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Biological Invasions

, Volume 17, Issue 6, pp 1817–1832 | Cite as

How invasion by Ailanthus altissima transforms soil and litter communities in a temperate forest ecosystem

  • Eric Motard
  • Sophie Dusz
  • Benoît Geslin
  • Marthe Akpa-Vinceslas
  • Cécile Hignard
  • Olivier Babiar
  • Danielle Clair-Maczulajtys
  • Alice Michel-Salzat
Original Paper

Abstract

The invasive tree Ailanthus altissima (Mill.) Swingle (tree of heaven) is considered as an ecosystem transformer, which alters plant communities in open areas and forests. Nothing is yet known about its potential effects on forest soil biota and ecosystem functioning. We present here the first study assessesing the impact of A. altissima on soil and litter invertebrate communities in a temperate forest. We analyzed the effect of varying A. altissima densities in a forest of north-eastern France on soil microbial activity, diversity of various litter and soil invertebrate groups (Arthropoda, Lumbricidae, Gastropoda), diversity of functional groups (predatory, detritivorous, coprophagous, phytophagous), and trophic structure. Our study shows that increasing density of A. altissima is associated to lower soil microbial activity, decreasing abundance of litter detritivores (Acari and Collembola) and aboveground predatory Coleoptera, and decreasing species richness of terrestrial Gastropoda. In contrast, increased A. altissima density corresponded with greater abundances of litter Lumbricidae and aboveground coprophagous Coleoptera. We found an overall impact of A. altissima invasion on the soil food web structure that could accelerate the mineralization of organic matter and potentially favor nitrophilous plant species in understory plant communities.

Keywords

Diversity Litter invertebrates Microbial activity Plant invasion Trophic structure 

Notes

Acknowledgments

We are grateful to Dr. Jean-François Ponge, “Muséum national d’Histoire Naturelle”, France, for his critical comments and suggestions in improving this manuscript. Our special thanks to Claude Lagarde, Office National des Forêts of Fontainebleau and Christian Desmier, “Conseil Général de la Seine et Marne”, who provided logistics, all the authorizations we needed for our sampling and prior GPS mapping of our study area. We especially thank Pr. Cécile Butor, Dr. Elisabeth Petit-Koskas, Dr. Patrick Laurenti, Dr. Romain Nattier and the two anonymous reviewers for their useful comments on the manuscript. We thank Audrey Muratet and Gabrielle Martin, MNHN for their assistance in statistical analyses, Steve Hubert, Laboratoire de Physiologie de l’Arbre, Université Paris Diderot for his assistance in identifying the invertebrates, Olivier Gargomini, MNHN for his assistance in identifying terrestrial Gastropoda, Odile Loison, for entrusting us with her team and having provided the facilities of “Station d’Écologie Forestière de Fontainebleau”.

References

  1. Ayre K (2001) Effect of predator size and temperature on the predation of Deroceras reticulatum (Muller) (Mollusca) by carabid beetles. J Appl Entomol 125(7):389–395CrossRefGoogle Scholar
  2. Babel U (1977) Influence of high densities of fine roots of Norway spruce on processes in humus covers. Ecol Bull 25:584–586Google Scholar
  3. Baguette M (1992) Sélection de l’habitat des Carabidae en milieu forestier. Ph.D. Thesis, Université catholique de Louvain, BelgiumGoogle Scholar
  4. Boch S, Berlinger M, Fischer M, Knop E, Nentwig W, Türke M, and Prati D. (2012) Fern and bryophyte endozoochory by slugs. Oecologia 172:817–822Google Scholar
  5. Bory G (1983) Quelques aspects de la biologie de l’Ailanthus altissima (Mill.) Swingle: Mouvements de métabolites, croissance, développement, sécrétion et floraison chez divers types d’arbres. Ph.D. Thesis, Université Paris 7, FranceGoogle Scholar
  6. Bouché MB (1969) Comparaison critique de méthodes d’évaluation des populations de Lombricidés. Pedobiologia 9:26–34Google Scholar
  7. Butenschoen O, Scheu S, Eisenhauer N (2011) Interactive effects of warming, soil humidity and plant diversity on litter decomposition and microbial activity. Soil Biol Chem 43:1902–1907CrossRefGoogle Scholar
  8. Carlsson NOL, Sarnelle O, Strayer DL (2009) Native predators and exotic prey –an acquired taste? Front Ecol Environ 7(10):525–532CrossRefGoogle Scholar
  9. Castro-Díez P, González-Muñoz N, Alonso A, Gallardo A, Poorter L (2009) Effects of exotic invasive trees on nitrogen cycling: a case study in Central Spain. Biol Invasions 11(8):1973–1986CrossRefGoogle Scholar
  10. Chahartaghia M, Langelb R, Scheua S, Ruessa L (2005) Feeding guilds in Collembola based on nitrogen stable isotope ratios. Soil Biol Biochem 37:1718–1725CrossRefGoogle Scholar
  11. Clair-Maczulajtys D, Bory G (1983) Pedicellate extrafloral nectaries in Ailanthus glandulosa. Can J Bot 61:683–691CrossRefGoogle Scholar
  12. Cook RT, Bailey SER, McCrohan CR, Nash B, Woodhouse RM (2000) The influence of nutritional status on the feeding behaviour of the field slug, Deroceras reticulatum (Müller). Anim Behav 59(1):167–176CrossRefPubMedGoogle Scholar
  13. Davis MA, Chew MK, Hobbs RJ, Lugo AE, Ewel JJ, Vermeij GJ, Brown JH, Rosenzweig ML, Gardener MR, Carroll SP, Thompson K, Pickett STA, Stromberg JC, Tredici PD, Suding KN, Ehrenfeld JG, Grime JP, Mascaro J, Briggs JC (2011) Don’t judge species on their origins. Nature 474:153–154CrossRefPubMedGoogle Scholar
  14. de Jong YSDM (ed) (2013) Fauna Europaea version 2.6. Web Service available online at http://www.faunaeur.org
  15. Deleporte S (2001) Changes in the earthworm community of an acidophilous lowland beech forest during a stand rotation. Eur J Soil Biol 37:1–7CrossRefGoogle Scholar
  16. Dormann CF, King R (2004) Comparing the palatability of native and non-native Mediterranean plants. Ecol Mediterr 30:39–46Google Scholar
  17. Dormont L, Rapior S, McKey DB, Lumaret JP (2007) Influence of dung volatiles on the process of resource selection by coprophagous beetles. Chemoecology 17:23–30CrossRefGoogle Scholar
  18. Duchaufour P (1977) Pédogénèse et classification. Pédologie, vol 1. Masson, Paris, pp 51–70Google Scholar
  19. Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523CrossRefGoogle Scholar
  20. El Keblawy A, Al Rawai A (2007) Impacts of the invasive exotic Prosopis juliflora (Sw.) D.C. on the native flora and soils of the UAE. Plant Ecol 190(1):1573–5052Google Scholar
  21. Falkner G, Obrdlík P, Castella E, Speight MCD (2001) Shelled gastropoda of western Europe. Friedrich-Held-Gesellschaft, MünchenGoogle Scholar
  22. Ferry C (1986) Étude éco-éthologique des relations trophiques entre le coléoptère carabique Abax ater Villers et quelques crustacés isopodes Thèse de Doctorat, Université Paris VI, FranceGoogle Scholar
  23. Finzi AC, Van Breemen N, Canham CD (1998) Canopy tree–soil interactions within temperate forests: species effects on soil carbon and nitrogen. Ecol Appl 8(2):440–446Google Scholar
  24. Gallardo A, Merino J (1992) Nitrogen immobilization in leaf litter at two Mediterranean ecosystems of SW Spain. Biogeochemistry 15(3):213–228CrossRefGoogle Scholar
  25. Garceau C, Coderre D (1991) Efficiency of an ethological method for earthworm exctraction from a recent plantation of deciduous trees. Pedobiologia 35:27–34Google Scholar
  26. Gerber E, Krebs C, Murrel C, Moretti MR, Schaffner U (2008) Exotic invasive knotweeds (Fallopia spp.) negatively affect native plant and invertebrate assemblages in European riparian habitats. Biol Conserv 141:646–654CrossRefGoogle Scholar
  27. Gillman GP (1979) A proposed method for the measurement of exchange properties of highly weathered soils. Soil Res 17(1):129–139CrossRefGoogle Scholar
  28. Gillman GP, Sumpter EA (1986) Modification to the compulsive exchange method for measuring exchange characteristics of soils. Soil Res 24(1):61–66CrossRefGoogle Scholar
  29. Global Invasive Species Database (2014) Ailanthus altissima. http://www.issg.org/database/species/ecology.asp?si=319&fr=1&sts=sss&lang=EN. Accessed 15 June 2014
  30. Gómez-Aparicio L, Canham CD (2008) Neighborhood models of the effects of invasive tree species on ecosystem processes. Ecol Monogr 78(1):69–86CrossRefGoogle Scholar
  31. Grayston SJ, Prescott CE (2005) Microbial communities in forest floors under four tree species in coastal British Columbia. Soil Biol Chem 37:1157–1167CrossRefGoogle Scholar
  32. Guillemain M, Loreau M, Daufresne T (1997) Relationships between the regional distribution of carabid beetles (Coleoptera, Carabidae) and the abundance of their potential prey. Acta Oecol 18(4):465–483CrossRefGoogle Scholar
  33. Heisey RM (1990a) Allelopathic and herbicidal effects of extracts from tree-of-heaven (Ailanthus altissima). Am J Bot 77:662–670CrossRefGoogle Scholar
  34. Heisey RM (1990b) Evidence for allelopathy by tree-of-heaven (Ailanthus altissima). J Chem Ecol 16:2039–2055CrossRefPubMedGoogle Scholar
  35. Heisey RM (1996) Identification of an allelopathic compound from Ailanthus altissima (Simaroubaceae) and characterization of its herbicidal activity. Am J Bot 83:192–200CrossRefGoogle Scholar
  36. Heisey RM (1997) Allelopathy and the secret life of Ailanthus altissima. Arnoldia 57(3):28–36Google Scholar
  37. Huo Q, Shao J, Lin Q (2012) Study on the antibacterial and bactericidal effects of Ailanthus altissima leaves extract. Asian J Chem 24(8):3545–3547Google Scholar
  38. Joshi BC, Pandey A, Chaurasia L, Pal M, Sharma RP, Khare A (2003) Antifungal activity of the stem bark of Ailanthus excelsa. Fitoterapia 74(7):689–691CrossRefPubMedGoogle Scholar
  39. Kleiner K, Smith G (2005) Effects of tree species on soil bacterial communities and positive feedback on Ailanthus altissima. ESA 2005 annual meeting, poster session 20Google Scholar
  40. Kourtev PS, Huang W, Ehrenfeld JG (1999) Differences in earthworm densities and nitrogen dynamics in soils under exotic and native plant species. Biol Invasions 1:237–245CrossRefGoogle Scholar
  41. Kowarik I (1983) Zur Einbürgerung und zum pflanzengeographischen Verhalten des Götterbaumes (Ailanthus altissima (Mill.) Swingle) im französischen Mittelmeergebiet (Bas-Languedoc). Phytocoenologia 11:389–405CrossRefGoogle Scholar
  42. Kowarik I, Säumel I (2007) Biological flora of central Europe: Ailanthus altissima (Mill.) Swingle. Perspect Plant Ecol Evol Syst 8:207–237CrossRefGoogle Scholar
  43. Lee DG, Chang YS, Park Y, Hahm K, Woo ER (2002) Antimicrobiologic effects of ocotillone isolated from stem bark of Ailanthus altissima. J Microbiol Biotechnol 12:854–857Google Scholar
  44. Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69(1):1–24CrossRefGoogle Scholar
  45. Lindsay EA, French K (2006) The impact of the weed Chrysanthemoides monilifera ssp. rotundata on coastal leaf litter invertebrates. Biol Invasions 8:177–192CrossRefGoogle Scholar
  46. Loreau M (1983a) Le régime alimentaire de Abax ater Vill. (Coleoptera, Carabidae). Acta Oecol 4:253–263Google Scholar
  47. Loreau M (1983b) Le régime alimentaire de huit carabides (Coleoptera) communs en milieu forestier. Acta Oecol 4:331–343Google Scholar
  48. Loreau M (1986) Niche differentiation and community organization in forest carabid beetles. Carabid beetles—their adaptations and dynamics. Gustav Fischer, Stuttgart, pp 465–487Google Scholar
  49. Lu JH, He YQ (2010) Fumigant toxicity of Ailanthus altissima Swingle, Atractylodes lancea (Thunb.) DC. and Elsholtzia stauntonii Benth extracts on three major stored-grain insects. Ind Crops Prod 32:681–683CrossRefGoogle Scholar
  50. Lu JH, Wu S (2010) Bioactivity of essential oil from Ailanthus altissima bark against 4 major stored-grain insects. Afr J Microbiol Res 4(3):154–157Google Scholar
  51. Matrai K, Szemethy L, Toth P, Katona K, Szekely J (2004) Resource use by deer in lowland non-native forests, Hungary. J Wildl Manage 68(4):879–888CrossRefGoogle Scholar
  52. McAvoy TJ, Snyder AL, Johnson N, Salom SM, Kok LT (2012) Road survey of the invasive tree-of-heaven (Ailanthus altissima) in Virginia. Invasive Plant Sci Manage 5(4):506–512CrossRefGoogle Scholar
  53. McDowall RM (2004) Shoot first, and then ask questions: a look at aquarium fish imports and invasiveness in New Zealand. NZ J Mar Freshwat Res 38(3):503–510CrossRefGoogle Scholar
  54. Motard E, Muratet A, Clair-Maczulajtys D, Machon N (2011) Does the invasive species Ailanthus altissima threaten floristic diversity of temperate peri-urban forests? C R Biol 334:872–879CrossRefPubMedGoogle Scholar
  55. Oksanen JF, Blanchet G, Kindt R, Legendre P, O’Hara RB, Simpson GL et al. (2013) Vegan: community ecology package. R package. http://CRAN.R-project.org/package=vegan
  56. Pascal M, Lorvelec O, Vigne JD (2006) Invasions biologiques et extinctions: 11 000 ans d’histoire des vertébrés en France. Belin, ParisGoogle Scholar
  57. Pascual-Villalobos MJ, Robledo A (1998) Screening for anti-insect activity in mediterranean plants. Ind Crops Prod 8:183–194CrossRefGoogle Scholar
  58. Pearce JL, Venier LA (2006) The use of ground beetles (Coleoptera: Carabidae) and spiders (Araneae) as bioindicators of sustainable forest management: a review. Ecol Ind 6(4):780–793CrossRefGoogle Scholar
  59. Pedersini C, Bergamin M, Aroulmoji V, Baldini S, Picchio R, Pesce PG, Ballarin L, Murano E (2011) Herbicide activity of extracts from Ailanthus altissima (Simaroubaceae). Nat Prod Commun 6(5):593PubMedGoogle Scholar
  60. Post RD, Beeby AN (1996) Activity of the microbial decomposer community in metal-contaminated roadside soils. J Appl Ecol 33:703–709CrossRefGoogle Scholar
  61. Prescott CE, Corbin JP, Parkinson D (1992) Immobilization and availability of N and P in the forest floors of fertilized Rocky Mountain coniferous forests. Plant Soil 143(1):1–10CrossRefGoogle Scholar
  62. Pritekel C, Whittemore-Olson A, Snow N, Moore JC (2006) Impacts from invasive plant species and their control on the plant community and belowground ecosystem at Rocky Mountain National Park, USA. Appl Soil Ecol 32:132–141CrossRefGoogle Scholar
  63. Radtke A, Ambrass S, Zerbe S, Tonon G, Fontana V, Ammer C (2013) Traditional coppice forest management drives the invasion of Ailanthus altissima and Robinia pseudoacacia into deciduous forests. For Ecol Manage 291:308–317CrossRefGoogle Scholar
  64. R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  65.  Reinhart KO, Greene E, Callaway RM (2005) Effects of Acer platanoides invasion on understory plant communities and tree regeneration in the northern Rocky Mountains. Ecography 28(5):573–582CrossRefGoogle Scholar
  66. Rejmánek M, Richardson DM (2013) Trees and shrubs as invasive alien species—2013 update of the global database. Divers Distrib 19:1093–1094CrossRefGoogle Scholar
  67. Richardson DM, Rejmánek M (2011) Trees and shrubs as invasive alien species—a global review. Divers Distrib 17:788–809CrossRefGoogle Scholar
  68. Salmon S, Frizzera L, Camaret S (2008) Linking forest dynamics to richness and assemblage of soil zoological groups and to soil mineralization processes. For Ecol Manage 256:1612–1623CrossRefGoogle Scholar
  69. Sarkar SK, Chang CK (1997) The Simes method for multiple hypothesis testing with positively dependent test statistics. J Am Stat Assoc 92:1601–1608CrossRefGoogle Scholar
  70. Schneider K, Maraun M (2005) Feeding preferences among dark pigmented fungal taxa (‘‘Dematiacea’’) indicate limited trophic niche differentiation of oribatid mites (Oribatida, Acari). Pedobiologia 49:61–67CrossRefGoogle Scholar
  71. Schneider K, Migge S, Norton RA, Scheu S, Langel R, Reineking A, Maraun M (2004) Trophic niche differentiation in soil microarthropods (Oribatida, Acari): evidence from stable isotope ratios (15N/14N). Soil Biol Biochem 36:1769–1774CrossRefGoogle Scholar
  72. Simberloff D (2000) No reserve is an island: marine reserves and non indigenous species. Bull Mar Sci 66(3):567–580Google Scholar
  73. Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson J, Courchamp F, Galil B, García-Berthou E, Pascal M, Pyšek P, Sousa R, Tabacchi E, Vila M (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28(1):58–66CrossRefPubMedGoogle Scholar
  74. Simes RJ (1986) An improved Bonferroni procedure for multiple tests of significance. Biometrika 73:751–754CrossRefGoogle Scholar
  75. Speiser B (2001) Food and feeding behaviour. In: Barker GM (ed) The biology of terrestrial molluscs. CABI, Wallingford, pp 259–288CrossRefGoogle Scholar
  76. Standish RJ (2004) Impact of an invasive clonal herb on epigaeic invertebrates in forest remnants in New Zealand. Biol Conserv 116:49–58CrossRefGoogle Scholar
  77. Sutherland WJ, Freckleton RP, Godfray HCJ, Beissinger SR, Benton T, Cameron DD, Carmel Y et al (2013) Identification of 100 fundamental ecological questions. J Ecol 101(1):58–67CrossRefGoogle Scholar
  78. Symondson WOC (2004) Coleoptera (Carabidae, Drilidae, Lampyridae and Staphylinidae) as predators of terrestrial gastropods. In: Barker GM (ed) Natural enemies of terrestrial molluscs. CAB International, Oxford, pp 37–84CrossRefGoogle Scholar
  79. Thiele HU (1977) Carabid beetles in their environment: a study on habitat selection by adaptations in physiology and behaviour. Springer, New-YorkCrossRefGoogle Scholar
  80. Török K, Botta-Dukát Z, Dancza I, Németh I, Kiss J, Mihály B, Magyar D (2003) Invasion gateways and corridors in the Carpathian Basin: biological invasions in Hungary. Biol Invasions 5:349–356CrossRefGoogle Scholar
  81. Tsao R, Romanchuk FE, Peterson CJ, Coats JR (2002) Plant growth regulatory effect and insecticidal activity of the extracts of the tree of heaven (Ailanthus altissima L.). BMC Ecol 2:1–6CrossRefPubMedCentralPubMedGoogle Scholar
  82. Udvardy L (1998) Spreading and coenological circumstances of the tree of heaven (Ailanthus altissima) in Hungary. Acta Bot Hung 41:299–314Google Scholar
  83. Vilà M, Tessier M, Suehs CM (2006) Local and regional assessments of the impacts of plant invaders on vegetation structure and soil properties of Mediterranean islands. J Biogeogr 33:853–861CrossRefGoogle Scholar
  84. Wardle DA, Nicholson KS, Rahman A (1995) Ecological effects of the invasive weed species Senecio jacobaea L. (ragwort) in a New Zealand pasture. Agric Ecosyst Environ 56:19–28CrossRefGoogle Scholar
  85. Wardle DA, Bardgett RD, Callaway RM, Van der Putten WH (2011) Terrestrial ecosystem responses to species gains and losses. Science 332(6035):1273–1277CrossRefPubMedGoogle Scholar
  86. Wu J, Joergensen RG, Pommerening B, Chaussod R, Brookes PC (1990) Measurement of soil microbial biomass C. by fumigation-extraction. An automated procedure. Soil Biol Biochem 22:167–169CrossRefGoogle Scholar
  87. Zhao CC, Shao JH, Li X, Xu J, Zhang P (2005) Antimicrobial constituents from fruits of Ailanthus altissima Swingle. Arch Pharmacal Res 28:1147–1151CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Eric Motard
    • 1
    • 2
  • Sophie Dusz
    • 2
    • 3
  • Benoît Geslin
    • 1
  • Marthe Akpa-Vinceslas
    • 4
  • Cécile Hignard
    • 2
    • 5
  • Olivier Babiar
    • 2
    • 5
  • Danielle Clair-Maczulajtys
    • 2
    • 3
  • Alice Michel-Salzat
    • 2
    • 6
  1. 1.UMR 7618Institute of Ecology and Environmental SciencesParisFrance
  2. 2.Université Paris DiderotSorbonne Paris CitéFrance
  3. 3.Laboratoire de Physiologie de l’ArbreUniversité Paris DiderotParis Cedex 13France
  4. 4.Laboratoire EA 1293 ECODIV, UFR Sciences et TechniquesUniversité de RouenMont Saint AignanFrance
  5. 5.Station d’Écologie ForestièreUniversité Paris DiderotFontainebleauFrance
  6. 6.Laboratoire Évolution, Génomes et Spéciation, UPR 9034CNRSGif-sur-YvetteFrance

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