Side effects of pesticides on the larvae of the hoverfly Episyrphus balteatus in the laboratory

Abstract

The hoverfly Episyrphus balteatus (Degeer) is one of the most abundant predators of the cabbage aphid (Brevicoryne brassicae (L.)) in brussels sprouts in Belgium. In the current laboratory study, the toxicity of several insecticides applied at maximum recommended field rates was investigated on the larvae of E. balteatus. Two- to 3-day-old larvae were confined in glass petri dishes with dry residues of freshly applied insecticides. Their mortality was checked daily until adult emergence. Sub-lethal effects were investigated by assessing the reproductive performance of adult hoverflies, originating from the surviving larvae. Of the five compounds tested, only pirimicarb caused 100% larval mortality. The corrected mortality for spinosad was 60% and the adults obtained from the surviving larvae did not succeed in laying eggs. Therefore, pirimicarb and spinosad were rated “harmful” (International Organization for Biological and Integrated Control of Noxious Animals and Plants (IOBC) category 4) for the larvae of E. balteatus. In contrast, flonicamid, thiacloprid and spirotetramat yielded much lower mortality percentages. The hatching rate of hoverfly eggs treated with flonicamid was 25.6% vs 48.7% in the control. Hence, flonicamid was rated “slightly harmful” (IOBC category 2). The fertility of adults treated as larvae with thiacloprid or spirotetramat was not affected (IOBC category 1). These laboratory trials suggest that thiacloprid and spirotetramat can be used safely in integrated pest management programs to control the cabbage aphid. Pirimicarb, spinosad and flonicamid should be tested in semi-field and field situations to assess their toxicity under more realistic conditions.

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References

  1. Abbott, W. S. (1925). A method of computing the effectiveness of an insecticide. Journal of Economic Entomology, 18, 265–267.

    CAS  Google Scholar 

  2. Almohamad, R., Verheggen, F., Francis, F., & Haubruge, E. (2007). How does the age of hoverfly females affect their reproduction? Communications in Agricultural and Applied Biological Sciences, Ghent University, 72, 503–508.

    Google Scholar 

  3. Ambrosino, M. D., Jepson, P. C., & Luna, J. M. (2007). Hoverfly oviposition response to aphids in broccoli fields. Entomologia Experimentalis et Applicata, 122, 99–107.

    Article  Google Scholar 

  4. Angeli, G., Baldessari, M., Maines, R., & Duso, C. (2005). Side-effects of pesticides on the predatory bug Orius laevigatus (Heteroptera: Anthocoridae) in the laboratory. Biocontrol Science and Technology, 15, 745–75.

    Article  Google Scholar 

  5. Ankersmit, G. W., Dijkman, H., Keuning, N. J., Mertens, H., Sins, A., & Tacoma, H. M. (1986). Episyrphus balteatus as a predator of the aphid Sitobion avenae on winter wheat. Entomologia Experimentalis et Applicata, 42, 271–277.

    Article  Google Scholar 

  6. Bacci, L., Picanco, M. C., Rosado, J. F., Silva, G. A., Crespo, A. L. B., Pereira, E. J. G., et al. (2009). Conservation of natural enemies in brassica crops: Comparative selectivity of insecticides in the management of Brevicoryne brassicae (Hemiptera: Sternorrhyncha: Aphididae). Applied Entomology and Zoology, 44, 103–113.

    CAS  Article  Google Scholar 

  7. Branquart, E., & Hemptinne, J. L. (2000). Development of ovaries, allometry of reproductive traits and fecundity of Episyrphus balteatus (Diptera: Syrphidae). European Journal of Entomology, 97, 165–170.

    Google Scholar 

  8. Brück, E., Elbert, A., Fischer, R., Krueger, S., Kuhnhold, J., Klueken, A. M., et al. (2009). Movento®, an innovative ambimobile insecticide for sucking insect pest control in agriculture: Biological profile and field performance. Crop Protection, 28, 838–844.

    Article  Google Scholar 

  9. Cabral, S., Garcia, P., & Soares, A. O. (2008). Effects of pirimicarb, buprofezin and pymetrozine on survival, development and reproduction of Coccinella undecimpunctata (Coleoptera: Coccinellidae). Biocontrol Science and Technology, 18, 307–318.

    Article  Google Scholar 

  10. Cloyd, R. A., & Dickinson, A. (2006). Effect of insecticides on mealybug destroyer (Coleoptera: Coccinellidae) and parasitoid Leptomastix dactylopii (Hymenoptera: Encyrtidae), natural enemies of citrus mealybug (Homoptera: Pseudococcidae). Journal of Economic Entomology, 99, 1596–1604.

    CAS  Article  PubMed  Google Scholar 

  11. Cloyd, R. A., Timmons, N. R., Goebel, J. M., & Kemp, K. E. (2009). Effect of pesticides on adult rove beetle Atheta coriaria (Coleoptera: Staphylinidae) survival in growing medium. Journal of Economic Entomology, 102, 1750–1758.

    CAS  Article  PubMed  Google Scholar 

  12. Colignon, P., Haubruge, E., Gaspar, C., & Francis, F. (2003). Effets de la reduction de doses de formulations d’insecticides et de fongicides sur l’insecte auxiliaire non ciblé Episyrphus balteatus (Diptera: Syrphidae). Phytoprotection, 84, 141–148.

    CAS  Google Scholar 

  13. Cordero, R. J., Bloomquist, J. R., & Kuhar, T. P. (2007). Susceptibility of two diamondback moth parasitoids, Diadegma insulare (Cresson) (Hymenoptera; Ichneumonidae) and Oomyzus sokolowskii (Kurdjumov) (Hymenoptera; Eulophidae), to selected commercial insecticides. Biological Control, 42, 48–54.

    CAS  Article  Google Scholar 

  14. Costello, M. J., & Altieri, M. A. (1995). Abundance, growth-rate and parasitism of Brevicoryne brassicae and Myzus persicae (Homoptera, Aphididae) on broccoli grown in living mulches. Agriculture Ecosystems & Environment, 52, 187–196.

    Article  Google Scholar 

  15. Elbert, A., Ebbinghaus, D., Maeyer, L. D., Nauen, R., Comparini, S., & Pittá, L. (2002). Calypso, a new foliar insecticide for berry fruit. Proceedings of the Eighth International Symposium on Rubus and Ribes (Dundee, Scotland), pp. 337–341.

  16. Galvan, T. L., Koch, R. L., & Hutchison, W. D. (2005). Toxicity of commonly used insecticides in sweet corn and soybean to multicolored Asian lady beetle (Coleoptera: Coccinellidae). Journal of Economic Entomology, 98, 780–789.

    CAS  Article  PubMed  Google Scholar 

  17. Geusen-Pfister, H. (1987). Studies on the biology and reproductive capacity of Episyrphus balteatus Deg (Dipt, Syriphidae) under greenhouse conditions. Journal of Applied Entomology—Zeitschrift für Angewandte Entomologie, 104, 261–270.

    Google Scholar 

  18. Godoy, M. S., Carvalho, G. A., Moraes, J. C., Júnior, M. G., Morais, A. A., & Cosme, L. V. (2004). Selectivity of insecticides used in citrus crops to eggs and larvae of Chrysoperla externa (Hagen) (Neuroptera: Chrysopidae). Neotropical Entomology, 33, 639–646.

    CAS  Google Scholar 

  19. Haseeb, M., Amano, H., & Nemoto, H. (2000). Pesticidal effects on mortality and parasitism rates of Diadegma semiclausum, a parasitoid of the diamondback moth. Biocontrol, 45, 165–178.

    CAS  Article  Google Scholar 

  20. Hassan, S. A. (1992). Meeting of the working group “Pesticides and beneficial organisms”, University of Southampton, UK, September 1991. IOBC/WPRS Bulletin, 15(3), 1–3.

    Google Scholar 

  21. Ishaaya, I., Barazani, A., Kontsedalov, S., & Horowitz, A. R. (2007). Insecticides with novel modes of action: Mechanism, selectivity and cross-resistance. Entomological Research, 37, 148–152.

    Article  Google Scholar 

  22. Jalali, M. A., Van Leeuwen, T., Tirry, L., & De Clercq, P. (2009). Toxicity of selected insecticides to the two-spot ladybird Adalia bipunctata. Phytoparasitica, 37, 323–326.

    CAS  Article  Google Scholar 

  23. Jansen, J. P. (1998). Side effects of insecticides on larvae of the aphid specific predator Episyrphus balteatus (Degeer) (Dipt. Syrphidae) in the laboratory. Mededelingen Faculteit Landbouwwetenschappen Universiteit Gent, 63, 585–592.

    CAS  Google Scholar 

  24. Jansen, J. P. (2000). A three-year field study on the short-term effects of insecticides used to control cereal aphids on plant-dwelling aphid predators in winter wheat. Pest Management Science, 56, 533–539.

    CAS  Article  Google Scholar 

  25. Liu, S. S., Hommes, M., & Hildenhagen, R. (1994). Damage to white cabbage by the aphid Brevicoryne brassicae (L.): Influence of aphid density and stage of plant growth. IOBC/WPRS Bulletin, 17, 75–89.

    CAS  Google Scholar 

  26. Mahdian, K., Van Leeuwen, T., Tirry, L., & De Clercq, P. (2007). Susceptibility of the predatory stinkbug Picromerus bidens to selected insecticides. Biocontrol, 52, 765–774.

    CAS  Article  Google Scholar 

  27. Mandour, N. S. (2009). Influence of spinosad on immature and adult stages of Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). Biocontrol, 54, 93–102.

    CAS  Article  Google Scholar 

  28. Medina, P., Budia, F., Tirry, L., Smagghe, G., & Vinuela, E. (2001). Compatibility of spinosad, tebufenozide and azadirachtin with eggs and pupae of the predator Chrysoperla carnea (Stephens) under laboratory conditions. Biocontrol Science and Technology, 11, 597–610.

    Article  Google Scholar 

  29. Miles, M., & Dutton, R. (2000). Spinosad: A naturally derived insect control agent with potential use in glasshouse integrated pest management systems. Mededelingen Faculteit Landbouwwetenschappen Universiteit Gent, 65, 393–400.

    CAS  Google Scholar 

  30. Morita, M., Ueda, T., Yoneda, T., Koyanagi, T., & Haga, T. (2007). Flonicamid, a novel insecticide with a rapid inhibitory effect on aphid feeding. Pest Management Science, 63, 969–973.

    CAS  Article  PubMed  Google Scholar 

  31. Nasreen, A., Mustafa, G., & Ashfaq, M. (2003). Selectivity of some insecticides to Chrysoperla carnea (Stephen) (Neuroptera: Chrysopidae) in laboratory. Pakistan Journal of Biological Sciences, 6, 536–538.

    Article  Google Scholar 

  32. Nauen, R., Reckmann, U., Thomzik, J., & Thielert, W. (2008). Biological profile of spirotetramat (Movento®)—a new two-way systemic (ambimobile) insecticide against sucking pest species. Bayer CropScience Journal, 61, 245–278.

    CAS  Google Scholar 

  33. Niehoff, B., & Poehling, H. M. (1995). Population dynamics of aphids and syrphid larvae in winter-wheat treated with different rates of pirimicarb. Agriculture Ecosystems & Environment, 52, 51–55.

    Article  Google Scholar 

  34. Overmeer, W. P. J., & Vanzon, A. Q. (1982). A standardized method for testing the side effects of pesticides on the predacious mite, Amblyseius potentillae [Acarina, Phytoseiidae]. Entomophaga, 27, 357–363.

    CAS  Article  Google Scholar 

  35. Rosell, G., Quero, C., Coll, J., & Guerrero, A. (2008). Biorational insecticides in pest management. Journal of Pesticide Science, 33, 103–121.

    CAS  Article  Google Scholar 

  36. Salgado, V. L. (1998). Studies on the mode of action of spinosad: Insect symptoms and physiological correlates. Pesticide Biochemistry and Physiology, 60, 91–102.

    CAS  Article  Google Scholar 

  37. Schnorbach, J., Elbert, A., Laborie, B., Navacerrada, J., Bangels, E., & Gobin, B. (2008). Movento®, an ideal tool for integrated pest management in pomefruit, citrus and vegetables. Bayer CropScience Journal, 61, 377–402.

    CAS  Google Scholar 

  38. Smith, H. A., Chaney, W. E., & Bensen, T. A. (2008). Role of syrphid larvae and other predators in suppressing aphid infestations in organic lettuce on California’s Central Coast. Journal of Economic Entomology, 101, 1526–1532.

    Article  PubMed  Google Scholar 

  39. SPSS Inc. (2006). SPSS 15.0 for Windows. Chicago, IL, USA.

  40. Tenhumberg, B., & Poehling, H. M. (1995). Syrphids as natural enemies of cereal aphids in Germany—aspects of their biology and efficacy in different years and regions. Agriculture Ecosystems & Environment, 52, 39–43.

    Article  Google Scholar 

  41. Tomizawa, M., & Casida, J. E. (2005). Neonicotinoid insecticide toxicology: Mechanisms of selective action. Annual Review of Pharmacology and Toxicology, 45, 247–268.

    CAS  Article  PubMed  Google Scholar 

  42. Tomlin, C. D. S. (Ed.). (1994). The pesticide manual. Farnham, UK: British Crop Protection Council.

    Google Scholar 

  43. Vanhaelen, N., Gaspar, C., & Francis, F. (2002). Influence of prey host plant on a generalist aphidophagous predator: Episyrphus balteatus (Diptera: Syrphidae). European Journal of Entomology, 99, 561–564.

    Google Scholar 

  44. Vanlaecke, K., & Degheele, D. (1993). Effect of insecticide synergist combinations on the survival of Spodoptera exigua. Pesticide Science, 37, 283–288.

    CAS  Article  Google Scholar 

  45. van Rijn, P. C. J., & Smit, J. T. (2007). Zweefvliegen (diptera: Syrphidae) voor de natuurlijke bestrijding van bladluizen. Entomologische Berichten, 67, 253–256.

    Google Scholar 

  46. Viñuela, E., Medina, M. P., Schneider, M., González, M., Budia, F., Adán, A., et al. (2001). Comparison of side-effects of spinosad, tebufenozide and azadirachtin on the predators Chrysoperla carnea and Podisus maculiventris and the parasitoids Opius concolor and Hyposoter didymator under laboratory conditions. Pesticides and Beneficial Organisms IOBC/WPRS Bulletin, 24(4), 25–34.

    Google Scholar 

  47. Youn, Y. N., Seo, M. J., Shin, J. G., Jang, C., & Yu, Y. M. (2003). Toxicity of greenhouse pesticides to multicolored Asian lady beetles, Harmonia axyridis (Coleoptera: Coccinellidae). Biological Control, 28, 164–170.

    CAS  Article  Google Scholar 

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Acknowledgments

The authors thank Leen Dierick for technical assistance and the Institute for the Promotion of Innovation by Science and Technology in Flanders (IWT-project S-050623) for financial support.

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Correspondence to Luc Tirry.

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Moens, J., De Clercq, P. & Tirry, L. Side effects of pesticides on the larvae of the hoverfly Episyrphus balteatus in the laboratory. Phytoparasitica 39, 1–9 (2011). https://doi.org/10.1007/s12600-010-0127-3

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Keywords

  • Brevicoryne brassicae
  • Flonicamid
  • Pirimicarb
  • Spinosad
  • Spirotetramat
  • Thiacloprid