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BioControl

, Volume 62, Issue 3, pp 319–330 | Cite as

Spotlight on the positive effects of the ladybird Harmonia axyridis on agriculture

  • Eric W. RiddickEmail author
Review

Abstract

In the midst of considerable negativity surrounding the ladybird Harmonia axyridis (Pallas), this paper sheds some light on the positive effects that this predator has had on agriculture. Using resources available at the USDA, National Agricultural Library (DigiTop literature database, Navigator platform), I searched the abstracts of published literature on H. axyridis using the search term “Harmonia axyridis” or “Leis axyridis.” After deleting duplicate records, there were 1193 total records on this ladybird in the database dating from 1961–2015. Of this total, 90 records (7.54 %) highlighted positive effects of H. axyridis on agriculture in terms of its spectacular voracity, predation capacity, and effectiveness in suppressing plant pests, primarily aphids and scales, in forests, orchards, crop fields, gardens, greenhouses, and in laboratory bioassays. More concerted research is necessary to develop methodologies to exploit the positive behaviors of H. axyridis, while managing its negative ones.

Keywords

Coccinellidae Multicolored Asian lady beetle Harlequin ladybird Pest management 

Notes

Acknowledgments

Ted E. Cottrell and Michael Grodowitz reviewed an earlier version of this manuscript. Comments from journal editors and anonymous peer reviewers improved the manuscript. The United States Government has the right to retain a non-exclusive, royalty free license in and to any copyright of this article. Mention of a commercial or proprietary product does not constitute an endorsement of the product by the United States Department of Agriculture (USDA). USDA-ARS is an equal opportunity provider and employer.

References

  1. Abbas MG, Karar H, Dutcher JD (2013) Efficacy of multicolored Asian ladybeetle (Coleoptera: Coccinellidae) as a control for aphids in pecan orchards. J Entomol Sci 48:70–74CrossRefGoogle Scholar
  2. 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 56:207–213CrossRefGoogle Scholar
  3. Alyokhin A, Sewell G (2004) Changes in a lady beetle community following the establishment of three alien species. Biol Invasion 6:463–471CrossRefGoogle Scholar
  4. Bahlai CA, Colunga-Garcia M, Gage SH, Landis DA (2015) The role of exotic ladybeetles in the decline of native ladybeetle populations: evidence from long-term monitoring. Biol Invasion 17:1005–1024CrossRefGoogle Scholar
  5. Brown M (1999) Temporal changes in the aphid predator guild in eastern North America. IOBC/WPRS Bull 22:7–11Google Scholar
  6. Brown MW (2004) Role of aphid predator guild in controlling spirea aphid populations on apple in West Virginia, USA. Biol Control 29:189–198CrossRefGoogle Scholar
  7. Brown MW (2011) Importance of early arrival of adult Harmonia axyridis for control of Aphis spiraecola on apple. BioControl 56:65–69CrossRefGoogle Scholar
  8. Brown MW, Mathews CR (2007) Conservation biological control of rosy apple aphid, Dysaphis plantaginea (Passerini), in eastern North America. Environ Entomol 36:1131–1139PubMedCrossRefGoogle Scholar
  9. Brown PMJ, Adriaens T, Bathon H, Cuppen J, Goldarazena A, Hägg T, Kenis M, Klausnitzer BEM, Kovář I, Loomans AJM, Majerus MEN, Nedved O, Pedersen J, Rabitsch W, Roy HE, Ternois V, Zakharov IA, Roy DB (2008) Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. BioControl 53:5–21CrossRefGoogle Scholar
  10. Brown PMJ, Thomas CE, Lombaert E, Jeffries DL, Estoup A, Lawson Handley L-J (2011) The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. BioControl 56:623–641CrossRefGoogle Scholar
  11. Butin EE, Elkinton JS, Havill NP, Montgomery ME (2004) Feeding preference of three lady beetle predators of the hemlock woolly adelgid (Homoptera: Adelgidae). J Econ Entomol 97:1635–1641PubMedCrossRefGoogle Scholar
  12. Chen P, Wang F, Li C, Wang X, Ruan C (2015) Control potential of Harmonia axyridis (Pallas) against Aphis craccivora (Koch) by life table technique. J Jilin Agric Univ 37:14–19Google Scholar
  13. Choi S-Y, Kim G-H (1985) Aphidivorous activity of a coccinellid beetle, Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Korean J Plant Prot 24:11–14Google Scholar
  14. Choi KS, Lee SG, Kim JK, Park JD (1995) Role of the coccinellid beetle, Harmonia axyridis in the biological control of the black pine bast scale insect, Matsucoccus thunbergianae. FRI J For Sci 51:115–118Google Scholar
  15. Comont RF, Roy HE, Harrington R, Shortall CR, Purse BV (2014) Ecological correlates of local extinction and colonisation in the British ladybird beetles (Coleoptera: Coccinellidae). Biol Invasion 16:1805–1817CrossRefGoogle Scholar
  16. Costamagna AC, Landis DA (2006) Predators exert top-down control of soybean aphid across a gradient of agricultural management systems. Ecol Appl 16:1619–1628PubMedCrossRefGoogle Scholar
  17. Costamagna AC, Landis DA (2007) Quantifying predation on soybean aphid through direct field observations. Biol Control 42:16–24CrossRefGoogle Scholar
  18. Dong YG (1988) Trials on the control of Aphis gossypii Glover with Coccinella axyridis Pallas. Zhejiang Agric Sci 3:135–139Google Scholar
  19. Dutcher JD (2004) Habitat manipulation for enhancement of aphidophagous insects in pecan orchards. Int J Ecol Environ Sci 30:13–22Google Scholar
  20. Dutcher JD, Estes PM, Dutcher MJ (1999) Interactions in entomology: Aphids, aphidophaga and ants in pecan orchards. J Entomol Sci 34:40–56Google Scholar
  21. Dutcher JD, Karar H, Abbas G (2012) Seasonal abundance of aphids and aphidophagous insects in pecan. Insects 3:1257–1270PubMedPubMedCentralCrossRefGoogle Scholar
  22. El-Arnaouty SA, Beyssat-Arnaouty V, Ferran A, 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 10:129–136Google Scholar
  23. Ellington JJ, Carrillo TD, LaRock D, Richman DB, Lewis BE, El-Salam AH (1995) Biological control of pecan insects in New Mexico. Hort Technol 5:230–233Google Scholar
  24. Facon B, Crespin L, Loiseau A, Lombaert E, Magro A, Estoup A (2011) Can things get worse when an invasive species hybridizes? The harlequin ladybird Harmonia axyridis in France as a case study. Evol Appl 4:71–88PubMedCrossRefGoogle Scholar
  25. Fan Y, Yang S (1983) Occurrence of Leis axyridis (Pallas) (Col.: Coccinellidae). Nat Enemies Ins 5:94–96Google Scholar
  26. Ferran A, Niknam H, Brun J, Iperti G, Lapchin L, Kabiri F, Picart J-L, De Herce C (1996) The use of Harmonia axyridis larvae (Coleoptera: Coccinellidae) against Macrosiphum rosae (Hemiptera: Sternorrhyncha: Aphididae) on rose bushes. Eur J Entomol 93:59–67Google Scholar
  27. Ferran A, Giuge L, Tourniaire R, Gambier J, Fournier D (1998) An artificial non-flying mutation to improve the efficiency of the ladybird Harmonia axyridis in biological control of aphids. BioControl 43:53–64CrossRefGoogle Scholar
  28. Flowers RW, Salom SM, Kok LT (2006) Competitive interactions among two specialist predators and a generalist predator of hemlock woolly adelgid, Adelges tsugae (Hemiptera: Adelgidae) in southwestern Virginia. Agric For Entomol 8:253–262CrossRefGoogle Scholar
  29. Fox TB, Landis DA, Cardoso FF, Difonzo CD (2004) Predators suppress Aphis glycines Matsumara population growth in soybean. Environ Entomol 33:608–618CrossRefGoogle Scholar
  30. Fye RE (1981) Rearing and release of coccinellids for potential control of pear psylla. Advances in agricultural technology. Agric Res Serv, USDA (AAT-W-20) pp. 9Google Scholar
  31. Gardiner MM, Landis DA (2007) Impact of intraguild predation by adult Harmonia axyridis (Coleoptera: Coccinellidae) on Aphis glycines (Hemiptera: Aphididae) biological control in cage studies. Biol Control 40:386–395CrossRefGoogle Scholar
  32. Glemser EJ, Dowling L, Inglis D, Pickering GJ, McFadden-Smith W, Sears MK, Hallett RH (2012) A novel method for controlling multicolored Asian lady beetle (Coleoptera: Coccinellidae) in vineyards. Environ Entomol 41:1169–1176PubMedCrossRefGoogle Scholar
  33. Gordon RD (1985) The Coccinellidae (Coleoptera) of America north of Mexico. J NY Entomol Soc 93:1–912Google Scholar
  34. Hesler LS (2014) Inventory and assessment of foliar natural enemies of the soybean aphid (Hemiptera: Aphididae) in South Dakota. Environ Entomol 43:577–588PubMedCrossRefGoogle Scholar
  35. Hu Y, Wang Z, Ning C, Pi Z, Gao G (1989) The functional response of Harmonia (Leis) axyridis to their prey of Cinara sp. Nat Enemies Ins 11:164–168Google Scholar
  36. Hukusima S, Kondo K (1962) Further evaluation in the feeding potential of the predaceous insects and spiders in association with aphids harmful to apple and pear growing, and the effect of pesticides on predators. Jpn J Appl Entomol Zool 6:274–279CrossRefGoogle Scholar
  37. Hukusima S, Ohwaki T (1972) Further notes on feeding biology of Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Res Bull Fac Agric 33:75–82Google Scholar
  38. Iguchi M, Fukushima F, Miura K (2012) Control of Aphis gossypii and Myzus persicae (Hemiptera: Aphididae) by a flightless strain of Harmonia axyridis (Coleoptera: Coccinellidae) on green pepper plants in open fields. Entomol Sci 15:127–132CrossRefGoogle Scholar
  39. Katsoyannos P, Kontodimas DC, Stathas GJ, Tsartsalis CT (1997) Establishment of Harmonia axyridis on citrus and some data on its phenology in Greece. Phytoparasitica 25:183–191CrossRefGoogle Scholar
  40. Kenis M, Roy HE, Zindel R, Majerus MEN (2008) Current and potential management strategies against Harmonia axyridis. BioControl 53:235–252CrossRefGoogle Scholar
  41. Kitagami T, Ohkubo N (2004) Biological control of the aphid Aphis gossypii on strawberry [Fragaria] in the greenhouse by release of the ladybird beetles Harmonia axyridis and Coccinella septempunctata, 1: effect of control by released ladybird beetle larvae. Bull agric res div mite prefect sci technol promot cent (Japan) 30:19–24Google Scholar
  42. Koch RL (2003) The multicolored Asian lady beetle, Harmonia axyridis: A review of its biology, uses in biological control, and non-target impacts. J Insect Sci 3:1–16CrossRefGoogle Scholar
  43. Koch RL, Venette RC, Hutchison WD (2006) Invasions by Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in the western hemisphere: implications for South America. Neotrop Entomol 35:421–434PubMedCrossRefGoogle Scholar
  44. Kuroda T, Miura K (2003) Comparison of the effectiveness of two methods for releasing Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) against Aphis gossypii Glover (Homoptera: Aphididae) on cucumbers in a greenhouse. Appl Entomol Zool 38:271–274CrossRefGoogle Scholar
  45. LaMana ML, Miller JC (1996) Field observations on Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in Oregon. Biol Control 6:232–237CrossRefGoogle Scholar
  46. LaRock DR, Ellington JJ (1996) An integrated pest management approach, emphasizing biological control, for pecan aphids. Southwest Entomol 21:153–166Google Scholar
  47. LaRock DR, Mirdad Z, Ellington JJ, Carrillo T, Southward M (2003) Control of green peach aphids Myzus persicae with lady beetles Harmonia axyridis on chile Capsicum annum in the greenhouse. Southwest Entomol 28:249–253Google Scholar
  48. Lei CL, Chen HX (1987) Effects of various aphid densities on the predation and development of larvae of Propylea japonica and Harmonia axyridis. Nat Enemies Ins 9:213–216Google Scholar
  49. Lieten F (1998) Strawberries. Integrated strawberry production: experiences with ladybirds to control aphids. Proeftuinnieuws 8:45–46Google Scholar
  50. Lucas É, Lapalme S, Coderre D (1997) Comparative voracity of three aphidophagous ladybeetles against the European red mite (Acarina: Tetranychidae). Phytoprotection 78:117–123CrossRefGoogle Scholar
  51. Lucas É, Gagné I, Coderre D (2002) Impact of the arrival of Harmonia axyridis on adults of Coccinella septempunctata and Coleomegilla maculata (Coleoptera: Coccinellidae). Eur J Entomol 99:457–463CrossRefGoogle Scholar
  52. Luo HH (1987) Functional response of Harmonia axyridis to the density of Rhopalosiphum prunifoliae. Nat Enemies Ins 9:84–87Google Scholar
  53. Majerus M, Strawson V, Roy H (2006) The potential impacts of the arrival of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in Britain. Ecol Entomol 31:207–215CrossRefGoogle Scholar
  54. McClure MS (1983) Lady beetle attacks red pine scale. Front Plant Sci 35:3–4Google Scholar
  55. McClure MS (1986a) Importing ladybird beetles to control red pine scale. Front Plant Sci 39:5–7Google Scholar
  56. McClure MS (1986b) Role of predators in regulation of endemic populations of Matsucoccus matsumurae (Homoptera: Margarodidae) in Japan. Environ Entomol 15:976–983CrossRefGoogle Scholar
  57. 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 16:224–230CrossRefGoogle Scholar
  58. Michaud JP (2000) Development and reproduction of ladybeetles (Coleoptera: Coccinellidae) on the citrus aphids Aphis spiraecola Patch and Toxoptera citricida (Kirkaldy) (Homoptera: Aphididae). Biol Control 18:287–297CrossRefGoogle Scholar
  59. Michaud JP (2002) Biological control of Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae) in Florida: a preliminary report. Entomol News 113:216–222Google Scholar
  60. Michaud JP (2004) Natural mortality of Asian citrus psyllid (Homoptera: Psyllidae) in central Florida. Biol Control 29:260–269CrossRefGoogle Scholar
  61. Michaud JP, Olsen LE (2004) Suitability of Asian citrus psyllid, Diaphorina citri, as prey for ladybeetles. BioControl 49:417–431CrossRefGoogle Scholar
  62. Mignault M, Roy M, Brodeur J (2006) Soybean aphid predators in Quebec and the suitability of Aphis glycines as prey for three Coccinellidae. BioControl 51:89–106CrossRefGoogle Scholar
  63. Miller SS, Brown MW (1998) Coccinellidae (Coleoptera) in apple orchards of eastern West Virginia and the impact of invasion by Harmonia axyridis. Entomol News 109:143–151Google Scholar
  64. Mizell RF III (2007) Impact of Harmonia axyridis (Coleoptera: Coccinellidae) on native arthropod predators in pecan and crape myrtle. Fla Entomol 90:524–536CrossRefGoogle Scholar
  65. Nalepa CA, Kidd KA, Ahlstrom KR (1996) Biology of Harmonia axyridis (Coleoptera: Coccinellidae) in winter aggregations. Ann Entomol Soc Am 89:681–685CrossRefGoogle Scholar
  66. Obata S (1997) The influence of aphids on the behaviour of adults of the ladybird beetle, Harmonia axyridis (Col.: Coccinellidae). Entomophaga 42:103–106CrossRefGoogle Scholar
  67. Okamoto H, Sato M (1973) The influence of different aphids as food upon the ecological and morphological characters of the lady beetles Harmonia axyridis Pallas and Coccinella septempunctata bruckii Mulsant (Coleoptera: Coccinellidae). (Laboratory studies on food ecology of aphidophagous coccinellids 1). Kontyu 41:342–358Google Scholar
  68. Okuno T (1961) Feeding tests and some field observations of three aphidophagous coccinellids. Publ Ent Lab, Coll Agric Univ Osaka 6:149–152Google Scholar
  69. Orlandini G, Martellucci R (1997) Melon: biological control of Aphis gossypii. Colt Prot 26:33–36Google Scholar
  70. Osawa N (2000) Population field studies on the aphidophagous ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae): Resource tracking and population characteristics. Popul Ecol 42:115–127CrossRefGoogle Scholar
  71. Pervez A, Omkar (2006) Ecology and biological control application of multicoloured Asian ladybird, Harmonia axyridis: a review. Biocontrol Sci Technol 16:111–128CrossRefGoogle Scholar
  72. Pickering G, Lin J, Reynolds A, Soleas G, Riesen R, Brindle I (2005) The influence of Harmonia axyridis on wine composition and aging. J Food Sci 70:S128–S135CrossRefGoogle Scholar
  73. Pickering GJ, Inglis D, McFadden-Smith W, Ker K, Glemser EJ, Hallett R (2012) Good bugs gone bad: Coccinellidae, sustainability and wine. WIT Trans Ecol Environ 167:239–251Google Scholar
  74. Piotte C, Tourniaire R, Brun J, Gambier J, Ferran A (1999) The sedentary Harmonia axyridis ladybird against aphids. A highly efficient ally in biological control. Phytoma 519:18–20Google Scholar
  75. Plotnikov VF (1981) Efficacy of the use of aphidophagous insects for the protection of glasshouse vegetable crops. Institut national de la recherche agronomique lutte biologique et intégrée contre les pucerons. Coll Fr Sov Rennes 1979:59–65Google Scholar
  76. Quattro JD (1995) Gotcha! tiny lady beetles have big biocontrol potential. Agric Res (Washington DC) 43:4–8Google Scholar
  77. Ray JN, Pence HL (2004) Ladybug hypersensitivity: report of a case and review of literature. Allergy Asthma Proc 25:133–136PubMedGoogle Scholar
  78. Riddick EW, Aldrich JR, De Milo A, Davis JC (2000) Potential for modifying the behavior of the multicolored Asian lady beetle (Coleoptera: Coccinellidae) with plant-derived natural products. Ann Entomol Soc Am 93:1314–1321CrossRefGoogle Scholar
  79. Roy HE, Brown PMJ (2015) Ten years of invasion: Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Britain. Ecol Entomol 40:336–348PubMedPubMedCentralCrossRefGoogle Scholar
  80. Roy HE, Lawson Handley L-J (2012) Networking: a community approach to invaders and their parasites. Funct Ecol 26:1238–1248CrossRefGoogle Scholar
  81. Roy HE, Adriaens T, Isaac NJ, Kenis M, Onkelinx T, Martin GS, Brown PM, Hautier L, Poland R, Roy DB, Comont R, Eschen R, Frost R, Zindel R, van Vlaenderen J, Nedvěd O, Ravn HP, Grégoire J, de Biseau J, Maes D (2012) Invasive alien predator causes rapid declines of native European ladybirds. Divers Distrib 18:717–725CrossRefGoogle Scholar
  82. Rutledge CE, O’Neil RJ, Fox TB, Landis DA (2004) Soybean aphid predators and their use in integrated pest management. Ann Entomol Soc Am 97:240–248CrossRefGoogle Scholar
  83. Savoiskaya GI (1970) The Far-Eastern ladybird against the apple aphid. Zash Rast 15:12–13Google Scholar
  84. Schmidt NP, O’Neal ME, Dixon PM (2008) Aphidophagous predators in Iowa soybean: a community comparison across multiple years and sampling methods. Ann Entomol Soc Am 101:341–350CrossRefGoogle Scholar
  85. Seko T, Miura K, Yamashita K-I (2008) Residence period of a flightless strain of the ladybird beetle Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in open fields. Biol Control 47:194–198CrossRefGoogle Scholar
  86. Seko T, Miura K, Sumi A, Nakano A, Kameshiro M, Kaneda T (2014) Suppression of aphids by augmentative release of larvae of flightless Harmonia axyridis. J Appl Entomol 138:326–337CrossRefGoogle Scholar
  87. Seo MJ, Youn YN (2000) The Asian ladybird, Harmonia axyridis, as biological control agents: I. predacious behavior and feeding ability. Korean J Appl Entomol 39:59–71Google Scholar
  88. Seo MJ, Youn YN (2002) Effective preservation methods of the Asian ladybird, Harmonia axyridis (Coleoptera: Coccinellidae), as an application strategy for the biological control of aphids. J Asia Pac Entomol 5:209–214CrossRefGoogle Scholar
  89. Sidlyarevich VI, Voronin KE (1973) Trials on using Leis axyridis under glass. Zash Rast 6:24Google Scholar
  90. Snyder WE, Ballard SN, Yang S, Clevenger GM, Miller TD, Ahn JJ, Hatten TD, Berryman AA (2004) Complementary biocontrol of aphids by the ladybird beetle Harmonia axyridis and the parasitoid Aphelinus asychis on greenhouse roses. Biol Control 30:229–235CrossRefGoogle Scholar
  91. Stals R, Prinsloo G (2007) Discovery of an alien invasive, the predatory insect in South Africa: the multicoloured Asian ladybird beetle, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). S Afr J Sci 103:123–126Google Scholar
  92. Sun X, Chen W, Chen Z, He J, Ye W (1996) A preliminary study on the artificial diet of an aphidophagous coccinellid, Harmonia axyridis (Pallas) and its use to control strawberry aphids under plastic covering. J Shanghai Agric Coll 14:133–137Google Scholar
  93. Tedders WL, Schaefer PW (1994) Release and establishment of Harmonia axyridis (Coleoptera: Coccinellidae) in the southeastern United States. Entomol News 105:228–243Google Scholar
  94. Tourniaire R, Ferran A, Giuge L, Gambier J, Brun J (1999) Flightless strains of Harmonia axyridis Pallas (Coleoptera: Coccinellidae): some behavioural and biological features. Ann Soc Entomol Fr 35(Suppl):509–513Google Scholar
  95. Tourniaire R, Ferran A, Gambier J, Giuge L, Bouffault F (2000a) Locomotory behavior of flightless Harmonia axyridis Pallas (Col., Coccinellidae). J Ins Physiol 46:721–726CrossRefGoogle Scholar
  96. Tourniaire R, Ferran A, Giuge L, Piotte C, Gambier J (2000b) A natural flightless mutation in the ladybird, Harmonia axyridis. Entomol Exp Appl 96:33–38CrossRefGoogle Scholar
  97. Trouvé C (1995) Tests on biological pest control against the hop aphid Phorodon humuli (Schrank) (Homoptera: Aphididae) in Northern France: results from 1993 to 1994. Med Fac Landbouw Toeg Biol Weten Univ Gent 60:781–792Google Scholar
  98. Trouvé C, Lédée S, Brun J, Ferran A (1996) Biological control of the hop aphid. A review of three years of tests in northern France. Phytoma 486:41–44Google Scholar
  99. Trouvé C, Lédée S, Ferran A, Brun J (1997) Biological control of the damson-hop aphid, Phorodon humuli (Hom.: Aphididae), using the ladybeetle Harmonia axyridis (Col.: Coccinellidae). Entomophaga 42:57–62CrossRefGoogle Scholar
  100. Turgeon J, Tayeh A, Facon B, Lombaert E, De Clercq P, Berkvens N, Lundgren JG, Estoup A (2011) Experimental evidence for the phenotypic impact of admixture between wild and biocontrol Asian ladybird (Harmonia axyridis) involved in the European invasion. J Evol Biol 24:1044–1052PubMedCrossRefGoogle Scholar
  101. van Lenteren JC, Loomans AJM, Babendreier D, Bigler F (2008) Harmonia axyridis: an environmental risk assessment for Northwest Europe. BioControl 53:37–54CrossRefGoogle Scholar
  102. Vandereycken A, Durieux D, Joie É, Haubruge É, Verheggen FJ (2012) Habitat diversity of the multicolored Asian ladybeetle Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in agricultural and arboreal ecosystems: a review. Biotechnol Agron Soc Environ 16:553–563Google Scholar
  103. Wang LY (1982) Control of Matsucoccus massonianae Young et Hu (Hom.: Margarodidae) by Leis axyridis (Pallas). Nat Enemies Ins 4:37–39Google Scholar
  104. Ware RL, Majerus MEN (2008) Intraguild predation of immature stages of British and Japanese coccinellids by the invasive ladybird Harmonia axyridis. BioControl 53:169–188CrossRefGoogle Scholar
  105. Weissenberger A, Brun J, Piotte C, Ferran A (1999) Comparison between the wild type and flightless type of the coccinellid Harmonia axyridis (Pallas) in the control of the damson hop aphid Phorodon humuli (Schrank). In: Proceedings 5th International Conference Pests Agriculture 3:727–734Google Scholar
  106. Wells ML, McPherson RM (1999) Population dynamics of three coccinellids in flue-cured tobacco and functional response of Hippodamia convergens (Coleoptera: Coccinellidae) feeding on tobacco aphids (Homoptera: Aphididae). Environ Entomol 28:768–773CrossRefGoogle Scholar
  107. Wenpeng S, Lanlan H, Changchun D, Zhifeng H, Kuijun Z (2015) Control of soybean aphid by dominant natural enemy complexes in field. Chin J Biol Control 31:193–201Google Scholar
  108. With KA, Pavuk DM, Worchuck JL, Oates RK, Fisher JL (2002) Threshold effects of landscape structure on biological control in agroecosystems. Ecol Appl 12:52–65CrossRefGoogle Scholar
  109. Wu S, Yu W (2000) A study on Physokermes shanxiensis Tang (Homoptera: Coccoidea: Coccidae). Sci Silvae Sin 36:98–102Google Scholar
  110. Xu FY, Wu DX (1989) Control of bamboo scale insects by intercropping rape in the bamboo forest to attract coccinellid beetles. Chin J Biol Control 5:117–119Google Scholar
  111. Xue Y, Bahlai CA, Frewin A, Sears MK, Hallett RH, Schaafsma AW (2009) Predation by Coccinella septempunctata and Harmonia axyridis (Coleoptera: Coccinellidae) on Aphis glycines (Homoptera: Aphididae). Environ Entomol 38:708–714PubMedCrossRefGoogle Scholar
  112. Yan F, Zhou Z, Wang S, Cao Y, Li K (2012) The effect of hedgerows on the distribution of Harmonia axyridis Pallas in agroforestry systems. Acta Ecol Sin 32:2230–2238CrossRefGoogle Scholar
  113. Yasuda H, Ishikawa H (1999) Effects of prey density and spatial distribution on prey consumption of the adult predatory ladybird beetle. J Appl Entomol 123:585–589CrossRefGoogle Scholar
  114. Yu H-L, Men X-Y, Ye B-H, Yu Y, Zhang A-S, Li L-L, Zhou X-H, Zhang S-C, Zhuang Q-YA (2014) Effects of suppression of natural enemies on cotton aphids. Chin J Appl Entomol 51:99–106Google Scholar

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© International Organization for Biological Control (outside the USA) 2016

Authors and Affiliations

  1. 1.USDA-ARS, Jamie-Whitten Delta States Research CenterStonevilleUSA

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