Biological Invasions

, Volume 18, Issue 4, pp 907–920 | Cite as

Temporal and interspecific variation in rates of spread for insect species invading Europe during the last 200 years

  • Alain RoquesEmail author
  • Marie-Anne Auger-Rozenberg
  • Tim M. Blackburn
  • Jeff Garnas
  • Petr Pyšek
  • Wolfgang Rabitsch
  • David M. Richardson
  • Michael J. Wingfield
  • Andrew M. Liebhold
  • Richard P. Duncan
Insect Invasions


Globalization is triggering an increase in the establishment of alien insects in Europe, with several species having substantial ecological and economic impacts. We investigated long-term changes in rates of species spread following establishment. We used the total area of countries invaded by 1171 insect species for which the date of first record in Europe is known, to estimate their current range radius (calculated as [invaded area]0.5/π). We estimated initial rates of radial spread and compared them among different groups of insects for all years (1800–2014) and for a subset of more recent decades (1950–2014). Accidentally introduced species spread faster than intentionally introduced species. Considering the whole period 1800–2014, spread patterns also differ between feeding guilds, with decreasing spread rates over residence time in herbivores but not in detritivores or parasitic species. These decreases for herbivorous species appeared mainly in those associated with herbaceous plants and crops rather than woody plants. Initial spread rate was significantly greater for species detected after 1990, roughly 3–4 times higher than for species that arrived earlier. We hypothesize that the political changes in Europe following the collapse of the Iron Curtain in 1989, and the further dismantling of customs checkpoints within an enlarged European Union (EU) have facilitated the faster spread of alien insect species. Also, the number of species first recorded in the Eastern Bloc of the politically-divided Europe before 1989 was lower than for the rest of Europe. A detailed analysis of six recent invaders indicated a dominant role of long-distance translocations related to human activities, especially with the plant trade, in determining rates of spread.


Biological invasions Insects Introductions Spread Europe Cold War 



This paper had its origin at a workshop on “Drivers, impacts, mechanisms and adaptation in insect invasions” hosted and co-funded by the DST-NRF Centre of Excellence for Invasion in Stellenbosch, South Africa, in November 2014. Additional financial support was provided by HortGro, the National Research Foundation of South Africa, Stellenbosch University, and SubTrop. PP was supported by long-term research development project RVO 67985939 (The Czech Academy of Sciences) and by Praemium Academiae award from The Czech Academy of Sciences. DMR acknowledges support from the DST-NRF Centre of Excellence for Invasion Biology and the National Research Foundation, South Africa (Grant 85417). We thank Lionel Roques and Samuel Soubeyrand, INRA Avignon, France for fruitful discussions about the statistical methods to be used in order to better exploit the data. The European COST projects Alien Challenge (TD1209) and Global Warning (TD1401) are also acknowledged for their support as well as the regional project INCA funded the French Region Centre.

Supplementary material

10530_2016_1080_MOESM1_ESM.xlsx (99 kb)
Supplementary material S1. List of the 1171 alien insect species for which the date of first record in Europe was known, including taxonomic details (insect order), date of first record in Europe, total surface invaded in Europe by 2014, intentionnality of the introduction (I: Intentionnal; U:Unintentionnal), feeding regime (DET: Detrivorous species; PAR: Parasites and Predators; PHY: Phytophagous species), and type of host plants for phytophagous species (W: woody plants and woody material; NW: herbaceaous plants and crops). (XLSX 99 kb)
10530_2016_1080_MOESM2_ESM.xlsx (100 kb)
Supplementary material S2. List of the 455 alien insect species first recorded in Europe following 1950, and for which the date of first record in every invaded country is known. (XLSX 99 kb)


  1. Aikio S, Duncan RP, Hulme PE (2010) Lag-phases in alien plant invasions: separating the facts from the artefacts. Oikos 119:370–378CrossRefGoogle Scholar
  2. Avtzis DN, Matošević D (2013) Taking Europe by storm: a first insight in the introduction and expansion of Dryocosmus kuriphilus in central Europe by mtDNA. Šumarski list 7–8:387–394Google Scholar
  3. Bella S (2013) The box tree moth Cydalima perspectalis (Walker, 1859) continues to spread in southern Europe: new records for Italy (Lepidoptera Pyraloidea Crambidae). Redia 96:51–55Google Scholar
  4. Bella S, Rapisarda C (2013) First record from Greece of the invasive red gum lerp psyllid Glycaspis brimblecombei Moore (Hemiptera Psyllidae) and its associated parasitoid Psyllaephagus bliteus Riek (Hymenoptera Encyrtidae). Redia 96:33–35Google Scholar
  5. Blackburn TM, Pyšek P, Bacher S, Carlton JT, Duncan RP, Jarošík V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339CrossRefPubMedGoogle Scholar
  6. Blank SM, Hara H, Mikulás J, Csóka G, Ciornei C, Constantineanu R, Constantineau C, Roller L, Altenhofer E, Huflejt T, Vétek G (2010) Aproceros leucopoda (Hymenoptera: Argidae): an East Asian pest of elms (Ulmus spp.) invading Europe. Eur J Entomol 107:357–367CrossRefGoogle Scholar
  7. Brown PMJ, Thomas CE, Lombaert E, Jeffries DL, Estoup A, Lawson Handley LJ (2011) The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. Biocontrol 56:623–641CrossRefGoogle Scholar
  8. Chiron F, Shirley SM, Kark S (2010) Behind the curtain: socio-economic and political factors shaped exotic bird introductions into Europe. Biol Conserv 143:351–356CrossRefGoogle Scholar
  9. Chytrý M, Pyšek P, Wild J, Pino J, Maskell LC, Vilà M (2009) European map of alien plant invasions, based on the quantitative assessment across habitats. Divers Distrib 15:98–107CrossRefGoogle Scholar
  10. Cini A, Ioriatti C, Anfora G (2012) A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management. Bull Insectol 65:149–160Google Scholar
  11. Costello C, Springborn M, McAusland C, Solow A (2007) Unintended biological invasions: Does risk vary by trading partner? J Env Econom Manag 54:262–276CrossRefGoogle Scholar
  12. DAISIE (2009) Handbook of alien species in Europe. Springer, BerlinGoogle Scholar
  13. Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G, Arpaia S, Narváez-Vasquez CA, González-Cabrera J, Catalán Ruescas D, Tabone E, Frandon J, Pizzol J, Poncet C, Cabello T, Urbaneja A (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83:197–215CrossRefGoogle Scholar
  14. Eschen R, Holmes T, Smith D, Roques A, Santini A, Kenis M (2014) Likelihood of establishment of tree pests and diseases based on their worldwide occurrence as determined by hierarchical cluster analysis. For Ecol Manag 315:103–111CrossRefGoogle Scholar
  15. Essl F, Dullinger S, Rabitsch W, Hulme PE, Hülber K, Jarošík V, Kleinbauer I, Krausmann F, Kühn I, Nentwig W, Vilà M, Genovesi P, Gherardi F, Desprez-Loustau ML, Roques A, Pyšek P (2011) Socioeconomic legacy yields an invasion debt. PNAS 108:203–207CrossRefPubMedPubMedCentralGoogle Scholar
  16. Essl F, Bacher S, Blackburn TM et al (2015) Crossing frontiers in tackling pathways of biological invasions. Bioscience 65:769–782CrossRefGoogle Scholar
  17. Garnas J, Auger-Rozenberg M-A, Roques A, Bertelsmeier C, Wingfield M, Saccaggi DL, Roy H, Slippers B (2016) Complex patterns of global spread in invasive insects: eco-evolutionary and management consequences Biol Invasions. doi: 10.1007/s10530-016-1082-9
  18. Gilbert M, Liebhold AM (2010) Comparing methods for measuring the rate of spread of invading populations. Ecography 33:809–817CrossRefGoogle Scholar
  19. Hajek AE, Hurley BP, Kenis M, Garnas JR, Bush SJ, Wingfield MJ, van Lenteren JC, Cock MJW (2016) Exotic biological control agents: a solution or contribution to arthropod invasions. Biol Invasions. doi: 10.1007/s10530-016-1075-8 Google Scholar
  20. Hastings A, Cuddington K, Davies KF, Dugaw CJ, Elmendorf S, Freestone A et al (2005) The spatial spread of invasions: new developments in theory and evidence. Ecol Lett 8:91–101CrossRefGoogle Scholar
  21. Hui C, Krug RM, Richardson DM (2011) Modelling spread in invasion ecology: a synthesis. In: Richardson DM (ed) Fifty years of invasion ecology. The legacy of Charles Elton. Wiley-Blackwell, Oxford, pp 329–343Google Scholar
  22. Hurley BP, Garnas J, Wingfield MJ, Branco M, Richardson DM, Slippers B (2016) Increasing numbers and intercontinental spread of invasive insects on eucalypts. Biol Invasions. doi: 10.1007/s10530-016-1081-x Google Scholar
  23. Karpun NN, Ignatova YA (2013) The first report about Cydalima perspectalis Walker on the Black Sea coast of Russia.
  24. Katsanevakis S, Deriu I, D’Amico F, Nunes AL, Sanchez SP, Crocetta F, Arianoutsou M, Bazos I, Christopoulou A, Curto G, Delipetrou P, Kokkoris Y, Panov V, Rabitsch W, Roques A, Scalera R, Shirley SM, Tricarino E, Vannini A, Zenetos A, Zervou S, Zikos A, Cardoso AC (2015) European Alien Species Information Network (EASIN): supporting European policies and scientific research. Manag Biol Invasions 6:147–157CrossRefGoogle Scholar
  25. Kowarik I (1995) Time lags in biological invasions with regard to the success and failure of alien species. In: Pyšek P, Prach K, Rejmánek M, Wade M (eds) Plant invasions: general aspects and special problems. SPB Academic Publishers, AmsterdamGoogle Scholar
  26. Kumschick S, Devenish A, Kenis M, Rabitsch W, Richardson DM, Wilson JRU (2016) Intentionally introduced terrestrial invertebrates: patterns, risks, and options for management. Biol Invasions. doi: 10.1007/s10530-016-1086-5 Google Scholar
  27. Lambdon PW, Pyšek P, Basnou C, Hejda M, Arianoutsou M, Essl F, Jarošík V, Pergl J, Winter M, Anastasiu P, Andriopoulos P, Bazos I, Brundu G, Celesti-Grapow L, Chassot P, Delipetrou P, Josefsson M, Kark S, Klotz S, Kokkoris Y, Kühn I, Marchante H, Perglová I, Pino J, Vilà M, Zikos A, Roy D, Hulme PE (2008) Alien flora of Europe: species diversity, temporal trends, geographical patterns and research needs. Preslia 80:101–149Google Scholar
  28. Lesieur V (2014) Invasion de la punaise américaine Leptoglossus occidentalis en Europe: une contribution à la compréhension des invasions fulgurantes. PhD Thesis, Orléans UniversityGoogle Scholar
  29. Liebhold A, Brockerhoff E, Garrett L, Parke J, Britton K (2012) Live plant imports: the major pathway for the forest insect and pathogen invasions of the US. Front Ecol Environ 10:135–143CrossRefGoogle Scholar
  30. Liebhold AM, McCullough DG, Blackburn LM, Frankel SJ, Von Holle B, Aukema JE (2013) A highly aggregated geographical distribution of forest pest invasions in the USA. Divers Distrib 19:1208–1216CrossRefGoogle Scholar
  31. Lockwood JL, Hoopes MF, Marchetti MP (2013) Invasion ecology, 2nd edn. Wiley, OxfordGoogle Scholar
  32. Lopez-Vaamonde C, Agassiz D, Augustin S, De Prins J, De Prins W, Gomboc S et al (2010) Lepidoptera. BioRisk 4:603–668CrossRefGoogle Scholar
  33. Mally R, Nuss M (2010) Phylogeny and nomenclature of the box tree moth, Cydalima perpectalis (Walker, 1859) comb. n., which was recently introduced into Europe (Lepidoptera: Pyraloidea: Crambidae: Spilomelinae). Eur J Entomol 107:393–400CrossRefGoogle Scholar
  34. Mifsud D, Cocquempot C, Mühlethaler R, Wilson M, Streito JC (2010) Other Hemiptera Sternorrhyncha (Aleyrodidae, Phylloxeroidea, and Psylloidea) and Hemiptera Auchenorrhyncha. BioRisk 4:511–552CrossRefGoogle Scholar
  35. Paini DR, Worner SP, Cook DC, De Barro PJ, Thomas MB (2010) Threat of invasive pests from within national borders. Nat Commun 1:115CrossRefPubMedGoogle Scholar
  36. Plummer M (2003) JAGS: a program for analysis of Bayesian graphical models using Gibbs sampling. In: Proceedings of the 3rd international workshop on distributed statistical computing, Vienna, AustriaGoogle Scholar
  37. Pyšek P, Jarošík V (2005) Residence time determines the distribution of alien plants. In: Inderjit (ed) Invasive plants: ecological and agricultural aspects. Birkhäuser Verlag-AG, Basel, pp 77–96Google Scholar
  38. Pyšek P, Prach K (1993) Plant invasions and the role of riparian habitats—a comparison of four species alien to central Europe. J Biogeogr 20:413–420CrossRefGoogle Scholar
  39. Pyšek P, Jarošík V, Pergl J (2011) Alien plants introduced by different pathways differ in invasion success: unintentional introductions as greater threat to natural areas? PLoS ONE 6:e24890CrossRefPubMedPubMedCentralGoogle Scholar
  40. Pyšek P, Manceur AM, Alba C, McGregor K, Pergl J, Štajerová K, Chytrý M, Danihelka J, Kartesz J, Klimešová J, Lučanová M, Moravcová L, Nishino M, Sádlo J, Suda J, Tichý L, Kühn I (2015) Naturalization of central European plants in North America: species traits, habitats, propagule pressure, residence time. Ecology 96:762–774CrossRefPubMedGoogle Scholar
  41. Rabitsch W (2010) Pathways and vectors of alien arthropods in Europe. BioRisk 4:27–43CrossRefGoogle Scholar
  42. Rejmánek M (2000) Invasive plants: approaches and predictions. Aust Ecol 25:497–506CrossRefGoogle Scholar
  43. Richardson DM, Rejmánek M (2011) Trees and shrubs as invasive alien species—a global review. Divers Distrib 17:788–809CrossRefGoogle Scholar
  44. Roques A (2010) Taxonomy, time and geographic patterns. BioRisk 4:11–26CrossRefGoogle Scholar
  45. Sauvard D, Branco M, Lakatos F, Faccoli M, Kirkendall LR (2010) Weevils and bark beetles (Coleoptera, Curculionoidea). BioRisk 4:219–266CrossRefGoogle Scholar
  46. Sharov AA, Pijanowski BC, Liebhold AM, Gage SH (1999) What affects the rate of gypsy moth (Lepidoptera: Lymantriidae) spread: Winter temperature or forest susceptibility? Agric For Entomol 1:37–45CrossRefGoogle Scholar
  47. Shigesada N, Kawasaki K (1997) Biological invasions: theory and practice. Oxford University Press, OxfordGoogle Scholar
  48. Skalski GT, Gilliam JF (2000) Modeling diffusive spread in a heterogeneous population: a movement study with stream fish. Ecology 81:1685–1700CrossRefGoogle Scholar
  49. Skuhravá M, Skuhravý V (2009) Species richness of gall midges (Diptera: Cecidomyiidae) in Europe (West Palaearctic): biogeography and coevolution with host plants. Acta Soc Zool Bohem 73:87–156Google Scholar
  50. Skuhravá M, Skuhravý V, Csóka G (2007) The invasive spread of the gall midge Obolodiplosis robiniae in Europe. Cecidology 22:84–90Google Scholar
  51. Solow AR, Costello CJ (2004) Estimating the rate of species introductions from the discovery record. Ecology 85:1822–1825CrossRefGoogle Scholar
  52. Tobin PC, Liebhold AM, Roberts EA, Blackburn LM (2015) Estimating spread rates of non-native species: the gypsy moth as a case study. In: Venette RC (ed) Pest risk modelling and mapping for invasive alien species. CABI International and USDA, Wallingford, pp 131–145Google Scholar
  53. Van der Straten MJ, Muus TST (2010) The box tree pyralid, Glyphodes perspectalis (Lepidoptera: Crambidae), an invasive alien moth ruining box trees. Proc Neth Entomol Soc Meet 21:107–111Google Scholar
  54. Wermelinger B, Skuhravá M (2007) First records of the gall midge Obolodiplosis robiniae (Haldeman) (Diptera: Cecidomyiidae) and its associated parasitoid Platygaster robiniae Buhl & Duso (Hymenoptera: Platygastridae) in Switzerland. Mitt Schweiz Entomol Ges 80:217–221Google Scholar
  55. Williamson M, Pyšek P, Jarošík V, Prach K (2005) On the rates and patterns of spread of alien plants in the Czech Republic, Britain, and Ireland. EcoScience 12:424–433CrossRefGoogle Scholar
  56. Wilson JRU, Richardson DM, Rouget M, Procheş Ş, Amis MA, Henderson L, Thuiller W (2007) Residence time and potential range: crucial considerations in modelling plant invasions. Divers Distrib 13:11–22CrossRefGoogle Scholar
  57. Wingfield MJ, Brockerhoff E, Wingfield BD, Slippers B (2015) Planted forest health: the need for a global strategy. Science 394:832–836CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Alain Roques
    • 1
    Email author
  • Marie-Anne Auger-Rozenberg
    • 1
  • Tim M. Blackburn
    • 2
  • Jeff Garnas
    • 3
    • 4
  • Petr Pyšek
    • 5
    • 6
  • Wolfgang Rabitsch
    • 7
  • David M. Richardson
    • 8
  • Michael J. Wingfield
    • 4
  • Andrew M. Liebhold
    • 9
  • Richard P. Duncan
    • 10
  1. 1.INRA, UR 0633, Zoologie ForestièreOrléansFrance
  2. 2.Department of Genetics, Evolution and Environment, Centre for Biodiversity and Environment ResearchUniversity College LondonLondonUK
  3. 3.Department of Zoology and EntomologyUniversity of PretoriaPretoriaSouth Africa
  4. 4.Forestry and Agricultural Biotechnology Institute (FABI)University of PretoriaPretoriaSouth Africa
  5. 5.Institute of BotanyThe Czech Academy of SciencesPrůhoniceCzech Republic
  6. 6.Department of Ecology, Faculty of ScienceCharles University in PraguePrague 2Czech Republic
  7. 7.Environment Agency AustriaViennaAustria
  8. 8.Department of Botany and Zoology, Centre for Invasion BiologyStellenbosch UniversityMatielandSouth Africa
  9. 9.US Forest Service Northern Research StationMorgantownUSA
  10. 10.Institute for Applied EcologyUniversity of CanberraCanberraAustralia

Personalised recommendations