Ten years of invasion: Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Britain

Ecological Entomology

Volumn 40, Issue 4, 2015, Pages 336-348

  Roy, Helen E ^a   Brown, Peter M J ^b  

^a CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

^b ANGLIA RUSKIN UNIVERSITY   (United Kingdom)

Author keywords

Biological invasions; Citizen science; Intra guild predation; Invasive species; Monitoring and surveillance; Non native species

Indexed keywords

APHID; BEETLE; BIOCONTROL AGENT; BIOLOGICAL INVASION; BIOMONITORING; DATA SET; DISPERSAL; DOMINANCE; FEEDING; FIELD SURVEY; HUMAN ACTIVITY; INTRAGUILD PREDATION; NATIVE SPECIES; NATURAL ENEMY; PHENOTYPIC PLASTICITY; POLYMORPHISM; POPULATION DECLINE; REPRODUCTIVE POTENTIAL; RESEARCH METHOD; SPATIAL DISTRIBUTION; TRACKING; WORLD WIDE WEB;

UNITED KINGDOM;

COCCINELLIDAE; COLEOPTERA; HARMONIA AXYRIDIS;

EID: 84935719462     PISSN: 03076946     EISSN: 13652311     Source Type: Journal    
DOI: 10.1111/een.12203     Document Type: Article

References (86)

1. Adachi-Hagimori, T., Shibao, M., Tanaka, H., Seko, T. & Miura, K. (2011) Control of Myzus persicae and Lipaphis erysimi (Hemiptera: Aphididae) by adults and larvae of a flightless strain of Harmonia axyridis (Coleoptera: Coccinellidae) on non-heading Brassica cultivars in the greenhouse. BioControl, 56, 207-213.
2. Berkvens, N., Bonte, J., Berkvens, D., Deforce, K., Tirry, L. & De Clercq, P. (2008) Pollen as an alternative food for Harmonia axyridis. From Biological Control to Invasion: The Ladybird Harmonia Axyridis as a Model Species, pp. 201-210. Springer-Verlag, Amsterdam, the Netherlands.
3. Berkvens, N., Landuyt, C., Deforce, K., Berkvens, D., Tirry, L. & De Clercq, P. (2010a) Alternative foods for the multicoloured Asian lady beetle Harmonia axyridis (Coleoptera: Coccinellidae). European Journal of Entomology, 107, 189-195.
4. Berkvens, N., Moensa, J., Berkvens, D., Samihc, M.A., Tirry, L. & De Clercq, P. (2010b) Dinocampus coccinellae as a parasitoid of the invasive ladybird Harmonia axyridis in Europe. Biological Control, 53, 92-99.
5. Bezzerides, A.L., McGraw, K.J., Parker, R.S. & Husseini, J. (2007) Elytra color as a signal of chemical defense in the Asian ladybird beetle Harmonia axyridis. Behavioral Ecology and Sociobiology, 61, 1401-1408.
6. Blackburn, T.M., Pyšek, P., Bacher, S., Carlton, J.T., Duncan, R.P., Jarošík, V. et al. (2011) A proposed unified framework for biological invasions. Trends in Ecology & Evolution, 26, 333-339.
7. Botezatu, A.I., Kotseridis, Y., Inglis, D. & Pickering, G.J. (2013) Occurrence and contribution of alkyl methoxypyrazines in wine tainted by Harmonia axyridis and Coccinella septempunctata. Journal of the Science of Food and Agriculture, 93, 803-810.
8. Brakefield, P.M. & De Jong, P.W. (2011) A steep cline in ladybird melanism has decayed over 25 years: a genetic response to climate change? Heredity, 107, 574-578.
9. Brown, P.M.J. (2010) The spread of the harlequin ladybird Harmonia axyridis (Coleoptera: Coccinellidae) in Europe and its effects on native ladybirds. PhD thesis, Anglia Ruskin University, Cambridge, U.K.
10. Brown, P.M.J., Adriaens, T., Bathon, H., Cuppen, J., Goldarazena, A., Hagg, T. et al. (2008a) Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. BioControl, 53, 5-21.
11. Brown, P.M.J., Roy, H.E., Rothery, P., Roy, D.B., Ware, R.L. & Majerus, M.E.N. (2008b) Harmonia axyridis in Great Britain: analysis of the spread and distribution of a non-native coccinellid. BioControl, 53, 55-67.
12. Brown, P.M.J., Frost, R., Doberski, J., Sparks, T., Harrington, R. & Roy, H.E. (2011a) Decline in native ladybirds in response to the arrival of Harmonia axyridis: early evidence from England. Ecological Entomology, 36, 231-240.
13. Brown, P.M.J., Thomas, C.E., Lombaert, E., Jeffries, D.L., Estoup, A. & Handley, L.-J.L. (2011b) The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. BioControl, 56, 623-641.
14. Brown, P.M.J., Ingels, B., Wheatley, A., Rhule, E.L., De Clercq, P., van Leeuwen, T. et al. (2014) Intraguild predation by Harmonia axyridis (Coleoptera: Coccinellidae) on native insects in Europe: molecular detection from field samples. Entomological Science, 18, 130-133.
15. Ceryngier, P., Roy, H.E. & Poland, R.L. (2012) Natural enemies of ladybird beetles, pp. 375-443. Wiley-Blackwell, Chichester, U.K.
16. Colautti, R.I., Ricciardi, A., Grigorovich, I.A. & Macisaac, H.J. (2004) Is invasion success explained by the enemy release hypothesis? Ecology Letters, 7, 721-733.
17. Comont, R.F., Roy, H.E., Lewis, O.T., Harrington, R., Shortall, C.R. & Purse, B.V. (2012) Using biological traits to explain ladybird distribution patterns. Journal of Biogeography, 39, 1772-1781.
18. Comont, R., Roy, H., Harrington, R., Shortall, C. & Purse, B. (2014a) Ecological correlates of local extinction and colonisation in the British ladybird beetles (Coleoptera: Coccinellidae). Biological Invasions, 16, 1805-1817.
19. Comont, R.F., Purse, B.V., Phillips, W., Kunin, W.E., Hanson, M., Lewis, O.T. et al. (2014b) Escape from parasitism by the invasive alien ladybird, Harmonia axyridis. Insect Conservation and Diversity, 7, 334-342.
20. Decourcy, G. (2009) Long term implications of the arrival in the British Isles of Harmonia axyridis, the harlequin ladybird.
21. Elliott, N., Kieckhefer, R. & Kauffman, W. (1996) Effects of an invading coccinellid on native coccinellids in an agricultural landscape. Oecologia, 105, 537-544.
22. Elton, C.S. (1958) The Ecology of Invasions by Animals and Plants. Methuen, London, U.K.
23. Firlej, I. (2012) Teratocytes growth pattern reflects host suitability in a host-parasitoid assemblage. Annals of the Entomological Society of America, 105, 328-338.
24. Flowers, R., Salom, S. & Kok, L. (2005) Competitive interactions among two specialist predators and a generalist predator of hemlock woolly adelgid, Adelges tsugae (Homoptera: Adelgidae), in the laboratory. Environmental Entomology, 34, 664-675.
25. Galvan, T.L., Koch, R.L. & Hutchison, W.D. (2008) Impact of fruit feeding on overwintering survival of the multicolored Asian lady beetle, and the ability of this insect and paper wasps to injure wine grape berries. Entomologia Experimentalis et Applicata, 128, 429-436.
26. Glemser, E.J., Dowling, L., Inglis, D., Pickering, G.J., McFadden-Smith, W., Sears, M.K. et al. (2012) A novel method for controlling multicolored Asian lady beetle (Coleoptera: Coccinellidae) in vineyards. Environmental Entomology, 41, 1169-1176.
27. Goetz, D.W. (2008) Harmonia axyridis ladybug invasion and allergy. Allergy and Asthma Proceedings, 123-129.
28. Hall, R., Ware, R. & Michie, L.J. (2009) First record of field parasitism of immature stages of the Harlequin Ladybird Harmonia axyridis (Pallas) (Col.: Coccinellidae) by the braconid wasp Dinocampus coccinellae (Shrank) (Hym.: Braconidae). Entomologist's Record and Journal of Variation, 121, 57-58.
29. Hautier, L., San Martin, G., Callier, P., De Biseau, J.-C. & Grégoire, J.-C. (2011) Alkaloids provide evidence of intraguild predation on native coccinellids by Harmonia axyridis in the field. Biological Invasions, 13, 1805-1814.
30. Hodek, I. & Evans, E.W. (2012) Food relationships. Ecology and Behaviour of the Ladybird Beetles (Coccinellidae) (ed. by I. Hodek, H. F. van Emden and A. Honek), pp. 141-274. Wiley-Blackwell, Chichester, U.K.
31. Holroyd, O., Brown, P.M.J., Roy, H.E. & Majerus, M.E.N. (2008) The harlequin ladybird, Harmonia axyridis, reaches Scotland. Entomologist's Record and Journal of Variation, 120, 42-43.
32. Hoogendoorn, A. & Heimpel, G. (2002) Indirect interactions between an introduced and a native ladybird beetle species mediated by a shared parasitoid. Biological Control, 25, 224-230.
33. Ingels, B. & De Clercq, P. (2011) Effect of size, extraguild prey and habitat complexity on intraguild interactions: a case study with the invasive ladybird Harmonia axyridis and the hoverfly Episyrphus balteatus. BioControl, 56, 871-882.
34. Jansen, J.P. & Hautier, L. (2008) Ladybird population dynamics in potato: comparison of native species with an invasive species, Harmonia axyridis. BioControl, 53, 223-233.
35. Jeffries, D.L., Chapman, J., Roy, H.E., Humphries, S., Harrington, R., Brown, P.M.J. et al. (2013) Characteristics and drivers of high-altitude ladybird flight: insights from vertical-looking entomological radar. PLoS ONE, 8, e82278.
36. Kenis, M., Roy, H.E., Zindel, R. & Majerus, M.E.N. (2008) Current and potential management strategies against Harmonia axyridis. BioControl, 53, 235-252.
37. Koch, R.L. (2003) The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. Journal of Insect Science, 3, 32.
38. Koch, R.L. & Galvan, T.L. (2008) Bad side of a good beetle: the North American experience with Harmonia axyridis. BioControl, 53, 23-35.
39. 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.
40. Koch, R., Burkness, E., Burkness, S.J.W. & Hutchison, W. (2004) Phytophagous preferences of the multicolored Asian lady beetle (Coleoptera: Coccinellidae) for autumn-ripening fruit. Journal of Economic Entomology, 97, 539-544.
41. Koyama, S. & Majerus, M.E.N. (2008) Interactions between the parasitoid wasp Dinocampus coccinellae and two species of coccinellid from Japan and Britain. BioControl, 53, 253-264.
42. Lombaert, E., Guillemaud, T., Cornuet, J.-M., Malausa, T., Facon, B. & Estoup, A. (2010) Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. PLoS ONE, 5, e9743.
43. Majerus, M., Strawson, V. & Roy, H. (2006) The potential impacts of the arrival of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in Britain. Ecological Entomology, 31, 207-215.
44. Michie, L.J., Mallard, F., Majerus, M.E.N. & Jiggins, F.M. (2010) Melanic through nature or nurture: genetic polymorphism and phenotypic plasticity in Harmonia axyridis. Journal of Evolutionary Biology, 23, 1699-1707.
45. Murchie, A.K., Moore, J.P., Moore, G.A. & Roy, H.E. (2008) The harlequin ladybird (Harmonia axyridis (Pallas)) (Coleoptera: Coccinellidae), found in Ireland. Irish Naturalists' Journal, 29, 25-26.
46. Nedvěd, O., Xenia, F., Ungerova, D. & Kalushkov, P. (2013) Alien vs. Predator-the native lacewing Chrysoperla carnea is the superior intraguild predator in trials against the invasive ladybird Harmonia axyridis. Bulletin of Insectology, 66, 73-78.
47. Onofre Soares, A., Coderre, D. & Schanderl, H. (2005) Influence of prey quality on the fitness of two phenotypes of Harmonia axyridis adults. Entomologia Experimentalis et Applicata, 114, 227-232.
48. Osawa, N. (2011) Ecology of Harmonia axyridis in natural habitats within its native range. BioControl, 56, 613-621.
49. Panigaj, L., Zach, P., Honěk, A., Nedvěd, O., Kulfan, J., Martinková, Z. et al. (2014) The invasion history, distribution and colour pattern forms of the harlequin ladybird beetle Harmonia axyridis (Pall.)(Coleoptera, Coccinellidae) in Slovakia, Central Europe. ZooKeys, 412, 89-102.
50. Pell, J.K., Baverstock, J., Roy, H.E., Ware, R.L. & Majerus, M.E.N. (2008) Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. BioControl, 53, 147-168.
51. Phoofolo, M.W. & Obrycki, J.J. (1998) Potential for intraguild predation and competition among predatory Coccinellidae and Chrysopidae. Entomologia Experimentalis et Applicata, 89, 47-55.
52. Poutsma, J., Loomans, A.J.M., Aukema, B. & Heijerman, T. (2008) Predicting the potential geographical distribution of the harlequin ladybird, Harmonia axyridis, using the CLIMEX model. BioControl, 53, 103-125.
53. Purse, B.V., Comont, R., Butler, A., Brown, P.M.J., Kessel, C. & Roy, H.E. (2014) Landscape and climate determine patterns of spread for all colour morphs of the alien ladybird Harmonia axyridis. Journal of Biogeography, 42, 575-588.
54. Rhule, E.L., Majerus, M.E., Jiggins, F.M. & Ware, R.L. (2010) Potential role of the sexually transmitted mite Coccipolipus hippodamiae in controlling populations of the invasive ladybird Harmonia axyridis. Biological Control, 53, 243-247.
55. Ribbands, B., Brown, P.M.J., Roy, H.E. & Majerus, M.E.N. (2009) The most northerly record of the Harlequin ladybird (Col., Coccinellidae) in the British Isles. Entomologist's Monthly Magazine, 145, 43-44.
56. Romanuk, T.N., Zhou, Y., Brose, U., Berlow, E.L., Williams, R.J. & Martinez, N.D. (2009) Predicting invasion success in complex ecological networks. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences, 364, 1743-1754.
57. Roy, H.E. & Cottrell, T.E. (2008) Forgotten natural enemies: interactions between coccinellids and insect-parasitic fungi. European Journal of Entomology, 105, 391-398.
58. Roy, H.E. & Lawson Handley, L.-J. (2012) Networking: a community approach to invaders and their parasites. Functional Ecology, 26, 1238-1248.
59. Roy, H.E. & Wajnberg, E. (2008) From biological control to invasion: the ladybird Harmonia axyridis as a model species. BioControl, 53, 1-4.
60. Roy, H.E., Baverstock, J., Ware, R.L., Clark, S.J., Majerus, M.E.N., Baverstock, K.E. et al. (2008a) Intraguild predation of the aphid pathogenic fungus Pandora neoaphidis by the invasive coccinellid Harmonia axyridis. Ecological Entomology, 33, 175-182.
61. Roy, H.E., Brown, P.M.J., Rothery, P., Ware, R.L. & Majerus, M.E.N. (2008b) Interactions between the fungal pathogen Beauveria bassiana and three species of coccinellid: Harmonia axyridis, Coccinella septempunctata and Adalia bipunctata. BioControl, 53, 265-276.
62. Roy, H.E., Brown, P.M.J., Frost, R. & Poland, R.L. (2011a) Atlas of the Ladybirds (Coccinellidae) of Britain and Ireland. Biological Records Centre, Wallingford, U.K.
63. Roy, H.E., Handley, L.J.L., Schoenrogge, K., Poland, R.L. & Purse, B.V. (2011b) Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids? BioControl, 56, 451-468.
64. Roy, H.E., Rhule, E., Harding, S., Handley, L.-J.L., Poland, R.L., Riddick, E.W. et al. (2011c) Living with the enemy: parasites and pathogens of the ladybird Harmonia axyridis. BioControl, 56, 663-679.
65. Roy, H.E., Adriaens, T., Isaac, N.J.B., Kenis, M., Onkelinx, T., San Martin, G. et al. (2012) Invasive alien predator causes rapid declines of native European ladybirds. Diversity and Distributions, 18, 717-725.
66. Roy, H.E., Brown, P.M.J., Comont, R.F., Poland, R.L., Sloggett, J.J., Majerus, M. et al. (2013) Naturalists' Handbook 10: Ladybirds. Pelagic Publishing, Exeter, U.K.
67. Roy, H.E., Peyton, J., Aldridge, D.C., Bantock, T., Blackburn, T.M., Britton, R. et al. (2014) Horizon scanning for invasive alien species with the potential to threaten biodiversity in Great Britain. Global Change Biology, 20, 3859-3871.
68. Saethre, M.G., Staverløkk, A. & Hofsvang, T. (2010) The history of Harmonia axyridis (Pallas 1773) in Norway. IOBC/WPRS Bulletin(Working Group "Benefits and Risks of exotic biological Control Agents"), 58, 97-104.
69. Sloggett, J.J. (2005) Are we studying too few taxa? Insights from aphidophagous ladybird beetles (Coleoptera: Coccinellidae). European Journal of Entomology, 102, 391-398.
70. Sloggett, J.J. (2012) Harmonia axyridis invasions: deducing evolutionary causes and consequences. Entomological Science, 15, 261-273.
71. Smith, C.A. & Gardiner, M.M. (2013) Biodiversity loss following the introduction of exotic competitors: does intraguild predation explain the decline of native lady beetles? PLoS ONE, 8, e84448.
72. Tedders, W.L. & Schaefer, P.W. (1994) Release and establishment of Harmonia axyridis (Coleoptera, Coccinellidae) in the southeastern United States. Entomological News, 105, 228-243.
73. Thomas, A.P., Trotman, J., Wheatley, A., Aebi, A., Zindel, R. & Brown, P.M.J. (2013) Predation of native coccinellids by the invasive alien Harmonia axyridis (Coleoptera: Coccinellidae): detection in Britain by PCR-based gut analysis. Insect Conservation and Diversity, 6, 20-27.
74. Torchin, M., Lafferty, K. & Kuris, A. (2001) Release from parasites as natural enemies: increased performance of a globally introduced marine crab. Biological Invasions, 3, 333-345.
75. Torchin, M.E., Lafferty, K.D., Dobson, A.P., McKenzie, V.J. & Kuris, A.M. (2003) Introduced species and their missing parasites. Nature, 421, 628-630.
76. Vandereycken, A., Brostaux, Y., Joie, E., Haubruge, E. & Verheggen, F.J. (2013) Occurrence of Harmonia axyridis (Coleoptera: Coccinellidae) in field crops. European Journal of Entomology, 110, 285-292.
77. Verheggen, F.J., Fagel, Q., Heuskin, S., Lognay, G., Francis, F. & Haubruge, E. (2007) Electrophysiological and behavioral responses of the multicolored Asian lady beetle, Harmonia axyridis Pallas, to sesquiterpene semiochemicals. Journal of Chemical Ecology, 33, 2148-2155.
78. Vilà, M., Basnou, C., Pyšek, P., Josefsson, M., Genovesi, P., Gollasch, S. et al. (2009) How well do we understand the impacts of alien species on ecosystem services? A pan-European, cross-taxa assessment. Frontiers in Ecology and the Environment, 8, 135-144.
79. Vilcinskas, A., Stoecker, K., Schmidtberg, H., Rohrich, C.R. & Vogel, H. (2013) Invasive harlequin ladybird carries biological weapons against native competitors. Science, 340, 862.
80. Ware, R.L. & Majerus, M.E.N. (2008) Intraguild predation of immature stages of British and Japanese coccinellids by the invasive ladybird Harmonia axyridis. BioControl, 53, 169-188.
81. Ware, R.L., Ramon-Portugal, F., Magro, A., Ducamp, C., Hemptinne, J.L. & Majerus, M.E.N. (2008) Chemical protection of Calvia quatuordecimguttata eggs against intraguild predation by the invasive ladybird Harmonia axyridis. BioControl, 53, 189-200.
82. Ware, R.L., Yguel, B. & Majerus, M.E.N. (2009) Effects of competition, cannibalism and intra-guild predation on larval development of the European coccinellid Adalia bipunctata and the invasive species Harmonia axyridis. Ecological Entomology, 34, 12-19.
83. Ware, R., Michie, L., Otani, T., Rhule, E. & Hall, R.J. (2010) Adaptation of native parasitoids to a novel host: the invasive coccinellid Harmonia axyridis. IOBC Bulletin, 58, 175-182.
84. Wells, P.M. (2011) Intraguild predation by Harmonia axyridis: effects on native enemies and aphid suppression. PhD thesis, University of Cambridge.
85. Wells, P.M., Baverstock, J., Majerus, M.E.N., Jiggins, F.M., Roy, H.E. & Pell, J.K. (2010) Intraguild predation of non-coccinellid aphid natural enemies by Harmonia axyridis: prey range and factors influencing intraguild predation. IOBC/WPRS Bulletin (Working Group "Benefits and Risks of exotic biological Control Agents"), 58, 185-196.
86. Wilson, J.R.U., Dormontt, E.E., Prentis, P.J., Lowe, A.J. & Richardson, D.M. (2009) Something in the way you move: dispersal pathways affect invasion success. Trends in Ecology & Evolution, 24, 136-144.