Journal of Pest Science

, Volume 91, Issue 3, pp 1153–1164 | Cite as

Sublethal effects of two reduced-risk insecticides: when the invasive ladybeetle is drastically affected, whereas the indigenous not

  • P. CabreraEmail author
  • D. Cormier
  • E. Lucas
Original paper


Chlorantraniliprole and novaluron, two reduced-risk insecticides (IRRs), are currently used to control codling moth (Cydia pomonella) in apple orchards in southeastern Canada. Reproduction of Harmonia axyridis (Pallas), an invasive ladybeetle, and the indigenous Coleomegilla maculata DeGeer, both important generalist predators, might be compromised after exposure of adults to these IRRs. The aim of the study was to compare the effects of chlorantraniliprole and novaluron on fecundity and fertility between the two ladybeetles in a laboratory setting. Reproductive mates were given chlorantraniliprole- or novaluron-treated prey for 24 h, and reproductive performance was followed during 15 days. Chlorantraniliprole did not affect reproduction of ladybeetles. However, novaluron-reduced fecundity, egg hatch, and fertility of the invasive ladybeetle H. axyridis, by 29, 43, and 78.7%, respectively, contrasting with no significant effect on the indigenous C. maculata. Additionally, H. axyridis oviposition pattern was altered by the same insecticide. This resulted in more egg masses containing fewer eggs, compared to the control. No such changes were detected for C. maculata. Chlorantraniliprole does not disturb reproduction of H. axyridis or C. maculata. Treatments of novaluron should have an important effect on populations of the invasive H. axyridis, and consequently on the impact of the invader on native ladybeetle species and on its dominance, and finally potentially on biocontrol services provided by the assemblage of ladybeetles.


Harmonia axyridis Coleomegilla maculata Chlorantraniliprole Novaluron Reproduction Invasive species 



Funding of this project was provided by the regional industry council of Quebec, executing the Canadian Agricultural Adaptation Program for Agriculture and Agri-Food Canada, the Program Prime-Vert from the Ministry of Agriculture, Fisheries and Food from Quebec, the Natural Sciences and Engineering Research Council of Canada (NSERC), and Canada Foundation for innovation (CFI). We also want to thank Jill Vandermeerschen for her advice with statistical analyses, Marc Fournier for his technical support in the laboratory, Franz Vanoosthuyse for the technical support, and all the students for assisting with the ladybeetle rearings and for helping us to take data during long hours in the laboratory.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Adama Agricultural Solutions (2015) RIMON 10 EC insecticide. Canadian Label, Winnipeg, p 26Google Scholar
  2. Agarwala B, Dixon A (1993) Why do ladybirds lay eggs in clusters? Funct Ecol 7:541–548CrossRefGoogle Scholar
  3. Agarwala BK, Yasuda H (2001) Overlapping oviposition and chemical defense of eggs in two co-occurring species of ladybird predators of aphids. J Ethol 19:47–53CrossRefGoogle Scholar
  4. Alyokhin A, Sewell G (2004) Changes in a lady beetle community following the establishment of three alien species. Biol Invasions 6:463–471CrossRefGoogle Scholar
  5. Alyokhin A, Guillemette R, Choban R (2009) Stimulatory and suppressive effects of novaluron on the Colorado potato beetle reproduction. J Econ Entomol 102:2078–2083CrossRefPubMedGoogle Scholar
  6. Amarasekare KG, Shearer PW (2013) Comparing effects of insecticides on two green lacewings species, Chrysoperla johnsoni and Chrysoperla carnea (Neuroptera: Chrysopidae). J Econ Entomol 106:1126–1133CrossRefPubMedGoogle Scholar
  7. Brown PM, Thomas CE, Lombaert E, Jeffries DL, Estoup A, Handley L-JL (2011) The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. Biocontrol 56:623–641CrossRefGoogle Scholar
  8. Brugger KE, Cole PG, Newman IC, Parker N, Scholz B, Suvagia P et al (2010) Selectivity of chlorantraniliprole to parasitoid wasps. Pest Manag Sci 66:1075–1081CrossRefPubMedGoogle Scholar
  9. Cabrera P, Cormier D, Fournier M, Lucas É (2014) Lethal effects of two reduced risk insecticides on Harmonia axyridis and Coleomegilla maculata (Col., Coccinellidae) following two routes of exposure. IOBC-WPRS Bull 103:41–45Google Scholar
  10. Cabrera P, Cormier D, Lucas É (2017) Differential sensitivity of an invasive and an indigenous ladybeetle to two reduced-risk insecticides. J Appl Entomol. CrossRefGoogle Scholar
  11. Carton B, Smagghe G, Tirry L (2003) Toxicity of two ecdysone agonists, halofenozide and methoxyfenozide, against the multicoloured Asian lady beetle Harmonia axyridis (Col., Coccinellidae). J Appl Entomol 127:240–242CrossRefGoogle Scholar
  12. Coderre D, Lucas É, Gagné I (1995) The occurrence of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Canada. Can Entomol 127:609–611CrossRefGoogle Scholar
  13. Collett D (2002) Modelling binary data. CRC Press, Boca Raton, p 408Google Scholar
  14. Cordova D, Benner EA, Sacher MD, Rauh JJ, Sopa JS, Lahm GP et al (2007) The novel mode of action of anthranilic diamide insecticides: ryanodine receptor activation, In: Synthesis and chemistry of agrochemical VII, Ch 17; ACS symposium series 948, pp 223–234Google Scholar
  15. Cormier D, Yelle PÉ (2010) Guide to foliar treatments of apple tress 2010–2011. Centre de Référence en Agriculture et Agroalimentaire du Québec, QuébecGoogle Scholar
  16. Cormier D, Pelletier F, Chouinard G (2013) Residual toxicity of six reduced-risk insecticides to codling moth eggs and neonate larvae. IOBC-WPRS Bull 91:147–151Google Scholar
  17. Costa HN, da Cunha FM, Cruz GS, D’Assunção CG, Rolim GG, Barros MEG et al (2017) Lufenuron impact upon Anthonomus grandis Boheman (Coleoptera: Curculionidae) midgut and its reflection in gametogenesis. Pestic Biochem Physiol 137(Supplement C):71–80CrossRefPubMedGoogle Scholar
  18. Coutanceau J-P (2006) Harmonia axyridis (Pallas, 1773): une coccinelle asiatique introduite, acclimatée et en extension en France. Bull Soc Entomol Fr 111:395–401Google Scholar
  19. Croft BA (1990) Arthropod biological control agents and pesticides. Wiley, New York, p 723Google Scholar
  20. Cutler GC, Scott-Dupree CD (2007) Novaluron: prospects and limitations in insect pest management. Pest Technol 1:38–46Google Scholar
  21. Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106CrossRefPubMedGoogle Scholar
  22. Detzel A, Wink M (1993) Attraction, deterrence or intoxication of bees (Apis mellifera) by plant allelochemicals. Chemoecology 4:8–18CrossRefGoogle Scholar
  23. Dinter A, Brugger K, Bassi A, Frost NM, Woodward MD (2008) Chlorantraniliprole (DPX-E2Y45, DuPont™ Rynaxypyr®, Coragen® and Altacor® insecticide)—a novel anthranilic diamide insecticide-demonstrating low toxicity and low risk for beneficial insects and predatory mites. IOBC-WPRS Bull 35:128–135Google Scholar
  24. Fernandes MES, Alves FM, Pereira RC, Aquino LA, Fernandes FL, Zanuncio JC (2016) Lethal and sublethal effects of seven insecticides on three beneficial insects in laboratory assays and field trials. Chemosphere 156:45–55CrossRefPubMedGoogle Scholar
  25. Fernandez L (2015) Lethal and sublethal effects of pesticides used in Western United States Orchards on Hippodamia convergens [Ph.D.]. University of California, Ann ArborGoogle Scholar
  26. Gagnon A-È, Heimpel GE, Brodeur J (2011) The ubiquity of intraguild predation among predatory arthropods. PLoS ONE 6:e28061CrossRefPubMedPubMedCentralGoogle Scholar
  27. Heimbach U, Dohmen P, Barrett KL, Brown K, Kennedy PJ, Kleiner R et al (2000) A method for testing effects of plant protection products on the carabid beetle Poecilus cupreus (Coleoptera, Carabidae) under laboratory and semi-field conditions. In: Candolfi MP (ed) Guidelines to evaluate side-effects of plant protection products to non-target arthropods. International Organization for Biological and Integrated Control of Noxious Animals and Plants, West Palearctic Regional Section (IOBC/WPRS), Ghent, pp 87–106Google Scholar
  28. Hodek I, Evans EW (2012) Food relationships. In: Hodek I, van Emden HF, Honek A (eds) Ecology and behaviour of the ladybird beetles (Coccinellidae). Wiley, Chichester, pp 110–140CrossRefGoogle Scholar
  29. Ishaaya I, Yablonski S, Mendelson Z, Mansour Y, Horowitz AR (1996) Novaluron (MCW-275), a novel benzoylphenyl urea, suppressing developing stages of Lepidoptera, white fly and leafminer pests. In: International conference, British crop protection council Brighton, pp 1013–1020Google Scholar
  30. Ishaaya I, Lebedev G, Ghanim M, Horowithz R (2011) Biorational control of arthropod pests with emphasis on the use of the chitin synthesis inhibitor novaluron. Pesticides 1:17–22Google Scholar
  31. Kabaluk J, Vernon R, Henderson D (2006) Population development of the green peach aphid and beneficial insects in potato fields in British Columbia. Can Entomol 138:647–660CrossRefGoogle Scholar
  32. Kim SHS, Wise JC, Gokce A, Whalon ME (2011) Novaluron causes reduced egg hatch after treating adult codling moths, Cydia pomenella: support for transovarial transfer. J Insect Sci 11:1–10CrossRefGoogle Scholar
  33. Kim SHS, Vandervoort C, Whalon ME, Wise JC (2014) Transovarial transmission of novaluron in Choristoneura rosaceana (Lepidoptera: Tortricidae). Can Entomol 146:347–353CrossRefGoogle Scholar
  34. 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
  35. Koch RL, Galvan TL (2008) Bad side of a good beetle: the North American experience with Harmonia axyridis. Biocontrol 53:23–35CrossRefGoogle Scholar
  36. Koch RL, Venette RC, Hutchison WD (2006) Invasions by Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in the western hemisphere: implications for South America. Neotrop Entomol 35:421–434CrossRefPubMedGoogle Scholar
  37. Kostyukovsky M, Trostanetsky A (2006) The effect of a new chitin synthesis inhibitor, novaluron, on various developmental stages of Tribolium castaneum (Herbst). J Stored Prod Res 42:136–148CrossRefGoogle Scholar
  38. Lucas E (2005) Intraguild predation among aphidophagous predators. Eur J Entomol 102:351–364CrossRefGoogle Scholar
  39. Lucas E (2012) Intraguild interactions. In: Hodek I, van Emden HF, Honek A (eds) Ecology and behaviour of the ladybird beetles (Coccinellidae). Wiley, Chichester, pp 343–374CrossRefGoogle Scholar
  40. Lucas E, Giroux S, Demougeot S, Duchesne RM, Coderre D (2004) Compatibility of a natural enemy, Coleomegilla maculata lengi (Col., Coccinellidae) and four insecticides used against the Colorado potato beetle (Col., Chrysomelidae). J Appl Entomol 128:233–239CrossRefGoogle Scholar
  41. Lucas E, Vincent C, Labrie G, Chouinard G, Fournier F, Pelletier F et al (2007) The multicolored Asian ladybeetle Harmonia axyridis (Coleoptera: Coccinellidae) in Quebec agroecosystems ten years after its arrival. Eur J Entomol 104:737CrossRefGoogle Scholar
  42. Lundgren JG, Razzak AA, Wiedenmann RN (2004) Population responses and food consumption by predators Coleomegilla maculata and Harmonia axyridis (Coleoptera: Coccinellidae) during anthesis in an Illinois cornfield. Environ Entomol 33:958–963CrossRefGoogle Scholar
  43. Mansur JF, Figueira-Mansur J, Santos AS, Santos-Junior H, Ramos IB, de Medeiros MN et al (2010) The effect of lufenuron, a chitin synthesis inhibitor, on oogenesis of Rhodnius prolixus. Pestic Biochem Physiol 98:59–67CrossRefGoogle Scholar
  44. Michaud J (2002) Invasion of the Florida citrus ecosystem by Harmonia axyridis (Coleoptera: Coccinellidae) and asymmetric competition with a native species, Cycloneda sanguinea. Environ Entomol 31:827–835CrossRefGoogle Scholar
  45. Mirande L, Desneux N, Haramboure M, Schneider M (2015) Intraguild predation between an exotic and a native coccinellid in Argentina: the role of prey density. J Pest Sci 88:155–162CrossRefGoogle Scholar
  46. Moscardini VF, Gontijo PC, Michaud JP, Carvalho GA (2015) Sublethal effects of insecticide seed treatments on two nearctic lady beetles (Coleoptera: Coccinellidae). Ecotoxicology 24:1152–1161CrossRefPubMedGoogle Scholar
  47. Moser SE, Harwood JD, Obrycki JJ (2008) Larval feeding on Bt hybrid and non-Bt corn seedlings by Harmonia axyridis (Coleoptera: Coccinellidae) and Coleomegilla maculata (Coleoptera: Coccinellidae). Environ Entomol 37(2):525–533PubMedGoogle Scholar
  48. Nawaz M, Cai W, Jing Z, Zhou X, Mabubu JI, Hua H (2017) Toxicity and sublethal effects of chlorantraniliprole on the development and fecundity of a non-specific predator, the multicolored Asian lady beetle, Harmonia axyridis (Pallas). Chemosphere 178:496–503CrossRefPubMedGoogle Scholar
  49. Nedvěd O, Honek A (2012) Life history and development. In: Hodek I, Van Emden HF, Honek A (eds) Ecology and behaviour of the ladybird beetles (Coccinellidae). Wiley, Chichester, pp 54–109CrossRefGoogle Scholar
  50. Nedvěd O, Háva J, Kulíková D (2011) Record of the invasive alien ladybird Harmonia axyridis (Coleoptera, Coccinellidae) from Kenya. ZooKeys 106:77CrossRefGoogle Scholar
  51. Oppenoorth FJ, Welling W (1976) Biochemistry and physiology of resistance. In: Wilkinson CF (ed) Insecticide biochemistry and physiology. Springer, Boston, pp 507–551CrossRefGoogle Scholar
  52. Preetha G, Stanley J, Suresh S, Kuttalam S, Samiyappan R (2009) Toxicity of selected insecticides to Trichogramma chilonis: assessing their safety in the rice ecosystem. Phytoparasitica 37:209–215CrossRefGoogle Scholar
  53. Romano FCB (2007) Ação de alguns inseticidas com propriedades esterilizantes sobre Spodoptera frugiperda (JE Smith, 1797) (Lepidoptera: Noctuidae) e seu predador Doru luteipes (Scudder, 1876) (Dermaptera: Forficulidae): Escola Superior de Agricultura “Luiz de Queiroz”Google Scholar
  54. Roy H, Wajnberg E (2007) From biological control to invasion: the ladybird Harmonia axyridis as a model species. Springer, Dordrecht, pp 1–4Google Scholar
  55. Roy HE, Brown PMJ, Adriaens T, Berkvens N, Borges I, Clusella-Trullas S et al (2016) The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol Invasions 18:997–1044CrossRefGoogle Scholar
  56. Sáenz-de-Cabezón Irigaray FJ, Zalom FG (2012) Transovarial biotransference of etoxazole through a terrestrial trophic web. Pest Manag Sci 68:1467–1470CrossRefPubMedGoogle Scholar
  57. SAS Institute (2016a). JMP® 12. Nonparametric. Accessed 14 Oct 2017
  58. SAS Institute (2016b) The GLIMMIX procedure. In: SI Inc. (ed) SAS/STAT® 142 user’s guide, Cary, pp 3266–3608Google Scholar
  59. Schmuck R, Candolfi MP, Kleiner R, Mead-Briggs M, Moll M, Kemmeter F et al (2000) A laboratory test system for assessing effects of plant protection products on the plant dwelling insect Coccinella semptempunctata L. (Coleoptera: Coccinellidae). In: Candolfi MP (ed) Guidelines to evaluate side-effects of plant protection products to non-target arthropods. International Organization for Biological and Integrated Control of Noxious Animals and Plants, West Palearctic Regional Section (IOBC/WPRS), Ghent, pp 45–54Google Scholar
  60. Sedivy C, Piskorski R, Müller A, Dorn S (2012) Too low to kill: concentration of the secondary metabolite ranunculin in buttercup pollen does not affect bee larval survival. J Chem Ecol 38:996–1002CrossRefPubMedGoogle Scholar
  61. Sokal R, Rohlf J (1995) Biometry: the principles and practice of statistics in biological research. W. H. Freeman, New York, p 850Google Scholar
  62. Stals R, Prinsloo G (2007) Discovery of an alien invasive, predatory insect in South Africa: the multicoloured Asian ladybird beetle, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). S Afr J Sci 103:123–126Google Scholar
  63. Stark JD, Banks JE (2003) Population-level effects of pesticides and other toxicants on arthropods. Annu Rev Entomol 48:505–519CrossRefPubMedGoogle Scholar
  64. Sun R, Liu C, Zhang H, Wang Q (2015) Benzoylurea chitin synthesis inhibitors. J Agric Food Chem 63:6847–6865CrossRefPubMedGoogle Scholar
  65. Talebi K, Kavousi A, Sabahi Q (2008) Impacts of pesticides on arthropod biological control agents. Pest Technol 2:87–97Google Scholar
  66. Todorova SI, Côté JC, Coderre D (1996) Evaluation of the effects of two Beauveria bassiana (Balsamo) Vuillemin strains on the development of Coleomegilla maculata lengi Timberlake (Col., Coccinellidae). J Appl Entomol 120:159–163CrossRefGoogle Scholar
  67. Trisyono A, Puttler B, Chippendale GM (2000) Effect of the ecdysone agonists, methoxyfenozide and tebufenozide, on the lady beetle, Coleomegilla maculata. Entomol Exp Appl 94:103–105CrossRefGoogle Scholar
  68. Trostanetsky A, Kostyukovsky M (2008) Transovarial activity of the chitin synthesis inhibitor novaluron on egg hatch and subsequent development of larvae of Tribolium castaneum. Phytoparasitica 36:38–41CrossRefGoogle Scholar
  69. Trostanetsky A, Kostyukovsky M, Quinn E (2015) Transovarial effect of novaluron on Tribolium castaneum (Coleoptera: Tenebrionidae) after termination of direct contact. J Insect Sci 15:125CrossRefPubMedPubMedCentralGoogle Scholar
  70. Zhang X, Xu Q, Lu W, Liu F (2015) Sublethal effects of four synthetic insecticides on the generalist predator Cyrtorhinus lividipennis. J Pest Sci 88:383–392CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratoire de Lutte Biologique, Departement des Sciences BiologiquesUniversité du Québec à MontréalMontréalCanada
  2. 2.Institut de recherche et de développement en agroenvironnementSaint-Bruno-de-MontarvilleCanada

Personalised recommendations