Side effects of different pesticides used in citrus on the adult stage of the parasitoid Aphytis melinus DeBach (Hymenoptera Aphelinidae) and its progeny

J. E. Gonzalez-Zamora, M. L. Castillo, C. Avilla


Twelve pesticides commonly used in citrus in Spain were tested on adults of Aphytis melinus DeBach to determine their effects on parasitoid survival and fecundity, and the duration of the residue of each pesticide. Six of these pesticides were found to be harmless to moderately harmful to this parasitoid in a laboratory assay in closed Petri dishes: spinosad (bait formulation), azadirachtin, fenbutatin, fosetyl-Al, copper oxichloride, and mancozeb, with their scores on the reduction of beneficial capacity (RBC) index being between 21.4 and 94.6% after one week. The other six pesticides classified as harmful were tested on citrus plants to study their persistence over time under greenhouse conditions: Pirimicarb, pyriproxifen, paraffinic oil, abamectin, chlorpyrifos, and lambda-cyhalothrin. Most of these products reduced their negative effect on adults of A. melinus between one and six weeks after treatment, although lambda-cyhalothrin was still harmful to parasitoids 11 weeks after application. This information can help growers and consultants to make decisions about pesticide selection and application timing in citrus in order to support IPM implementation when A. melinus is present.


mortality; fecundity; persistence; IPM; parasitism

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Abbott WS, 1925. A method of computing the effectiveness of an insecticide. J Econ Entomol 18: 265-267. 

Barret KI, Grandy N, Harrison EG, Hassan S, Oomen P, 1994. Guidance document on regulatory testing procedures for pesticides with non-target arthropods. SETAC-EUROPE, UK. 51 pp.

Bellows TS, Morse JG, 1993. Toxicity of insecticides used in citrus to Aphytis melinus Debach (Hymenoptera, Aphelinidae) and Rhizobius lophanthae (Blaisd) (Coleoptera, Coccinellidae). Can Entomol 125(6): 987-994. 

Bellows TS, Morse JG, Gaston LK, 1993. Residual toxicity of pesticides used for lepidopteran insect control on citrus to Aphytis melinus Debach (Hymenoptera, Aphelinidae). Can Entomol 125(6): 995-1001. 

Biobest, 2011. Side-effects manual. Available in [15 December 2011].


Boller EF, Vogt H, Ternes P, Malavolta C, 2005. Working document on selectivity of pesticides. IOBC/wprs: 1-9. Available in [10 December 2011].


Campos JM, Martinez Ferrer MT, Forés V, 2008. Secondary effects of seven pesticides on Anagyrus pseudococci (Girault) and Leptomastix dactylopii Howard (Hymenoptera: Encyrtidae), parasitoids of Planoccocus citri (Risso) (Hemiptera: Pseudococcidae). IOBC/wprs Bull 38: 111-116. 

DeBach P, White EB, 1960. Commercial mass culture of the California red scale parasite. Calif Agric Expt Sta Bull 770: 4-58. 

Demchak RJ, Dybas RA, 1997. Photostability of Abamectin/Zein microspheres. J Agric Food Chem 45(1): 260-262. 

Dominguez J, Pina T, Verdú MJ, 2003. Effects of the mineral oil Sunspray UltrafineR on California red scale parasitoids Aphytis chrysomphali, A. lingnanensis, Comperiella bifasciata and Encarsia perniciosi. IOBC/wprs Bull 26(6): 117. 

European Union, 2011. Eur-Lex web page. Available in [07 July 2011].


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): 335-346. 

Grafton-Cardwell EE, Reagan CA, 1995. Selective use of insecticides for control of armored scale (Homoptera, Diaspididae) in San Joaquin valley California citrus. J Econ Entomol 88(6): 1717-1725. 

Grafton-Cardwell EE, Lee JE, Stewart JR, Olsen KD, 2006. Role of two insect growth regulators in integrated pest management of citrus scales. J Econ Entomol 99(3): 733-744.

Grafton-Cardwell EE, Lee JE, Robillard SM, Gorden JM, 2008. Role of imidacloprid in integrated pest management of California citrus. J Econ Entomol 101(2): 451-460.[451:ROIIIP]2.0.CO;2 

Grafton-Cardwell EE, Morse JG, O'Connell NV, Phillips PA, Kallsen CE, Haviland DR, 2011. UC Pest management guidelines, citrus: California red scale and yellow scale. Available in [07 December 2011].


Hassan SA, Bigler F, Bogenschütz H, Boller E, Brun J, Calis JNM, Coremans-Pelseneer J, Duso C, Grove A, Heimbach U et al., 1994. Results of the sixth joint pesticide testing programme of the IOBC/wprs-working group ''Pesticides and beneficial organisms''. Entomophaga 39: 107-119. 

IVIA, 2012. Gestión integrada de plagas de cítricos. Instituto Valenciano de Investigaciones Agrarias, Moncada (Valencia). Available in [17 January 2012].


Jacas JA, Urbaneja A, 2010. Biological control in citrus in Spain: from classical to conservation biological control. In: Integrated management of arthropod pests and insect borne diseases (Ciancio A, Mukerji KG, eds.). Springer Science+Business Media B.V., Dordrecht (Netherland). pp: 61-72.


Jacas JA, Urbaneja A, Vi-uela E, 2006. History and future of introduction of exotic arthropod biological control agents in Spain: a dilemma? BioControl 51: 1-30. 

Jacas JA, Karamaouna F, Vercher R, Zappalà L, 2010. Citrus pest management in the northern mediterranean basin (Spain, Italy and Greece). In: Integrated management of arthropods pests and insect borne diseases (Ciancio A, Mukerji KG, eds.). Springer Science+Business Media B.V., Dordrecht (Netherland), pp: 3-27.


Kennett CE, McMurtry JA, Beardsley JW, 1999. Biological control in tropical and subtropical crops. In: Handbook of biological control (Bellows TS, Fisher TW, eds.). Academic Press, San Diego, CA, USA. pp: 713-742. 

Koppert Biological Systems, 2011. Side effects. Available in [15 December 2011].


Liang W, Meats A, Beattie GAC, Spooner-Hart R, Jiang L, 2010. Conservation of natural enemy fauna in citrus canopies by horticultural mineral oil: Comparison with effects of carbaryl and methidathion treatments for control of armored scales. Insect Sci 17(5): 414-426. 

Mazih A, 2008. Current situation of citrus pests and the control methods in use in Morocco. IOBC/wprs Bull 38: 10-16. 

Michaud JP, 2003. Toxicity of fruit fly baits to beneficial insects in citrus. J Insect Sci 3(8): 1-9. 

Morse JG, Bellows TSJ, Gaston LK, Iwata Y, 1987. Residual toxicity of acaricides to three beneficial species on California citrus. J Econ Entomol 80(4): 953-960. 

Olivas J, Lucas A, Calvo J, Belda JE, 2011. Biological control of diaspidid scales Aspidiotus nerii Bouche and Aonidiella aurantii (Maskell) by means of commercial Aphytis melinus DeBach (Hym., Aphelinidae) releases: basis for an IPM strategy in Spanish citrus. IOBC/wprs Bull 62: 311-316. 

Overmeer WP, van Zon AQ, 1982. A standardised method for testing the side effects of pesticides on the predacious mite Amblyseius potentillae Garman (Acarina: Phytoseiidae). Entomophaga 27: 357-364. 

Pina T, Verdú MJ, 2007. Establecimiento y dispersión de Aphytis melinus y A. lingnanensis (Hym.: Aphelinidae), dos parasitoides introducidos para el control de Chrysomphalus dictyospermi Morgan y Aonidiella aurantii (Maskell) (Hem.: Diaspididae) en cítricos de la Comunidad Valenciana. Bol San Veg -Plagas 33(3): 311-320.


Prabhaker N, Morse JG, Castle SJ, Naranjo SE, Henneberry TJ, Toscano NC, 2007. Toxicity of seven foliar insecticides to four insect parasitoids attacking citrus and cotton pests. J Econ Entomol 100(4): 1053-1061.[1053:TOSFIT]2.0.CO;2 

Prabhaker N, Castle SJ, Naranjo SE, Toscano NC, Morse JG, 2011. Compatibility of two systemic neonicotinoids, imidacloprid and thiamethoxam, with various natural enemies of agricultural pests. J Econ Entomol 104: 773-781.

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): 125-134. 

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(4): 579-587. 

Rose M, 1990. Rearing and mass rearing. In: Armored scale insects. Their biology, natural enemies and control (Rosen D. ed.). Elsevier, Jerusalen (Israel), pp: 357-365.


Sorribas JJ, García-Marí F, 2010. Comparative efficacy of different combinations of natural enemies for the biological control of California red scale in citrus groves. Biol Control 55(1): 42-48. 

Sorribas JJ, Rodriguez R, Rodrigo E, García-Marí F, 2008. Parasitism levels and species of natural enemies in field populations of California red scale Aonidiella aurantii (Hemiptera: Diaspididae) in Eastern Spain. IOBC/wprs Bull 38: 26-33. 

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(4): 1027-1032.[1027:IERMOP]2.0.CO;2 

Stat Point Technologies, 2010. Statgraphics Centurion XVI. 16.1.07. Warrenton, VA (USA). 

Sterk G, Hasssan SA, Baillod M, Bakker F, Bigler F, Blümel S, Bogenschütz H, Boller E, Bromand B, Brun J et al., 1999. Results of the seventh joint pesticide testing programme carried out by the IOBC/wprs-Working Group 'Pesticides and Beneficial Organisms'. Biocontrol 44: 99-117. 

Suma P, Zappalà L, Mazzeo G, Siscaro G, 2009. Lethal and sub-lethal effects of insecticides on natural enemies of citrus scale pests. Biocontrol 54(5): 651-661. 

Thomas DB, Mangan RL, 2005. Nontarget impact of spinosad GF-120 bait sprays for control of the Mexican fruit fly (Diptera : Tephritidae) in Texas citrus. J Econ Entomol 98(6): 1950-1956.

Urbaneja A, Dembilio O, Pascual S, Vi-uela E, Casta-era P, 2006. Side effects on natural enemies of bait insecticide applications for the control of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). IOBC/wprs Bull 29(3): 215. 

Van de Veire M, Vi-uela E, Bernardo U, Tirry L, Adan A, Viggiani G, 2004. Duration of the toxicity of abamectin and spinosad on the parasitic wasp Encarsia formosa Gahan in Northern and Southern Europe. IOBC/wprs Bull 27: 21-30. 

Vanaclocha P, Vidal-Quist C, Oheix S, Montón H, Planes L, Catalán J, Tena A, Verdú MJ, Urbaneja A, 2012. Acute toxicity in laboratory tests of fresh and aged residues of pesticides used in citrus on the parasitoid Aphytis melinus. J Pest Sci: [DOI 10.1007/s10340-012-0448-8]. 

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: 49-54. 

Zappalà L, Biondi A, Siscaro G, 2011. Side effects of pesticides on Aphytis melinus DeBach adults and young instars. IOBC/wprs Bull 62: 317-323.

DOI: 10.5424/sjar/2013112-3556