Sublethal effects of imidacloprid on the whitefly parasitoid Encarsia formosa Gahan

  • Tanja Drobnjaković Institute of Pesticides and Environmental Protection, Banatska 31B, 11080, Belgrade
  • Dejan Marčić Institute of Pesticides and Environmental Protection, Banatska 31B, 11080, Belgrade
  • Mirjana Prijović Institute of Pesticides and Environmental Protection, Banatska 31B, 11080, Belgrade
  • Pantelija Perić Institute of Pesticides and Environmental Protection, Banatska 31B, 11080, Belgrade
  • Slobodan Milenković Megatrend University, Faculty of Biofarming, Maršala Tita 39, 24300 Bačka Topola
  • Jelena Bošković Faculty of Economics and Engineering Management, University Business Academy, 21 000 Novi Sad
Keywords: Encarsia formosa, Imidacloprid, Sublethal effects, Life history traits, Population growth,

Abstract


Acute toxicity of an imidacloprid-based product (Confidor 200 SL) to pupae of the whitefly parasitoid Encarsia formosa Gahan (Hymenoptera: Aphelinidae), and its effects on life history traits and population growth in F1 generation of the surviving parasitoid females of a commercial strain (“Dutch” strain, D) and two local populations from Serbia (Bujanovac, B; Negotin, N) were examined in laboratory bioassays. All trials were carried out at 27±1°C temperature and 60±10% relative humidity, and under 16/8 h daylight/darkness photoperiod in four replications. In acute toxicity bioassays, tobacco leaves carrying parasitoid pupae were treated with a series of symmetrical concentrations (800, 400, 200, 100, 50 and 25 mg a.i./l) covering a 10-90% mortality range. The product based on imidacloprid, applied directly onto parasitoid pupae at mean lethal concentrations (LC50) determined in the acute toxicity assays (30 mg/l, 20 mg/l and 25 mg/l, for populations B, N and D,  respectively), significantly affected the survival of females developed from the treated pupae, extended the duration of juvenile development (by 1.81, 1.59 and 1.73 days for populations B, N and D, respectively), significantly reduced total parasitism of females D (25.92 %), total female adult emergence in populations B (27.48 %) and D (17.92 %), and significantly reduced the instantaneous rate of increased only of females N (4.23 %). Considering the high acute toxicity of the imidacloprid product to the pupal stage of E. formosa, and significant reductions in life table and population parameters, imidacloprid is not considered compatible for simultaneous use with the parasitoid E. formosa. A more precise assessment of risks involved in the use of that insecticide requires a more detailed testing in the field. The implications of these results for the concept of  integrated control of the greenhouse whitefly are discussed.

References

Albajes, R., Gullino, M.L., van Lenteren, J.C., & Elad, Y. (1999): Integrated Pest and Disease Management in Greenhouse Crops. Dordrecht, Netherlands: Kluwer Academic Publishers.

Cahill, M., Denholm, I., Byrne, F.J., & Devonshire, A.L. (1996). Insecticide resistance in Bemisia tabaci - current status and implications for management. In Proceedings of Brighton Crop Protection Conference: Pests & Diseases, Volume 1 (pp 75-80). Farnham,UK: BCPC.

Carvalho, S.S. Vendramim, J.D., Pitta, R.M., & Forim, M.R. (2012). Efficiency of neem oil nanoformulations to Bemisia tabaci (Genn.) biotype B (Hemiptera: Aleyrodidae). Semina: Ciencias Agrarias, 33(1), 193-202. doi:10.5433/1679-0359.2012v33n1p193

Croft, B.A. (1990). Arthropod biological control agents and pesticides. New York, NY: JohnWiley.

Drobnjaković, T., Marčić, D., Prijović, M., Perić, P., Milenković, S., & Bošković, J. (2016). Life history traits and population growth of Encarsia formosa Gahan (Hymenoptera: Aphelinidae) local population from Serbia. Entomologia Generalis, 35(4), 281-295. doi: 10.1127/entomologia/2016/0183

Elbert, A., Becker, B., Hartwig, J., & Erdelen, C. (1991). Imidacloprid - a new systemic insecticide. Pflanzenschutz Nachrichten Bayer, 44, 113-116.

Elbert, A., & Nauen, R. (1996). Bioassays for imidacloprid for a resistance monitoring against the whitefly Bemisia tabaci. In Proceedings of Brighton Crop Protection Conference:Pests & Diseases, Volume 2 (pp 731-738). Brighton,UK: BCPC.

Elzen, G.W. (2001). Lethal and sublethal effects of insecticide residues on Orius incidiosusi (Hemiptera: Anthocoridae) and Geocoris punctipes (Hemiptera:Lygaeidae). Journal of Economical Entomology, 94 (1), 55-59. doi:10.1603/0022-0493-94.1.55

Enkegaard, A. (1993). Encarsia formosa parasitizing the Poinsettia-strain of the cotton whitefly, Bemisia tabaci, on Poinsettia: bionomics in relation to temperature. Entomologia Experimentalis et Applicata, 69(3), 251-261. doi: 10.1111/j.1570-7458.1993.tb01748.x

Enkegaard, A., & Brǿdsgaard, H.F. (2006). Biocontrol in protected crops: is lack of biodiversity a limiting factor? In J. Eilenberg & H.M.T. Hokkanen (Eds.), An Ecological and Societal Approach to Biological Control (pp 91-122). Dordrecht, Netherlands: Springer.

EPPO (Europian Plant Protection Organisation) (2004). Side effects on Encarsia formosa. EPPO, Paris, PP1/142(2).

Finney, D.J. (1971): Probit analysis (2nd ed.). Cambridge, UK: Cambridge University Press.

Gentz, M.C., Murdoch, G., & King, G.F. (2010). Tandem use of selective insecticides and natural enemies for effective, reduced-risk pest management. Biological Control, 52(3), 208-215. doi:10.1016/j.biocontrol.2009.07.012

Gerling, D. (1990). Whiteflies: Their bionomics, pest status and management. Andover, UK: Intercept.

Gholamzadeh, M. Ghadamyari, M., Salehi, L., & Hoseininaveh, V. (2012). Effects of amitraz, buprofezin and propargite on some fitness parameters of the parasitoid Encarsia formosa (Hym.:Aphelinidae), using life table and IOBC methods. Journal of Entomological Society of Iran, 31(2), 1-14.

Grafton-Cardwell, E.E., Lee, J.E., Robillard, S.M., & Gorden, J.M. (2008). Role of imidacloprid in integrated pest management of California citrus. Journal of Economic Entomology, 101(2), 451-460. doi: 10.1603/0022-0493

James, D.G. (1997). Imidacloprid increases egg production in Amblyseius victoriensis (Acari: Phytoseiidae). Experimental and Applied Acarology, 21(2), 75-82. doi:10.1023/a:1018493409832

James, D.G., & Price, T.S. (2002). Fecundity in twospotted spider mite (Acari: Tetranychidae) is increased by direct and systemic exposure to imidacloprid. Journal of Economic Entomology, 95(4), 729-732. doi:10.1603/0022-0493-95.4.729

James, D.G., & Vogele, B. (2001). The effect of imidacloprid on survival of some beneficial arthropods. Plant Protection Quarterly, 16(2), 58-62.

Hoddle, M.S., van Driesche, R.G., & Sanderson, J.P. (1998). Biology and use of the whitefly parasitoid Encarsia formosa. Annual Review of Entomology, 43, 645-669. doi:10.1146/annurev.ento.43.1.645

Horowitz, A.R., Kontsedalov, S., & Ishaaya, I., (2004). Dynamics of resistance to the neonicotinoids acetamiprid and thiamethoxam in Bemisia tabaci (Homoptera: Aleyrodidae). Journal of Economic Entomology, 97(6), 2051-2056. Retrieved from https://doi.org/10.1093/jee/97.6.2051

Kheradmand, K., Khosravian, M., & Shahrokhi, S. (2012). Side effect of four insecticides on demographic statistics of aphid parasitoid, Diaeretiella rapae (McIntosh )(Hym., Braconidae). Annals of Biological Research, 3(7), 3340-3345.

Manzano, M.R., & van Lenteren, J.C. (2009). Life history parameters of Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) at different environmental conditions on two bean cultivars. Neotropical Entomology, 38(4), 452-458. doi:10.1590/S1519-566X2009000400002

Morales, J.J., Medina, P., & Vinuela, E. (2006). Compatibility of Hyposoter didymator, an endoparasitoid of Spodoptera littoralis, with several insecticides used on horticultural crops. IOBC/WPRS Bulletin, 29, 345-350.

Nauen, R., Koob, B., & Elbert, A. (1998). Antifeedant effects of sublethal dosages of imidacloprid on Bemisia tabaci. Entomologia Experimentalis et Applicata, 88(3), 287-293. doi:10.1046/j.1570-7458.1998.00373.x

Nauen, R., Strobel, J., Tietjen, K., Otsu, Y., Erdelen, C., & Elbert, A. (1996). Aphicidal activity of imidacloprid against a tobacco feeding strain of Myzus persicae (Homoptera: Aleyrodidae) from Japan closely related to Myzus nicotianae and highly resistant to carbamates and organophosphates. Bulletin of Entomological Research, 86(2), 165-171. doi:10.1017/S0007485300052408

Perić, P., Marčić, D., & Stamenković, S. (2009). Natural enemies of whitef ly (Trialeurodes vaporariorum Westwood) in Serbia. Acta Horticulturae, 830, 539-544. doi:10.17660/ActaHortic.2009.830.77

Polaszek, A., Evans, G.A., & Bernett, E.D. (1992). Encarsia parasitoids of Bemisia tabaci (Hymenoptera:Aphelinidae, Homoptera:Aleyrodidae): a preliminary guide to identification. Bulletin of Entomological Research, 82(3), 375-392. doi:10.1017/S0007485300041171

Prijović, M., Škaljac, M., Drobnjaković, T., Žanić, K., Perić, P., Marčić, D., & Puizina, J. (2014). Genetic variation of the greenhouse whitefly, Trialeurodes vaporariorum (Hemiptera: Aleyrodidae), among populations from Serbia and neighbouring countries, as inferred from COI sequence variability. Bulletin of Entomological Research, 104(3), 357-366. doi:10.1017/S0007485314000169.

Qiu, Y.T., van Lenteren, J.C., Drost, Y.C., & Posthuma-Doodeman, J.A.M. (2004). Life history parameters of Encarsia formosa, Eretmocerus eremicus and E. mundus, aphelinid parasitoids of Bemisia argentifolii (Homoptera: Aleyrodidae). European Journal of Entomology, 101(1), 83-94. doi:10.14411/eje.2004.017

Richter, S.E., Albert, R., Jaeckel, B. , & Leopold, D. (2003): Encarsia formosa –a parasitoid for biological control under influence at insecticides and changing hosts. Nachrichtenbl Deut Pflanzenschutzd Journal, 55, 161-172.

Robertson, J.L., Russell, R.M., Preisler, H.K., & Savin, N.E. (2007): Bioassays with Arthropods (2nd edition). Boca Raton, FL., USA: CRC Press, Taylor & Francis Group.

Sabahi, Q, Rasekh, A., & Michaud, J.P. (2011). Toxicity of three insecticides to Lysiphlebus fabarum, a parasitoid of the black bean aphid, Aphis fabae. Journal of Insect Science 11, 104. doi:10.1673/031.011.10401

Saber, M. (2011). Acute and population level toxicity of imidacloprid and fenpyroximate on an important egg parasitoid, Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae). Ecotoxicology, 20(6), 1476-1484. doi:10.1007/s10646-011-0704-3

Saber, M., Hassan, S.A., & Hejazi, M.J. (2009). The effect of a neonicotinoid insecticide, imidacloprid, on an important egg parasitoid Trichogramma cacoeciae Marchal (Hymenoptera: Trichogrammatidae). In Proceedings of German Society of Basic and Applied Entomology (DGaaE) (pp 16-19). Gottingen, Germany: Georg-August University.

Sclar, D.C., Gerace, D. & Cranshaw, W.S. (1998). Observations of population increases and injury by spider mites (Acari: Tetranychidae) on ornamental plants treated with imidacloprid. Journal of Economic Entomology, 91(1), 250-255. doi:10.1093/jee/91.1.250

Simmonds, M.S.J., Manlove, J.D., Blaney, W.M., & Khambay, B.P.S. (2002). Effects of selected botanical insecticides on the behaviour and mortality of the glasshouse whitefly Trialeurodes vaporariorum and the parasitoid Encarsia formosa. Entomologia Experimentalis et Applicata, 102(1), 39-47. doi:10.1046/j.1570-7458.2002.00923.x

Sohrabi, F., Shishehbor, P., Saber M., & Mosaddegh, M.S. (2012). Lethal and sublethal effects of buprofezin and imidacloprid on the whitefly parasitoid Encarsia inaron (Hymenoptera: Aphelinidae). Crop Protection, 32, 83–89. doi:10.1016/j.cropro.2011.10.005

Sohrabi, F., Shishehbor, P., Saber, M., & Mosaddegh, M.S. (2013). Lethal and sublethal effects of imidacloprid and buprofezin on the sweetpotato whitefly parasitoid Eretmocerus mundus (Hymenoptera: Aphelinidae). Crop Protection, 45, 98-103. doi:10.1016/j.cropro.2012.11.024

Stapel, J.O., Cortescero, A.M., & Lewis, W.J. (2000). Disruptive sublethal effects of insecticides on biological control: altered foraging ability and lifespan of a parasitoid after feeding on extrafloral nectar of cotton treated with systemic insecticides. Biological Control, 17(3), 243-249. doi:10.1006/bcon.1999.0795

Stark, J.D., & Banks, J.E. (2003). Population-level effects of pesticides and other toxicants on arthropods. Annual Review of Entomology, 48, 505-519. doi:10.1146/annurev.ento.48.091801.112621

Stark, J.D., Tanigoshi, L., Bounfour, M., & Antonelli, A. (1997). Reproductive potential: its influence on the susceptibility of a species to pesticides. Ecotoxicology and Environmental Safety, 37(3), 273-279. doi:10.1006/eesa.1997.1552

Sterk, G., Heuts, F., Merck, N. & Bock, J. (2002). Sensitivity of non-target arthropods and beneficial fungal species to chemical and biological plant protection products: Results of laboratory and semi-field trials. In First International Symposium on Biological Control of Arthropods (pp 306-313). Retrieved from USDA, USFS at https://www.fs.fed.us/foresthealth/technology/webpubs/FHTET-2003-05/day4/sterk.pdf

Stouthamer, R., & Mak, F. (2002). Influence of antibiotics on the offspring production of the Wolbachia-infected parthenogenetic parasitoid Encarsia formosa. Journal of Inverterbrate Pathology, 80(1), 41-45. doi:10.1016/S0022-2011(02)00034-4

Torres, J.B., Silva-Torres, C.S.A., Silva, M.R., & Ferreira, J. (2002). Compatibilidade de inseticidas e acaricidascom o percevejo predador Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) em algodoeiro. Neotropical Entomology, 31(2), 311-317. doi:10.1590/S1519-566X2002000200020

van Lenteren, J.C., & Martin, N.A.. (1999). Biological control of whiteflies. In R.Albajes, M. L. Gullino, J.C. van Lenteren & Y. Elad (Eds.), Integrated pest and disease menagement in greenhouse crops (pp 202-216). Dordrecht, Netherlands: Kluwer Academic Publishers.

van de Veire, M., & Tirry, L. (2003). Side effects of pesticides on four species of beneficials used in IPM in glasshouse vegetable crops: “worst case” laboratory tests. IOBC/WPRS Bulletin 26(5), 41-50.

Whalon, M.E., Mota-Sanchez, D., & Hollingworth, R.M. (2008): Global Pesticide Resistance in Arthropods. Wallingford, UK: CAB International.

Whalon, M.E., Mota-Sanchez, D., Hollingworth, R.M., & Duynslager, L. (2017): Arthropod pesticide resistance database. Retrieved from https://www.pesticideresistance.org/

Yankova, V. Masheva, S. Boev, B., & Toskov, K. (2011). Toxicity of plant protection products towards the imago of Encarsia formosa Gah. Agricultural Science and Technology, 3(4), 374, 377. Retrieved from http://www.nhm.ac.uk/resources/research-curation/projects/chalcidoids/pdf_X/YankovMaBo2011.pdf

Zchori-Fein, E., Roush, R.T., & Hunter, M.S. (1992). Male production induced by antibiotic treatment in Encarsia formosa (Hymenoptera: Aphelinidae), an asexual species. Experientia, 48(1), 102-105. doi:10.1007/BF01923619

Published
2017/12/29
Section
Original Scientific Paper