, Volume 54, Issue 5, pp 651–661 | Cite as

Lethal and sub-lethal effects of insecticides on natural enemies of citrus scale pests

  • Pompeo SumaEmail author
  • Lucia Zappalà
  • Gaetana Mazzeo
  • Gaetano Siscaro
Forum paper


Laboratory trials were conducted to test the side-effects of the insecticides chlorpyrifos-methyl, buprofezin, pyriproxifen, spinosad and a narrow range mineral oil on Aphytis melinus DeBach, Coccophagus lycimnia Walker (Hymenoptera: Aphelinidae) and Leptomastix dactylopii Howard (Hymenoptera: Encyrtidae). The effects of chlorpyrifos-methyl, spinosad and pyriproxifen were also investigated in semi-field conditions on L. dactylopii. Contact toxicity on adult female parasitoids after 24, 48 and 72 h, the effects on their fertility as well as the sex ratio of the progeny were measured. In the laboratory trials chlorpyrifos-methyl and spinosad caused 100% mortality on all tested parasitoids just 24 h after the treatment. According to the IOBC classification, the mineral oil was slightly harmful on L. dactylopii; buprofezin was harmful on C. lycimnia, and slightly harmful on L. dactylopii and A. melinus; pyriproxifen resulted moderately harmful on C. lycimnia and slightly harmful on L. dactylopii and A. melinus. The progeny production of each L. dactylopii surviving female treated with buprofezin was not affected by the treatment while in the case of A. melinus it was significantly reduced. C. lycimnia females treated with pyriproxifen did not produce any progeny. In semi-field conditions the tested insecticides were less harmful to L. dactylopii adults but, although none of them influenced the progeny production of the survived females, the longevity was negatively affected.


Side-effects Hymenoptera parasitoids Semi-field Aphytis melinus Coccophagus lycimnia Leptomastix dactylopii 



The authors are very grateful to two anonymous reviewers for most valuable comments improving the manuscript considerably.


  1. Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267Google Scholar
  2. Abd-Rabou S (2001) Biological control of Mediterranean scale Saissetia oleae (Oliver) (Hemiptera: Coccidae) on olive in Egypt. Boll Zool Agr Bachic 33(3):483Google Scholar
  3. Banken JAO, Stark JD (1998) Multiple routes of pesticide exposure and the risk of pesticides to biological control: a study of neem and the sevenspotted lady beetle (Coleoptera: Coccinellidae). J Econ Entomol 91:1–6Google Scholar
  4. Barbagallo S, Longo S, Mineo G (1992) Integrated control of Citrus pest in Italy. Proceedings 7th international citrus congress: 978–984Google Scholar
  5. Bartlett BR (1964) Integration of chemical and biological control. In: DeBach P (ed) Biological control of insect pests and weeds. Chapman & Hall Ltd., London, pp 489–511Google Scholar
  6. Bernal JS, Luck RF, Morse JG (1998) Sex ratios in field populations of two parasitoids (Hymenoptera: Chalcidoidea) of Coccus hesperidum L. (Homoptera: Coccidae). Oecologia 116:510–518CrossRefGoogle Scholar
  7. Bernal JS, Luck RF, Morse JG, Drury MS (2001) Seasonal and scale size relationships between Citricola scale (Homoptera: Coccidae) and its parasitoids complex (Hymenoptera: Chalcidoidea) on San Joaquin Valley citrus. Biol Control 20:210–221CrossRefGoogle Scholar
  8. Boller EF, Vogt H, Ternes P, Malavolta C (2005) Working document on selectivity of pesticides. Available at Accessed May 2008
  9. Copping LG, Menn JJ (2000) Biopesticides: a review of their action, applications and efficacy. Pest Manag Sci 56:651–676CrossRefGoogle Scholar
  10. Davies RAH, McLaren IW (1977) Tolerance of Aphytis melinus DeBach (Hymenoptera: Aphelinidae) to 20 orchard chemical treatments in relation to integrated control of red scale, Aonidiella aurantii (Maskell) (Homoptera: Diaspididae). Aust J Exp Agric Anim Husb 17:323–328CrossRefGoogle Scholar
  11. Delaplane KS (2000) Pesticide usage in the United States: history, benefits, risks, and trends. Cooperative Extension Service/The University of Georgia College of Agricultural and Environmental Sciences. Bulletin 1121. Available at Accessed Dec 2008
  12. Franco JC, Suma P, Silva EB, Blumberg D, Mendel Z (2004) Management strategies of mealybug pests of citrus in Mediterranean countries. Phytoparasitica 32:507–522CrossRefGoogle Scholar
  13. Franco JC, García-Marí F, Ramos AP, Besri M (2006) Survey on the situation of citrus pest management in Mediterranean countries. IOBC/WPRS Bull 29(3):335–346Google Scholar
  14. Grafton-Cardwell EE, Gu P (2003) Conserving vedalia beetle, Rodolia cardinalis (Mulsant) (Coleoptera: Coccinellidae), in citrus: a continuing challenge as new insecticides gain registration. J Econ Entomol 96:1388–1398PubMedCrossRefGoogle Scholar
  15. Grafton-Cardwell EE, Reagan CA (1995) Selective use of insecticides for control of armoured scale (Homoptera: Diaspididae) in San Joaquin Valley California citrus. J Econ Entomol 88:1717–1725Google Scholar
  16. Haseeb M, Liu TX, Jones WA (2004) Effects of selected insecticides on Cotesia plutellae, endoparasitoid of Plutella xylostella. BioControl 49:33–46CrossRefGoogle Scholar
  17. Hassan E (1997) Chlorpyrifos toxicity to Aphytis lingnanensis Compere (Hymenoptera: Aphelinidae) a parasitoid of California red scale, Aonidiella aurantii (Mask.) in citrus. Z Pflanzenk Pflanzen 104:102–104Google Scholar
  18. Hassan SA, Bigler F, Bogenschütz H, Boller E, Brun J, Calis JNM, Coremans-Pelseneer J, Duso C, Grove A, Heimbach U, Helyer N, Hokkanen H, Lewis GB, Mansour F, Moreth L, Polgar L, Samsøe-Petersen L, Sauphanor B, Stäubli A, Sterk G, Vainio A, van de Viere M, Viggiani G, Vogt H (1994) Results of the sixth joint pesticide testing programme of the IOBC/WPRS-working group “Pesticides and beneficial organisms”. Entomophaga 39:107–119CrossRefGoogle Scholar
  19. Hoy MA (2000) Conceptual framework for assessing non-target effects of pesticides on arthropod natural enemies. Proceedings international social citricult IX congress: 792–794Google Scholar
  20. Huffaker CB, Messenger PS, DeBach P (1971) The natural enemy component in natural control and the theory of biological control. In: Huffaker CB (ed) Biological control. Plenum Press, New York, pp 16–67Google Scholar
  21. Ishaaya I, Degheele D (eds) (1998) Insecticides with novel modes of action. Springer, BerlinGoogle Scholar
  22. Jacas Miret JA, Garcia-Marí F (2001) Side-effects of pesticides on selected natural enemies occurring in citrus in Spain. IOBC/WPRS Bull 24(4):103–112Google Scholar
  23. James DG (2004) Effect of Buprofezin on survival of immature stages of Harmonia axyridis, Stethorus punctum picipes (Coleoptera: Coccinellidae), Orius tristicolor (Hemiptera: Anthocoridae), and Geocoris spp. (Hemiptera: Geocoridae). J Econ Entomol 97:900–904PubMedCrossRefGoogle Scholar
  24. James JR, Tweedy BG, Newby LC (1993) Efforts by industry to improve the environmental safety of pesticides. Annu Rev Phytopathol 31:423–439CrossRefGoogle Scholar
  25. Kumar P, Whitten M, Thoeming G, Borgemeister C, Poehling HM (2008) Effects of bio-pesticides on Eretmocerus warrae (Hym., Aphelinidae), a parasitoid of Bemisia tabaci (Hom. Aleyrodidae). J Appl Entomol 132:605–613CrossRefGoogle Scholar
  26. Lizzio S, Siscaro G, Longo S (1998) Analisi dei principali fattori di mortalità di Aonidiella aurantii (Maskell) in agrumeti della Sicilia. Boll Zool Agr Bachic Ser II 30(2):165–183Google Scholar
  27. Mazzeo G, Benfatto D, Palmeri V, Scazziotta B (2004) Risultati di un triennio di prove di lotta biologica contro Aonidiella aurantii con lanci aumentativi di Aphytis melinus. Tecnica Agricola LVI 1–2:19–33Google Scholar
  28. Mendel Z, Blumberg D, Ishaaya I (1994) Effects of some insect growth-regulators on natural enemies of scale insects (Hom, Coccoidea). Entomophaga 39:199–209CrossRefGoogle Scholar
  29. Michaud JP (2003) Toxicity of fruit fly baits to beneficial insects in citrus. J Insect Sci 3.8: 9 pp. Available online: Accessed April 2008
  30. Michaud JP, Grant AK (2003) IPM-compatibility of foliar insecticides for citrus: Indices derived from toxicity to beneficial insects from four orders. J Insect Sci 3.18: 10 pp. Available online: Accessed Nov 2008
  31. Morse JG, Bellows TS Jr (1986) Toxicity of major citrus pesticides to Aphytis melinus Hymenoptera Aphelinidae and Cryptolaemus montrouzieri Coleoptera Coccinellidae. J Econ Entomol 79:311–314Google Scholar
  32. Peleg BA (1983) Effect of 3 insect growth regulators on larval development, fecundity and egg viability of the coccinellid Chilocorus bipustulatus (Col. Coccinellidae). Entomophaga 28:117–121CrossRefGoogle Scholar
  33. Raciti E, Saraceno F, Siscaro G (2003) Mass rearing of Aphytis melinus for biological control of Aonidiella aurantii in Sicily. IOBC/WPRS Bull 26(6):125–134Google Scholar
  34. Rill SM, Grafton-Cardwell EE, Morse JG (2008) Effects of two insect growth regulators and a neonicotinoid on various life stages of Aphytis melinus (Hymenoptera: Aphelinidae). BioControl 53:579–587CrossRefGoogle Scholar
  35. Schmutterer H (1990) Properties and potential of natural pesticides from the Neem tree, Azadirachta indica. Annu Rev Entomol 35:271–297PubMedCrossRefGoogle Scholar
  36. Schneider M, Smagghe G, Pineda S, Viñuela E (2004) Action of insect growth regulator insecticides and spinosad on life history parameters and absorption in third-instar larvae of the endoparasitoid Hyposoter didymator. Biol Control 31:189–198CrossRefGoogle Scholar
  37. SCOPE (Scientific Committee on Problems of the Environment) (1992) Methods to assess adverse effects of pesticides on non-target organisms, SCOPE 49. Wiley, UKGoogle Scholar
  38. Siscaro G, Mazzeo G (2003) El piojo rojo de California, Aonidiella aurantii, en Italia. Metodos de control. Proc 14th Int Symp “Healthy Citruses: Citrus crop protection in the Mediterranean Basin”. Phytoma España 153:124–126Google Scholar
  39. Staal GB (1975) Insect growth regulators with juvenile hormone activity. Annu Rev Entomol 20:417–460PubMedCrossRefGoogle Scholar
  40. Stark JD, Banks JE (2003) Population-level effects of pesticides and other toxicants on arthropods. Annu Rev Entomol 48:505–519PubMedCrossRefGoogle Scholar
  41. Stark JD, Banks JE, Acheampong S (2004) Estimating susceptibility of biological control agents to pesticides: influence of life history strategies and population structure. Biol Control 29:392–398CrossRefGoogle Scholar
  42. Stark JD, Vargas R, Banks JE (2007) Incorporating ecologically relevant measures of pesticide effect for estimating the compatibility of pesticides and biocontrol agents. J Econ Entomol 100:1027–1032PubMedCrossRefGoogle Scholar
  43. Statsoft Inc (2003) Statistica (data analysis software system) version 6. StatSoft, Inc., Tulsa, Oklahoma.
  44. Sterk G, Hasssan SA, Baillod M, Bakker F, Bigler F, Blümel S, Bogenschütz H, Boller E, Bromand B, Brun J, Calis JNM, Coremans-Pelseneer J, Duso C, Garrido A, Grove A, Heimbach U, Hokkanen H, Jacas J, Lewis GB, Moreth L, Polgar L, Roversti L, Samsøe-Petersen L, Sauphanor B, Schaub L, Stäubli A, Tuset JJ, Vainio A, van de Viere M, Viggiani G, Viñuela E, Vogt H (1999) Results of the seventh joint pesticide testing programme carried out by the IOBC/WPRS-Working group “Pesticides and beneficial organisms”. BioControl 44:99–117CrossRefGoogle Scholar
  45. Studebaker GE, Kring TJ (2003) Effects of insecticides on Orius insidiosus (Hemiptera: Anthocoridae), measured by field, greenhouse and petri dish bioassays. Fla Entomol 86:178–185CrossRefGoogle Scholar
  46. Suma P, Mazzeo G (2008) Laboratory evaluation of pesticide secondary effects on Anagyrus sp. nov. near pseudococci, parasitoid of the citrus mealybug Planococcus citri. IOBC/WPRS Bull 38:99–103Google Scholar
  47. Thomson GD, Dutton R, Sparks TC (2000) Spinosad–a case study: an example from a natural products discovery programme. Pest Manag Sci 56:696–702CrossRefGoogle Scholar
  48. Tumminelli R, Conti F, Saraceno F, Raciti E, Lonzi M, Pedrotti C (2000) Aphytis melinus (Hymenoptera: Aphelinidae) augmentation in Eastern Sicily citrus orchards to suppress Aonidiella aurantii (Homoptera: Diaspididae). Proceedings 9th international Citrus Congress: 862–866Google Scholar
  49. Viggiani G, Loia M (1991) I rischi della lotta agli insetti dannosi con i regolatori di crescita. L’Informatore agrario 47(91):67–69Google Scholar
  50. Viggiani G, Tranfaglia A (1978) A method for laboratory test of side effects of pesticides on Leptomastix dactylopii (How.) (Hym. Encyrtidae). Boll Lab Ent Agr Portici 35:8–15Google Scholar
  51. Vogt H (2000a) Concepts and experiences of the IOBC/WPRS Working Group, pesticides and beneficial organisms. Proceedings 9th international Citrus congress: 789–791Google Scholar
  52. Vogt H (2000b) Sensitivity of non-target arthropod species to plant protection products according to laboratory results of the IOBC WG “Pesticides and Beneficial Organisms”. IOBC/WPRS Bull 23(9):3–15Google Scholar
  53. Walter GH (1988) Heteronomous host relationships in aphelinids—evolutionary pathways and adaptive significance (Hymenoptera: Chalcidoidea). Adv Parasit Hymenopt Res 1988:313–326Google Scholar
  54. Wang XG, Jarjees EA, McGraw BK, Bokonon-Ganta AH, Messing RH, Johnson MW (2005) Effects of spinosad-based fruit fly bait GF-120 on tephritid fruit fly and aphid parasitoids. Biol Control 35:155–162CrossRefGoogle Scholar
  55. Ware AB, Hattingh V (2000) The non-target effect of some agrochemical pesticides on the chalcid biocontrol agent Aphytis lingnanensis. Proceedings 9th International Citrus Congress: 808–810Google Scholar
  56. Williams L, Price LD (2004) A space-efficient contact toxicity bioassay for minute Hymenoptera, used to test the effects of novel and conventional insecticides on the egg parasitoids Anaphes iole and Trichogramma pretiosum. BioControl 49:163–185CrossRefGoogle Scholar
  57. Williams T, Valle J, Viñuela E (2003) Is the naturally-derived spinosad® compatible with insect natural enemies? Biocontrol Sci Techn 13:459–475CrossRefGoogle Scholar
  58. WinBDF (2008) Banca dati fitofarmaci, version 2.6.6. Ecospi Srl Milano, Italy (Update: March 2008)Google Scholar
  59. Zappalà L, Campolo O, Saraceno F, Grande SB, Raciti E, Siscaro G, Palmeri V (2008) Augmentative releases of Aphytis melinus (Hymenoptera: Aphelinidae) to control Aonidiella aurantii (Hemiptera: Diaspididae) in Sicilian citrus groves. IOBC/WPRS Bull 38:49–54Google Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2009

Authors and Affiliations

  • Pompeo Suma
    • 1
    Email author
  • Lucia Zappalà
    • 1
  • Gaetana Mazzeo
    • 1
  • Gaetano Siscaro
    • 1
  1. 1.Dipartimento di Scienze e Tecnologie Fitosanitarie, Sezione Entomologia agrariaUniversity of CataniaCataniaItaly

Personalised recommendations