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

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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.

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References

  • Addison JA (2009) Distribution and impacts of invasive earthworms in Canadian forest ecosystems. Biol Invasions 11:59–79

    Article  Google Scholar 

  • 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 158:472–477

    Article  Google Scholar 

  • Belote RT, Jones RH (2009) Tree leaf litter composition and nonnative earthworms influence plant invasion in experimental forest floor mesocosms. Biol Invasions 11:1045–1052

    Article  Google Scholar 

  • 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 15:707–716

    Article  Google Scholar 

  • 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 2:427–435

    Article  Google Scholar 

  • Brothers TS, Spingarn A (1992) Forest fragmentation and alien plant invasion of central Indiana old- growth forests. Conserv Biol 6:91–100

    Article  Google Scholar 

  • 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

  • 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

    Article  Google Scholar 

  • Butt KR, Nuutinen V (1998) Reproduction of the earthworm Lumbricus terrestris Linné after the first mating. Can J Zool 76:104–109

    Article  Google Scholar 

  • Cameron EK, Bayne EM (2009) Road age and its importance in earthworm invasion of northern boreal forests. J Appl Ecol 46:28–36

    Article  Google Scholar 

  • Cameron EK, Bayne EM, Clapperton MJ (2007) Human-facilitated invasion of exotic earthworms into northern boreal forests. Ecoscience 14:482–490

    Article  Google Scholar 

  • 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 17:1189–1197

    Article  CAS  PubMed  Google Scholar 

  • 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

  • Crooks JA (2005) Lag times and exotic species: the ecology and management of biological invasions in slow-motion. Ecoscience 12:316–329

    Article  Google Scholar 

  • 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 36:27–46

    Article  Google Scholar 

  • 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 29:265–273

    Article  Google Scholar 

  • 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 121:1121–1133

    Article  Google Scholar 

  • Essl F, Mang T, Moser D (2012) Ancient and recent alien species in temperate forests: steady state and time lags. Biol Invasions 14:1331–1342

    Article  Google Scholar 

  • Flinn KM, Vellend M (2005) Recovery of forest plant communities in post-agricultural landscapes. Front Ecol Environ 3:243–250

    Article  Google Scholar 

  • Foster DR (2000) Conservation lessons and challenges from ecological history. Forest History Today Fall 2000: 2–11

  • 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 81:191–197

    Article  Google Scholar 

  • 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 8:1235–1245

    Article  Google Scholar 

  • Fridley JD (2011) Invasibility of communities and ecosystems. In: Simberloff D, Rejmanek M (eds) Encyclopedia of biological invasions. University of California Press, Oakland, pp 356–360

    Google Scholar 

  • 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 25:1505–1518

    Article  Google Scholar 

  • Gilbert B, Lechowicz MJ (2004) Neutrality, niches, and dispersal in a temperate forest understory. Proc Natl Acad Sci 101:7651–7656

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gilbert B, Lechowicz MJ (2005) Invasibility and abiotic gradients: the positive correlation between native and exotic plant diversity. Ecology 86:1848–1855

    Article  Google Scholar 

  • Guisan A, Harrell FE (2000) Ordinal response regression models in ecology. J Veg Sci 11:617–626

    Article  Google Scholar 

  • 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 151:179–185

    Article  Google Scholar 

  • Hale CM, Frelich LE, Reich PB (2005) Exotic European earthworm invasion dynamics in northern hardwood forests of Minnesota, USA. Ecol Appl 15:848–860

    Article  Google Scholar 

  • Harrell FE (2013) rms: regression modeling strategies. R package version 3.6-3. http://CRAN.R-project.org/package=rms. Accessed 06 May 2012

  • 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 17:909–944

    Article  PubMed  Google Scholar 

  • 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 12:2913–2931

    Article  Google Scholar 

  • Hendriksen NB (1990) Leaf litter selection by detritivore and geophagous earthworms. Biol Fertil Soils 10:17–21

    Google Scholar 

  • Hendrix PF, Bohlen PJ (2002) Exotic earthworm invasions in North America: ecological and policy implications. Bioscience 52:801–811

    Article  Google Scholar 

  • 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 39:593–613

    Article  Google Scholar 

  • Hobbs RJ, Huenneke LF (1992) Disturbance, diversity, and invasion: implications for conservation. Conserv Biol 6:324–337

    Article  Google Scholar 

  • Holdsworth AR, Frelich LE, Reich PB (2007) Regional extent of an ecosystem engineer: earthworm invasion in northern hardwood forest. Ecol Appl 17:1666–1677

    Article  PubMed  Google Scholar 

  • Jackson ST, Sax DF (2010) Balancing biodiversity in a changing environment: extinction debt, immigration credit and species turnover. Trends Ecol Evol 25:153–160

    Article  PubMed  Google Scholar 

  • 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 75–88

    Google Scholar 

  • 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 45:459–466

    Article  Google Scholar 

  • 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 12:1017–1036

    Article  Google Scholar 

  • Kalisz PJ, Dotson DB (1989) Land-use history and the occurrence of exotic earthworms in the mountains of eastern Kentucky. Am Midl Nat 122:288–297

    Article  Google Scholar 

  • Kolanowska M (2013) Niche conservatism and the future potential range of Epipactis helleborine (Orchidaceae). PLoS ONE 8:e77352

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 12:227–233

    Article  Google Scholar 

  • Kostel-Hughes F, Young TP, Carreiro MM (1998) Forest leaf litter quantity and seedling occurrence along an urban-rural gradient. Urban Ecosyst 2:263–278

    Article  Google Scholar 

  • Kourtev PS, Huang WZ, Ehrenfeld JG (1999) Differences in earthworm densities and nitrogen dynamics in soils under exotic and native plant species. Biol Invasions 1:237–245

    Article  Google Scholar 

  • 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 12:1053–1066

    Article  Google Scholar 

  • 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 18:180–190

    Article  Google Scholar 

  • Leckie S, Vellend M, Bell G, Waterway MJ, Lechowicz MJ (2000) The seed bank in an old-growth, temperate deciduous forest. Can J Bot 78:181–192

    Google Scholar 

  • Lilley PL, Vellend M (2009) Negative native-exotic diversity relationship in oak savannas explained by human influence and climate. Oikos 118:1373–1382

    Article  Google Scholar 

  • MacDougall AS, Turkington R (2005) Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86:42–55

    Article  Google Scholar 

  • Magnuson JJ (1990) Long-term ecological research and the invisible present. Bioscience 40:495–501

    Article  Google Scholar 

  • Martin PH, Marks PL (2006) Intact forests provide only weak resistance to a shade-tolerant invasive Norway maple (Acer platanoides L.). J Ecol 94:1070–1079

    Article  Google Scholar 

  • 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 7:142–149

    Article  Google Scholar 

  • 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

  • Meunier G, Lavoie C (2012) Roads as corridors for invasive plant species: new evidence from smooth bedstraw (Galium mollugo). Invasive Plant Sci Manag 5:92–100

    Article  Google Scholar 

  • Natural Resources Research Institute (NRRI) (2011) Great lakes worm watch. http://http://www.nrri.umn.edu/worms/. Accessed 10 Apr 2012

  • 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 23:966–974

    Article  PubMed  Google Scholar 

  • 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 26:823–836

    Article  Google Scholar 

  • 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 14:1753–1763

    Article  Google Scholar 

  • 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 8:811–818

    Article  Google Scholar 

  • Rejmanek M (1989) Invasibility of plant communities. In: Drake JA (ed) Biological invasions: a global perspective. Wiley, Hoboken, pp 369–388

    Google Scholar 

  • Reynolds JW (1977) The earthworms (Lumbricidae and Sparganophilidae) of Ontario. Royal Ontario Museum, Toronto

    Google Scholar 

  • 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 42:375–381

    Article  Google Scholar 

  • Shartell LM, Lilleskov EA, Storer AJ (2013) Predicting exotic earthworm distribution in the northern Great Lakes region. Biol Invasions 15:1665–1675

  • Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9:912–919

    Article  PubMed  Google Scholar 

  • Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32

    Article  Google Scholar 

  • 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 62:124–130

    Article  Google Scholar 

  • 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 21:297–306

    Article  Google Scholar 

  • 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 26:10–16

    Article  PubMed  Google Scholar 

  • Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176:256–273

    Article  PubMed  Google Scholar 

  • 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 8:1223–1234

    Article  Google Scholar 

  • 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 19–38

    Chapter  Google Scholar 

  • 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 19:3375–3392

    Article  Google Scholar 

  • 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 100:1294–1305

    Article  PubMed  Google Scholar 

  • Von Holle B, Delcourt HR, Simberloff D (2003) The importance of biological inertia in plant community resistance to invasion. J Veg Sci 14:425–432

    Article  Google Scholar 

  • 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 36:845–854

    Article  Google Scholar 

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Acknowledgments

We are grateful to McGill University for its stewardship of the Gault Nature Reserve. Thank you to David Maneli for logistic support, Anne-Sophie Goyette, Leonardo Claver Garcia and Véronique Demers for field and laboratory assistance, and the professionals of the Centre d’Étude de la Forêt Mélanie Desrochers, Daniel Lessieur and Marc Mazerolle for technical support. We thank two anonymous reviewers for their helpful comments on the manuscript. Financial support was provided through Natural Sciences and Engineering Research Council (NSERC) grants to MV and ITH and graduate scholarships to RB from NSERC and the Fonds de Recheche du Québec Nature et Technologies.

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Authors and Affiliations

  1. Département de biologie, Université de Sherbrooke, Sherbrooke, QC, J1K 2R1, Canada

    Robin Beauséjour & Mark Vellend

  2. Département de sciences biologiques, Université du Québec à Montréal, C.P. 8888, succ. Centre-Ville, Montreal, QC, H3C 3P8, Canada

    I. Tanya Handa

  3. Department of Biology, McGill University, 1205 Avenue Docteur Penfield, Montreal, QC, H3A 1B1, Canada

    Martin J. Lechowicz

  4. Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, M5S 3B2, Canada

    Benjamin Gilbert

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  1. Robin Beauséjour
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  2. I. Tanya Handa
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  5. Mark Vellend
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Correspondence to Robin Beauséjour.

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Beauséjour, R., Handa, I.T., Lechowicz, M.J. et al. Historical anthropogenic disturbances influence patterns of non-native earthworm and plant invasions in a temperate primary forest. Biol Invasions 17, 1267–1281 (2015). https://doi.org/10.1007/s10530-014-0794-y

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