityMontrealCanada
  4. 4.Department of Ecology and Evolutionary BiologyUniversity of TorontoTorontoCanada

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