HARMONIA AXYRIDIS: A SUCCESSFUL BIOCONTROL AGENT OR AN INVASIVE THREAT?

  • Helen Roy
  • Peter Brown
  • Michael Majerus

Abstract

The harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) is an aphidophagous coccinellid, native to central and eastern Asian (Kuznetsov, 1997). This predatory ladybird has been available in many countries for use as a biological control agent of pest insects including aphids and scale insects. Since 1916 H. axyridis has been repeatedly released as a classical biological control agent in the USA (Gordon, 1985). It established in the 1980s and has spread and increased in number dramatically so that it is now the dominant species of ladybird in many parts of North America (Hesler et al., 2001; Smith et al., 1996; Tedders and Schaefer, 1994). In mainland Europe it has been commercially available for both classical and inundative biological control strategies since 1982 (Iperti and Bertand, 2001) and has become established in France, Belgium, Holland, Germany, Luxemburg and Italy. It has also been released in South America and the Middle East. Harmonia axyridis has not been intentionally released in the UK, however given the proximity of the SE of Britain to the French, Belgium and Dutch coasts it was inevitable that it would arrive. In mid September 2004 a male was found in Essex (SE England).

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Agarwala, B.K. & Dixon, A.F.G. (1992). Laboratory study of cannibalism and interspecific predation in ladybirds. Ecology Entomology, 17: 303–9CrossRefGoogle Scholar
  2. Brown, M.W. & Miller, S.S. (1998). Coccinellidae (Coleoptera) in apple orchards of eastern West Virginia and the impact of invasion by Harmonia axyridis. Entomological News, 109(2): 143–151.Google Scholar
  3. Buntin, G.D. & Bouton, J.H. (1997). Aphid (Homoptera: Aphididae) management in alfalfa by spring grazing cattle. Journal of Entomological Science, 32: 332–342.Google Scholar
  4. Burgio, G., Santi, F. & Maini, S. (2002). On intra-guild predation and cannibalism in Harmonia axyridis (Pallas) and Adalia bipunctata L. (Coleoptera: Coccinellidae). Biological Control, 24: 110–116.CrossRefGoogle Scholar
  5. Chapin, J.B. & Brou, V.A. (1991). Harmonia axyridis (Pallas), the third species of the genus to be found in the United States (Coleoptera: Coccinellidae). Proceedings of the Entomological Society Washington, 93: 630–635.Google Scholar
  6. Coderre, D. (1988). The numerical response of predators to aphid availability in maize: Why coccinellids fail? In Ecology and Effectiveness of Aphidophaga, (Eds. Niemczyk, E. & Dixon, A.F.G.). pp. 219–223. SPB Academic Publishing: The Hague.Google Scholar
  7. Colunga-Garcia, M. & Gage, S. H. (1998). Arrival, establishment, and habitat use of the multicolored Asian lady beetle (Coleoptera: Coccinellidae) in a Michigan landscape. Environmental Entomology, 27: 15741580.Google Scholar
  8. Day, W.H., Prokrym, D.R., Ellis, D.R. & Chianese, R.J. (1994). The known distribution of the predator Propylea quatuordecimpunctata (Coleoptera: Coccinellidae) in the United States, and thoughts on the origin of this species and five other exotic lady beetles in eastern North America. Entomological News, 105: 224–256.Google Scholar
  9. De Bach, P. (1964). Biological control of insect pests and weeds. Chapman and Hall: LondonGoogle Scholar
  10. Dixon, A.F.G. (2000). Insect predator-prey dynamics: Ladybird beetles and biological control. Cambridge University Press: Cambridge and New YorkGoogle Scholar
  11. Dobzhansky, T. (1933). Geographical variation in lady-beetles. American Naturalist, 67, 97–126.CrossRefGoogle Scholar
  12. Ferry, N., Raemaekers, R.J.M., Majerus, M.E.N., Jouanin, L., Port, G., Gatehouse, J.A. & Gatehouse, A.M.R. (2003). Impact of oilseed rape expressing the insecticidal cysteine proteinase inhibitor oryzacystatin on the beneficial predator Harmonia axyridis (multicoloured Asian ladybeetle). Molecular Ecology, 12: 493–504.PubMedCrossRefGoogle Scholar
  13. Gordon, R.D. (1985). The Coccinellidae (Coleoptera) of America North of Mexico. Journal of the New York Entomological Society, 93: 1–912.Google Scholar
  14. Grill, C.P., Moore, A.J. & Brodie, E.D. (1997). The genetics of phenotypic plasticity in a colonizing population of the ladybird beetle Harmonia axyridis. Heredity, 78 (3): 261–269.CrossRefGoogle Scholar
  15. Hesler, L.S. Keickhefer, R.W. & Beck, D.A. (2001). First record of Harmonia axyridis (Coleoptera: Coccinellidae) in South Dakota and notes on its activity there and in Minnesota. Entomological News, 112: 264–270.Google Scholar
  16. Hironori, Y. & Katsuhiro, S. (1997). Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. Entomophaga, 42: 153–163.Google Scholar
  17. Hodek, I. (1973). Life history and biological properties. In: Biology of Coccinellidae, 70–76. The Hague, Holland: Dr. W. Junk N. V. Publishers.Google Scholar
  18. Hodek, I. (1996). Food Relationships. In Ecology of Coccinellidae, (Eds. Hodek, I. & Honek, A.). pp. 143–238. Kluwer Academic Publishers: Dordrecht.Google Scholar
  19. Horn, D.J. (1991). Potential impact of Coccinella septempunctata on endangered Lycaenidae (Lepidoptera) in Northwestern Ohio, USA. In Behaviour and Impact of Aphidophaga (eds Polgar, L., Chambers, R.J., Dixon, A.F.G. & Hodek, I.) SPB Academic Publishing: The Hague.Google Scholar
  20. Hosino, Y. (1933). On variation in the pattern of Harmonia axyridis. Zoological Magazine, 45, 255–67.Google Scholar
  21. Hosino, Y. (1936). Genetical study of the lady-bird beetle, Harmonia axyridis Pallas Rep. II. Japanese Journal of Genetics, 12, 307–20.Google Scholar
  22. Howarth, F.G. (1991). Environmental impacts of classical biological control. Annual Review of Entomology, 36: 485–509CrossRefGoogle Scholar
  23. Huelsman, M.F., Kovach, J., Jasinski, J., Young, C. & Eisley, B. (2002). Multicolored Asian lady beetle (Harmonia axyridis) as a nuisance pest in housholds in Ohio. In: Jones, S.C., Zhai, J. & Robinson, W.H. (Eds.) Proceedings of 4th International Conference on Urban Pests, 243–250.Google Scholar
  24. Iperti, G. & Bertand, E. (2001). Hibernation of Harmonia axyridis (Coleoptera: Coccinellidae) in South-Eastern France. Acta Societatis Zoologicae Bohemicae, 65: 207–210.Google Scholar
  25. Kidd, K.A., Nalepa, C.A., Day, E.R. & Waldvogel, M.G. (1995). Distribution of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in North Carolina and Virginia. Proceedings of the Entomological Society of Washington, 97: 729–731.Google Scholar
  26. Koch, R.L. (2003). The multicoloured Asian lady beetle, Harmonia axyridis: A review of its biology, uses in biological control and non-target impacts??? Journal of Insect Science, 3: 32.PubMedGoogle Scholar
  27. Koch, R.L., Hutchison, W.D., Venette, R.C. & Heimpel, G.E. (2003). Susceptibility of immature monarch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae: Danainae), to predation by Harmonia axyridis (Coleoptera: Coccinellidae). Biological Control, 28: 265–270.CrossRefGoogle Scholar
  28. Komai, T. (1956). Genetics of Ladybeetles. Advances in Genetics, 8,155–88.CrossRefGoogle Scholar
  29. Kuznetsov, V.N. (1997). Ladybeetles of Russian Far East. Gainesville, FL: Memoir Seis Editor, CSE.Google Scholar
  30. LaMana, M. L. & Miller, J. C. (1996). Field observation on Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Oregon. Biological Control, 6: 232237.CrossRefGoogle Scholar
  31. LaMana, M. L. & Miller, J. C. (1998). Temperature-dependent development in an Oregon population of Harmonia axyridis (Coleoptera: Coccinellidae). Environmental Entomology, 27: 10011005.Google Scholar
  32. LaRock, D.R. & Ellington, J.J. (1996). An integrated pest management approach, emphasizing biological control, for pecan aphids. Southwestern Entomologist, 21: 153–167.Google Scholar
  33. Lynch, L.D., Hokkanen, H.M.T., Babendreier, D., Bigler, F., Burgio, G., Gao, Z.H., Kuske, S., Loomans, A., Menzler-Hokkanen, I., Thomas, M.B., Tommasini, G., Waage, J.K., Lenteren, J.C.v. & Zeng, Q.Q. (2001). Insect biological control and non-target effects: a European perspective. In: Wajnberg, E., Scott, J.K., Quinby, P.C. (eds.). Evaluating Indirect Ecological Effects of Biological Control. pp. 99–125. CABI Publishing: Wallingford, Oxon, UK.Google Scholar
  34. Majerus, M.E.N. (1994). Ladybirds. No. 81, New Naturalist Series. HarperCollins: London.Google Scholar
  35. Majerus, M.E.N. & Roy, H.E. (in press a) Colour pattern variation in the founding population of the harlequin ladybird, Harmonia axyridis, in Britain. Entomologist's Record and Journal of Variation.Google Scholar
  36. Majerus, M.E.N. & Roy, H.E. (in press b) Scientific opportunities presented by the arrival of the harlequin ladybird, Harmonia axyridis, in Britain. Antenna.Google Scholar
  37. Majerus, M.E.N., Rowland, F., Mabbott, P. & Roy, H.E. (in press) The arrival of the harlequin ladybird, Harmonia axyridis, in Britain. Entomologist's Monthly Magazine.Google Scholar
  38. Michaud, J.P. (2000). Development and reduction of ladybeetles (Coleoptera: Coccinellidae) on citrus aphids Aphis spiraecola Ratch and Toxoptera citricida (Kircaldy) (Homoptera: Aphidae). Biological Control, 18: 287–297.CrossRefGoogle Scholar
  39. Michaud, J.P. & Grant, A.K. (2003). Sub-lethal effects of a copper sulfate fungicide on development and reproduction in three coccinellid species. Journal of Insect Science, 3: 1–6.Google Scholar
  40. Musser, F.R. & Shelton, A.M. (2003). Bt sweet corn and selective insecticides: impacts on pests and predators. Journal of Economic Entomology, 96: 71–80.PubMedCrossRefGoogle Scholar
  41. Nakata, T. (1995). Population fluctuations of aphids and their natural enemies on potato in Hokkaido. Japanese Journal of Applied Entomology and Zoology. 30: 129–138.Google Scholar
  42. Ratcliffe, S. (2002). National pest alert: Multicolored Asian lady beetle. USDA CSREES Regional Integrated Pest Management Program & Pest Mangement Centers.Google Scholar
  43. Rosenheim, J.A., Wilhoit, J.C. & Armer, C.A. (1994). Influence of intraguild predation among generalist predators on the suppression of an herbivore population. Oecologia, 96: 439–449.CrossRefGoogle Scholar
  44. Roy, H.E. & Pell, J.K. (2000). Interactions between entomopathogenic fungi and other natural enemies: implications for biological control. Biocontrol Science and Technology, 10, 737–752CrossRefGoogle Scholar
  45. Sato, S., Yasuda, H. & Evans, E.W. (2005). Dropping behaviour of larvae of aphidophagous ladybirds and its effect on incidence of intraguild predation: interactions between the intraguild prey, Adalia bipunctata (L.) and Coccinella septempunctata (L.), and the intraguild predator, Harmonia axyridis Pallas. Ecological Entomology, 30, 220–224CrossRefGoogle Scholar
  46. Smith, W.M., Arnold, D.C., Eikenbary, R.D., Rice, N.R., Shiferaw, A., Cheary, B.S. & Carroll, B.L. (1996). Influence of ground cover on beneficial arthropods in pecan. Biological Control, 6: 164–176.CrossRefGoogle Scholar
  47. Takahashi, K. (1989). Intra- and interspecific predations of lady beetles in spring alfalfa fields. Japanese Journal of Entomology, 57: 199–203.Google Scholar
  48. Tan, C.-C., & Li, J.-C. (1934). Inheritance of the elytral color patterns in the lady-bird beetle, Harmonia axyridis Pallas. American Naturalist, 68, 252–65.CrossRefGoogle Scholar
  49. Tedders, W.L. & Schaefer, P.W. (1994). Release and establishment of Harmonia axyridis (Coleoptera: Coccinellidae) in the south-eastern United States. Entomological News, 105: 228243.Google Scholar
  50. Van Lenteren, J.C., Babendreier, D., Bigler, F., Burgio, G., Hokkanen, H.M.T., Kuske, S., Loomans, A.J.M., Menzler-Hokkanen, I., Van Rijn, P.C.J., Thomas, M.B. and Zeng, Q.Q. (2003). Environmental risk assessment of exotic natural enemies used in inundative biological control. Biocontrol, 48, 3–38.CrossRefGoogle Scholar
  51. Wang, L.Y. (1986). Mass rearing and utilization in biological control of the lady beetle Leis axyridis (Pallas). Acta Entomologica Sinica, 29: 104.Google Scholar
  52. Wells, M.L. and McPherson, R.M. (1999). Population dynamics of three coccinellids in flue-cured tobacco and functional response of Hippodamia convergens (Coleoptera: Coccinellidae) feeding on tobacco aphids (Homoptera: Aphididae). Environmental Entomology, 28: 768–773.Google Scholar
  53. Wells, M.L., McPherson, R.M., Ruberson, J.R. & Herzog, G.A. (2001). Coccinellids in cotton: population response to pesticide application and feeding response to cotton aphids (Homoptera: Aphididae). Environmental Entomology, 30: 785–793.CrossRefGoogle Scholar
  54. Wold, S.J., Burkness, E.C., Hutchison, W.D. & Venette, R.C. (2001). In-field monitoring of beneficial insect populations in transgenic sweet corn expressing a Bacillus thuringiensis toxin. Journal of Entomological Science, 36: 177–187.Google Scholar
  55. Yakhontov, V.V. (1960). Utilisation of Coccinellids in the Control of Agricultural Pests. Izdanii—Akademiia Nauk Uzbekskoi SSR: Tashkent.Google Scholar
  56. Yarbrough, J.A., Armstrong, J.L., Blumberg, M.Z., Phillips, A.E., McGahee, E. & Dolen, W.K. (1999). Allergic rhinoconjunctivitis caused by Harmonia axyridis (Asian lady beetle, Japanese lady beetle, or lady bug). Journal of Allergy and Clinical Immunology, 104: 705.CrossRefGoogle Scholar
  57. Yasuda, H. & Ohnuma. N. (1999). Effect of cannibalism and predation on the larval performance of two ladybird beetles. Entomologia Experimentalis et Applicata, 93: 63–67.CrossRefGoogle Scholar
  58. Yasuda, H., Kikuchi, T., Kindlmann, P. & Sato, S. (2001). Relationships between attacks and escape rates, cannibalism, and intraguild predation in larvae of two predatory ladybirds. Journal of Insect Behavior, 14: 373–384.CrossRefGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Helen Roy
  • Peter Brown
  • Michael Majerus

There are no affiliations available

Personalised recommendations