Skip to main content
SpringerLink
Log in
Book cover

From Biological Control to Invasion: the Ladybird Harmonia axyridis as a Model Species pp 5–21Cite as

Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid

  • Chapter

Abstract

Native to Asia, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) is considered an invasive alien ladybird in Europe and North America, where it was widely introduced as a biological control agent of aphids and coccids. In Europe, H. axyridis was sold by various biological control companies from 1995 in France, Belgium and the Netherlands, and was also intentionally released in at least nine other countries. It has spread very rapidly, particularly since 2002, and is now regarded as established in thirteen European countries. The established range extends from Denmark in the north to southern France in the south, and from Czech Republic in the east to Great Britain in the west. In this paper we map the spread and distribution of H. axyridis in Europe, and examine the situation on a country-by-country basis. We report first records of the species in five countries; Spain, Sweden, Denmark, Czech Republic and Italy; and first evidence of H. axyridis establishment in the latter three countries. Despite releases of H. axyridis in Portugal, Spain and Greece, there is little evidence of establishment in southern Europe. It is predicted that the spread and increase within Europe will continue and that H. axyridis will become one of the most widely distributed coccinellids in the continent.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Abbas I, Nakamura K, Katakura H, Sasaji H (1988) Geographical variation of elytral spot patterns in the phytophagous ladybird, Epilachna vigintioctopunctata (Coleoptera: Coccinellidae) in the province of Sumatra Barat, Indonesia. Res Population Ecol 30:43–56

    Article  Google Scholar 

  • Adriaens T, Branquart E, Maes D (2003) The multicoloured Asian ladybird Harmonia axyridis Pallas (Coleoptera: Coccinellidae), a threat for native aphid predators in Belgium? Belgian J Zool 133:195–196

    Google Scholar 

  • Adriaens T, San Martin y Gomez G, Maes D (2007) Invasion history, habitat preferences and phenology of the invasive ladybird Harmonia axyridis in Belgium. BioControl (this issue). doi:10.1007/s10526-007-9137-6

    Google Scholar 

  • Andermatt M (1996) Marienkäferlarven als blattlaus-bekämpfungsmittel? Andermatt Biocontrol 3:10–11

    Google Scholar 

  • Berkvens N, Bonte J, Berkvens D, Deforce K, Tirry L, De Clercq P (2007) Pollen as an alternative food for Harmonia axyridis. BioControl (this issue). doi:10.1007/s10526-007-9128-7

    Google Scholar 

  • Brown MW, Miller SS (1998) Coccinellidae (Coleoptera) in apple orchards of eastern West Virginia and the impact of invasion by Harmonia axyridis. Entomol News 109:143–151

    Google Scholar 

  • Brown PMJ, Roy HE, Rothery P, Roy DB, Ware RL, Majerus MEN (2007) Harmonia axyridis in Great Britain: analysis of the spread and distribution of a non-native coccinellid. BioControl (this issue). doi:10.1007/s10526-007-9124-y

    Google Scholar 

  • Chapin JB, Brou VA (1991) Harmonia axyridis (Pallas), the third species of the genus to be found in the United States (Coleoptera, Coccinellidae). Proc Entomol Soc Wash 93:630–635

    Google Scholar 

  • Colunga-Garcia M, Gage SH (1998) Arrival, establishment, and habitat use of the multicolored Asian lady beetle (Coleoptera: Coccinellidae) in a Michigan landscape. Environ Entomol 27:1574–1580

    Google Scholar 

  • Coutanceau J-P (2006) Harmonia axyridis (Pallas, 1773): une coccinelle asiatique introduite, acclimatée et en extension en France. Bull Soc Entomol France 111:395–401

    Google Scholar 

  • 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 

  • Cuppen J, Heijerman T, van Wielink P, Loomans A (2004) Het lieveheersbeestje Harmonia axyridis in Nederland: een aanwinst voor onze fauna of een ongewenste indringer (Coleoptera: Coccinellidae)? Nederlandse Faunistische Mededelingen 20:1–12

    Google Scholar 

  • Day WH, Prokrym DR, Ellis DR, Chianese RJ (1994) The known distribution of the predator Propylea quattuordecimpunctata (Coleoptera, Coccinellidae) in the United States, and thoughts on the origin of this species and 5 other exotic lady beetles in eastern North America. Entomol News 105:244–256

    Google Scholar 

  • de Almeida LM, da Silva VB (2002) First record of Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae): a lady beetle native to the Palaearctic region. Rev Bras Zool 19:941–944

    Google Scholar 

  • Dobzhansky T (1933) Geographical variation in ladybeetles. Am Nat 67:97–126

    Article  Google Scholar 

  • Eschen R, Babendreier D, Nauer S, Bigler F, Kenis M (2007) Surveys for ladybirds (Coleoptera: Coccinellidae) in Switzerland and confirmation of the presence of the invasive alien ladybird species Harmonia axyridis (Pallas). Mitteilungen der Schweizerischen Entomologischen Gesellschaft 80:7–14

    Google Scholar 

  • Ferran A, El-Arnaouty S, Beyssat-Arnaouty V, Galal H (2000) Introduction and release of the coccinellid Harmonia axyridis Pallas for controlling Aphis craccivora Koch on faba beans in Egypt. Egypt J Biol Pest Control 10:129–136

    Google Scholar 

  • Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, Oxford

    Google Scholar 

  • Gordon RD (1985) The Coleoptera (Coccinellidae) of America north of Mexico. J New York Entomol Soc 93:1–912

    Google Scholar 

  • Haldane JBS (1927) A mathematical theory of natural and artificial selection, part V: selection and mutation. Proc Cambridge Philosophical Soc 28:838–844

    Article  Google Scholar 

  • Hodek I (1973) Life history and biological properties. In: Hodek I (ed) Biology of Coccinellidae. Dr W Junk, The Hague

    Google Scholar 

  • Iperti G, Bertand E (2001) Hibernation of Harmonia axyridis (Coleoptera: Coccinellidae) in south-eastern France. Acta Soc Zool Bohem 65:207–210

    Google Scholar 

  • Jacas J-A, Urbaneja A, Viñuela E (2006) History and future of introduction of exotic arthropod biological control agents in Spain: a dilemma? BioControl 51:1–30

    Article  Google Scholar 

  • Kabiri F (2006) Harmonia axyridis: a problem or a distraction? In: Regulation of biological control agents (REBECA), Wageningen, Netherlands, 4–6 April 2006. http://www.rebeca-net.de/downloads/Risk%20assessment%20macrobials%20Kabiri.pdf

  • Katsoyannos P, Kontodimas DC, Stathas GJ, Tsartsalis CT (1997) Establishment of Harmonia axyridis on citrus and some data on its phenology in Greece. Phytoparasitica 25:183–191

    Google Scholar 

  • Klausnitzer B (2002) Harmonia axyridis (Pallas, 1773) in Deutschland (Col.,Coccinellidae). Entomologische Nachrichten und Berichte 46:177–183

    Google Scholar 

  • Klausnitzer B (2004) Harmonia axyridis (Pallas, 1773) in Basel-Stadt (Coleoptera, Coccinellidae). Entomologische Gesellschaft Basel 54:115–122

    Google Scholar 

  • Klausnitzer B, Klausnitzer H (1997) Marienkäfer (Coccinellidae). 4. überarbeitete auflage. Die Neue Brehm-Bücherei, Magdeburg

    Google Scholar 

  • Koch RL (2003) The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. J Ins Sci 3:1–16

    Article  Google Scholar 

  • Kontodimas DC, Stathas GJ, Martinou AF Status of the aphidophagous predator Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Greece. Eur J Entomol (in press)

    Google Scholar 

  • Koyama S, Majerus MEN (2007) Interactions between the parasitoid wasp Dinocampus coccinellae and two species of coccinellid from Japan and Britain. BioControl (this issue). doi:10.1007/s10526-007-9138-5

    Google Scholar 

  • Krafsur ES, Kring TJ, Miller JC, Nariboli P, Obrycki JJ, Ruberson JR, Schaefer PW (1997) Gene flow in the exotic colonizing ladybeetle Harmonia axyridis in North America. Biol Control 8:207–214

    Article  Google Scholar 

  • Kuznetsov VN (1997) Lady beetles of Russian far east. The Sandhill Crane Press, Gainesville, Florida

    Google Scholar 

  • Loomans A (2004) Veelkleurig Aziatisch lieveheersbeestje Harmonia axyridis bezig aan een opmars in Nederland. Coccinula 10:62–63

    Google Scholar 

  • Machado A (2005) El sarantontón asiático Harmonia axyridis (Pallas, 1773) presente en Canarias (Coleoptera: Coccinellidae). Vieraea 34:71–72

    Google Scholar 

  • Majerus MEN (1994) Ladybirds. No. 81, New Naturalist series. HarperCollins, London

    Google Scholar 

  • Majerus MEN (1998) Melanism: evolution in action. Oxford University Press, Oxford

    Google Scholar 

  • Majerus MEN (2003) Sex wars: genes, bacteria, and sex ratios. Princeton University Press, Princeton, New Jersey

    Google Scholar 

  • Majerus MEN, Mabbott P, Rowland F, Roy HE (2006) The harlequin ladybird, Harmonia axyridis, arrives in Britain. Entomol Mon Magaz 142:87–92

    Google Scholar 

  • Majerus MEN, Roy HE (2005) Scientific opportunities presented by the arrival of the harlequin ladybird, Harmonia axyridis, in Britain. Antenna 29:196–208

    Google Scholar 

  • McClure MS (1987) Potential of the Asian predator, Harmonia axyridis Pallas (Coleoptera, Coccinellidae), to control Matsucoccus resinosae Bean and Godwin (Homoptera, Margarodidae) in the United States. Environ Entomol 16:224–230

    Google Scholar 

  • Michaud JP (2002) Invasion of the Florida citrus ecosystem by Harmonia axyridis (Coleoptera: Coccinellidae) and asymmetric competition with a native species, Cycloneda sanguinea. Environ Entomol 31:827–835

    Article  Google Scholar 

  • Nalepa CA, Kidd KA, Ahlstrom KR (1996) Biology of Harmonia axyridis (Coleoptera: Coccinellidae) in winter aggregations. Ann Entomol Soc Am 89:681–685

    Google Scholar 

  • Pell JK, Baverstock J, Roy HE, Ware RL, Majerus MEN (2007) Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. BioControl (this issue). doi:10.1007/s10526-007-9125-x

    Google Scholar 

  • Rabitsch W, Schuh R (2006) First record of the multicoloured Asian ladybird Harmonia axyridis (Pallas, 1773) in Austria. Beiträge zur Entomofaunistik 7:161–164

    Google Scholar 

  • Roy HE, Baverstock J, Ware RL, Clark SJ, Majerus MEN, Baverstock KE, Pell JK Intraguild predation of the aphid pathogenic fungus Pandora neoaphidis by the invasive coccinellid Harmonia axyridis. Ecol Entomol (in press)

    Google Scholar 

  • Roy HE, Brown P, Majerus MEN (2006) Harmonia axyridis: a successful biocontrol agent or an invasive threat? In: Eilenberg J, Hokkanen H (eds) An ecological and societal approach to biological control. Springer, Dordrecht

    Google Scholar 

  • Roy HE, Brown PMJ, Rothery P, Ware RL, Majerus MEN (2007) Interactions between the fungal pathogen Beauveria bassiana and three species of coccinellid: Harmonia axyridis, Coccinella septempunctata and Adalia bipunctata. BioControl (this issue). doi:10.1007/s10526-007-9122-0

    Google Scholar 

  • Roy HE, Rowland F, Brown PMJ, Majerus MEN (2005) Ecology of the harlequin ladybird: a new invasive species. Br Wildl 16:403–407

    Google Scholar 

  • Schneider N, Loomans AJM (2006) Sur la présence au Luxembourg de la coccinelle arlequin Harmonia axyridis (Pallas, 1773) (Insecta, Coleoptera, Coccinellidae). Bulletin de la Société des Naturalistes Luxembourgeois 106:71–74

    Google Scholar 

  • Sidlyarevich VI, Voronin KE (1973) Trials on using Leis axyridis under glass. Zashchita Rastenii 6:24

    Google Scholar 

  • SIFA (Servicio de información fitosanitaria de Almería) (2004) Organismos de control biológico

    Google Scholar 

  • Soares AO, Borges I, Borges PAV, Labrie G, Lucas É (2007) Harmonia axyridis; What will stop the invader? BioControl (this issue). doi:10.1007/s10526-007-9141-x

  • Soares AO, Serpa A (2007) Interference competition between ladybird beetle adults (Coleoptera: Coccinellidae): effects on growth and reproductive capacity. Popul Ecol 49:37–43

    Article  Google Scholar 

  • Staverloekk A, Saethre MG, Haagvar E A review of the biology of the invasive harlequin ladybird Harmonia axyridis (Pallas, 1773) (Coleoptera, Coccinellidae). Norwegian J Entomol (in press)

    Google Scholar 

  • Tedders WL, Schaefer PW (1994) Release and establishment of Harmonia axyridis (Coleoptera, Coccinellidae) in the southeastern United States. Entomol News 105:228–243

    Google Scholar 

  • Tolasch T (2002) Harmonia axyridis (Pallas, 1773) breitet sich in Hamburg aus – ausgangspunkt für en besiedlung mitteleuropas? Entomologische Nachrichten und Berichte 46:185–188

    Google Scholar 

  • Trouvé C (1995) Essais de lutte biologique contre le puceron du houblon (Phorodon humuli) dans le nord de la France: résultats 1993 et 1994. In: 47th international symposium on crop protection, Ghent, 9 May 1995. Abstract book, p 109

    Google Scholar 

  • van Lenteren JC, Babendreier D, Bigler F, Burgio G, Hokkanen H, Kuske S, Loomans A, Menzler-Hokkanen I, van Rijn P, Thomas M, Tommassini M, Zeng Q-Q (2003) Environmental risk assessment of exotic natural enemies used in inundative biological control. BioControl 48:3–38

    Article  Google Scholar 

  • van Lenteren JC, Loomans AJM, Babendreier D, Bigler F (2007) Harmonia axyridis: an environmental risk assessment for Northwest Europe. BioControl (this issue). doi:10.1007/s10526-007-9120-2

    Google Scholar 

  • Ware RL, Evans N, O’Farrell K, Majerus MEN, Malpas L, Michie LJ Intraguild predation by the invasive ladybird Harmonia axyridis: 1: British and Japanese coccinellid eggs. Neobiota (in press)

    Google Scholar 

  • Ware RL, Majerus MEN (2007) Intraguild predation of immature stages of British and Japanese coccinellids by the invasive ladybird Harmonia axyridis. BioControl (this issue). doi:10.1007/s10526-007-9135-8

    Google Scholar 

  • Ware RL, Majerus MEN, Roy HE, Symington F (2005) The harlequin ladybird arrives in Britain: a threat to our native species? Bull Amateur Entomol Soc 64:175–186

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. NERC Centre for Ecology and Hydrology – Monks Wood, Huntingdon, PE28 2LS, UK

    P. M. J. Brown, H. E. Roy & D. B. Roy

  2. Department of Life Sciences, Anglia Ruskin University, East Road, Cambridge, CB1 1PT, UK

    P. M. J. Brown & H. E. Roy

  3. Instituut voor Natuur- en Bosonderzoek, Kliniekstraat 25, 1070, Brussel, Belgium

    T. Adriaens

  4. Federal Biological Research Centre for Agriculture and Forestry, Institute for Biological Control, Heinrichstr. 243, 64287, Darmstadt, Germany

    H. Bathon

  5. Wageningen University, P. O. Box 8080, 6700 DD, Wageningen, Netherlands

    J. Cuppen

  6. Neiker-Tecnalia, Instituto Vasco de Investigación y Desarrollo Agrario, Centro Arkaute, Apdo. 46, 01080, Vitoria-Gasteiz Alava, Pais Vasco, Spain

    A. Goldarazena

  7. Kristianstadgatan 15, 21423, Malmo, Sweden

    T. Hägg

  8. CABI Europe-Switzerland, 2800, Delemont, Switzerland

    M. Kenis

  9. Institut für Ökologie und Entomologie, Lannerstraße 5, 01219, Dresden, Germany

    B. E. M. Klausnitzer

  10. The Natural History Museum, Kunratice 1, 148 00, Praha 4, Czech Republic

    I. Kovář

  11. Department of Entomology, National Reference Laboratory, Plant Protection Service, P. O. Box 9102, 6700 HC, Wageningen, Netherlands

    A. J. M. Loomans

  12. Department of Genetics, University of Cambridge, Downing Street, Cambridge, CB2 3EH, UK

    M. E. N. Majerus

  13. Faculty of Science, University of South Bohemia, Branišovská 31, 370 05, Ceske Budejovice, Czech Republic

    O. Nedved

  14. Zoological Museum, University of Copenhagen, Universitetsparken 15, 2100, Kobenhavn, Denmark

    J. Pedersen

  15. Federal Environment Agency, Spittelauer Lände 5, 1090, Wien, Austria

    W. Rabitsch

  16. Observatoire permanent pour le suivi de la Coccinelle asiatique en France, CPIE du Pays de Soulaines, Domaine de Saint-Victor, 10200, Soulaines-Dhuys, France

    V. Ternois

  17. Vavilov Institute of General Genetics RAS, Moscow, 119991, Russia

    I. A. Zakharov

Authors
  1. P. M. J. Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. Adriaens
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. Bathon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Cuppen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. Goldarazena
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. T. Hägg
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. Kenis
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. B. E. M. Klausnitzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. I. Kovář
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. A. J. M. Loomans
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. M. E. N. Majerus
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. O. Nedved
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. J. Pedersen
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. W. Rabitsch
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. H. E. Roy
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. V. Ternois
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. I. A. Zakharov
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. D. B. Roy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. M. J. Brown .

Editor information

Editors and Affiliations

  1. Biological Records Centre, Huntingdon, UK

    Helen E. Roy

  2. I.N.R.A., Sophia Antipolis Cedex, France

    Eric Wajnberg

Rights and permissions

Reprints and permissions

Copyright information

© 2007 International Organization for Biological Control (IOBC)

About this chapter

Cite this chapter

Brown, P.M.J. et al. (2007). Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. In: Roy, H.E., Wajnberg, E. (eds) From Biological Control to Invasion: the Ladybird Harmonia axyridis as a Model Species. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6939-0_2

Download citation

Publish with us

Policies and ethics

Search

Navigation