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Monitoring insecticide resistance and endosymbiont composition in greenhouse populations of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) from Mersin, Turkey

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Abstract

Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) is a destructive pest that causes significant damage on important agricultural crops through direct feeding, honeydew excretion and plant virus transmission. Chemical control is among the most widely used methods to suppress whitefly infestations but management efforts have become very challenging due to the development of insecticide resistance. This study was conducted to monitor insecticide resistance and detect endosymbiont composition in greenhouse-collected B. tabaci populations from Mersin, Turkey. All greenhouse-collected populations were identified as Middle East-Asia Minor 1 (MEAM-1). Based on Resistance ratios (RRs) of LC50 values, all greenhouse-collected populations were low to moderately resistant to the three neonicotinoids when compared to the reference population. Resistance ratios were in the range of 3.63–8.79-fold for acetamiprid; 7.29–15.29-fold for imidacloprid and 9.74–11.79-fold for thiamethoxam after 72 h of exposure. No or very low levels of resistance (RR ≤ 2.00) were detected for spinetoram, spinosad and sulfoxaflor. Spinetoram was the most toxic of all the other tested insecticides against all populations. Generally, LC90 values obtained for greenhouse-collected populations were much higher than the recommended concentrations of the neonicotinoids but lower for spinetoram, spinosad and sulfoxaflor. Molecular analysis of endosymbionts indicated that all populations were infected with Portiera and Hamiltonella, whereas only two out of five greenhouse-collected populations were infected with Rickettsia. The insecticide-susceptible lab strain had relatively the highest rate of Rickettsia infections. Moreover, a statistically significant negative correlation was detected between LC50 values and the rate of Rickettsia infections for imidacloprid and thiamethoxam (R = −0.930 and R = −0.866, respectively), while the relationship was non-significant for acetamiprid resistance (R = −0.598).

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References

  • Abdel-Razek, A. S., Abd El-Ghany, N. M., Djelouah, K., & Moussa, A. (2017). An evaluation of some eco-friendly biopesticides against Bemisia tabaci on two greenhouse tomato varieties in Egypt. Journal of Plant Protection Research, 57, 9–17. https://doi.org/10.1515/jppr-2017-0002.

    Article  CAS  Google Scholar 

  • Ambarish, S., Shashi, K. C., Somu, G., & Navi, S. (2017). Studies on the bio-efficacy of new insecticide molecules against insect pests in cotton aicrp on cotton. Journal of Entomology and Zoology Studies, 5, 544–548. https://doi.org/10.18805/LR-4074.

    Article  Google Scholar 

  • Anonymous. (2009). Susceptibility test methods series method no:008 version:3. Resource document. Insecticide Resistance Action Committee. https://www.irac-online.org/methods/bemisia-tabaci-adults/. Accessed 05 May 2017.

  • Aydin, M. H., & Gurkan, M. O. (2006). The efficacy of spinosad on different strains of Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae). Turkish Journal of Biology, 30, 5–9.

    CAS  Google Scholar 

  • Bacci, L., Covertini, S., & Rossaro, B. (2018). A review of sulfoxaflor, a derivative of biological acting substances as a class of insecticides with a broad range of action against many insect pests. Journal of Entomological and Acarological Research, 50, 51–71. https://doi.org/10.4081/jear.2018.7836.

    Article  Google Scholar 

  • Bahşi, Ş. Ü., Dağlı, F., İkten, C., & Göçmen, H. (2012). Susceptibility level of Bemisia tabaci (Gennadius) (Hemiptera : Aleyrodidae) populations collected from Antalya to acetamiprid, chlorpyrifos-ethyl and cypermethrin. Akdeniz University Journal of Faculty of Agriculture, 25, 17–22.

    Google Scholar 

  • Banazeer, A., Afzal, M. B. S., Ijaz, M., & Shad, S. A. (2019). Spinosad resistance selected in the laboratory strain of Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae): Studies on risk assessment and crossresistance patterns. Phytoparasitica, 47, 531–542. https://doi.org/10.1007/s12600-019-00753-y.

    Article  CAS  Google Scholar 

  • Basij, M., Talebi, K., Ghadamyari, M., Hosseininaveh, V., & Salami, S. A. (2017). Status of Bemisia tabaci (Hemiptera: Aleyrodidae) to neonicotinoids in Iran and detoxification by cytochrome P450-dependent Monooxygenases. Neotropical Entomology, 46, 115–124. https://doi.org/10.1007/s13744-016-0437-3.

    Article  CAS  PubMed  Google Scholar 

  • Basit, M. (2019). Status of insecticide resistance in Bemisia tabaci: Resistance, cross-resistance, stability of resistance, genetics and fitness costs. Phytoparasitica, 47, 207–225. https://doi.org/10.1007/s12600-019-00722-5.

    Article  CAS  Google Scholar 

  • Bayhan, E., Ulusoy, M. R., & Brown, J. K. (2006). Host range, distribution, and natural enemies of Bemisia tabaci ‘B biotype’ (Hemiptera: Aleyrodidae) in Turkey. Journal of Pest Science, 79, 233–240. https://doi.org/10.1007/s10340-006-0139-4.

    Article  Google Scholar 

  • Bedford, I. D., Briddon, R. W., Brown, J. K., Rosell, R. C., & Markham, P. G. (1994). Geminivirus transmission and biological characterisation of Bemisia tabaci (Gennadius) biotypes from different geographic regions. Annals of Applied Biology, 125, 311–325. https://doi.org/10.1111/j.1744-7348.1994.tb04972.x.

    Article  Google Scholar 

  • Berticat, C., Rousset, F., Raymond, M., Berthomieu, A., & Weill, M. (2002). High Wolbachia density in insecticide-resistant mosquitoes. Proceedings of the Royal Society B: Biological Sciences, 269, 1413–1416.

    Article  Google Scholar 

  • Bond, J. G., Marina, C. F., & Williams, T. (2004). The naturally derived insecticide spinosad is highly toxic to Aedes and Anopheles mosquito larvae. Medical and Veterinary Entomology, 18, 50–56. https://doi.org/10.1111/j.0269-283x.2004.0480.x.

    Article  CAS  PubMed  Google Scholar 

  • Boykin, L. M., Bell, C. D., Evans, G., Small, I., & De Barro, P. J. (2013). Is agriculture driving the diversification of the Bemisia tabaci species complex (Hemiptera: Sternorrhyncha: Aleyrodidae)?: Dating, diversification and biogeographic evidence revealed. BMC Evolutionary Biolology, 13, 228. https://doi.org/10.1186/1471-2148-13-228.

    Article  Google Scholar 

  • Brogdon, W. G., & McAllister, J. C. (1998). Insecticide resistance and vector control. Emerging Infectious Disease, 4, 605–613. https://doi.org/10.3201/eid0404.980410.

    Article  CAS  Google Scholar 

  • Brumin, M., Kontsedalov, S., & Ghanim, M. (2011). Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Sci., 18, 57–66. https://doi.org/10.1111/j.1744-7917.2010.01396.x.

    Article  Google Scholar 

  • Caballero, R., Cyman, S., & Schuster, D. J. (2013). Monitoring insecticide resistance in biotype B of Bemisia tabaci (Hemiptera: Aleyrodidae) in Florida. Florida Entomologist, 96, 1243–1256. https://doi.org/10.1653/024.096.0402.

    Article  Google Scholar 

  • Castle, S. J., Merten, P., & Prabhaker, N. (2014). Comparative susceptibility of Bemisia tabaci to imidacloprid in field-and laboratory-based bioassays. Pest Management Science, 7, 1538–1546. https://doi.org/10.1002/ps.3717.

    Article  CAS  Google Scholar 

  • Chu, D., Hu, X., Gao, X., Zhao, H., Nichols, R. L., & Li, X. (2012). Use of mitochondrial cytochrome oxidase I polymerase chain reaction-restriction fragment length polymorphism for identifying subclades of Bemisia tabaci Mediterranean group. Journal of Economic Entomology, 105, 242–251. https://doi.org/10.1603/ec11039.

    Article  CAS  PubMed  Google Scholar 

  • Cohen, S., & Berlinger, M. (1986). Transmission and cultural control of whitefly-borne viruses. Agriculture, Ecosystem & Environonment, 17, 89–97. https://doi.org/10.1016/0167-8809(86)90030-7.

    Article  Google Scholar 

  • Dağlı, F. (2018). Spinosad resistance in a population of Frankliniella occidentalis (Pergande, 1895) from Antalya and its cross resistance to acrinathrin and formetanate. Turkish Journal of Entomology, 42, 241–251. https://doi.org/10.16970/entoted.424746.

    Article  Google Scholar 

  • De Barro, P. J., Liu, S. S., Boykin, L. M., & Dinsdale, A. B. (2011). Bemisia tabaci: A statement of species status. Annual Review of Entomology, 56, 1–19. https://doi.org/10.1146/annurev-ento-112408-085504.

    Article  CAS  PubMed  Google Scholar 

  • Dinsdale, A., Cook, L., Riginos, C., Buckley, Y. M., & De Barro, P. (2010). Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Annals of Entomological Society of America, 103, 196–208. https://doi.org/10.1603/AN09061.

    Article  Google Scholar 

  • Dripps, J., Olson, B., Sparks, T., & Crouse, G. (2008). Spinetoram: How artificial intelligence combined natural fermentation with synthetic chemistry to produce a new spinosyn insecticide. Online. Plant Health Progress. https://doi.org/10.1094/PHP-2008-0822-01-PS.

  • Durmuşoğlu, E., Tiryaki O., & Canhilal R. (2010). Türkiye’de pestisit kullanımı, kalıntı ve dayanıklılık sorunları. Resource document. Ministry of Agriculture and Forestry. http://www.zmo.org.tr/resimler/ekler/52cf38361a20908_ek.pdf. Accessed 11 Nov 2019.

  • El-Zoghby, I. R. M. (2017). Studies on the impact of successive sprays with certain insecticides on whitefly and aphids infesting roselle plants and its yield in Aswan governorate, Egypt. Middle East Journal of Applied Sciences, 7, 162–167.

    Google Scholar 

  • Farghaley, S., Singab, M., Ghoneim, Y. F., & Abou-Yousef, H. M. (2010). Identification of mutation in the Bemisia tabaci (Genn.) para sodium channel gene associated with resistance to pyrethroids. Egyptian Journal of Agricultural Research, 88, 153–165. https://doi.org/10.13140/RG.2.2.30453.22241.

    Article  Google Scholar 

  • Fidan, H., Karacaoglu, M., Koc, G., & Caglar, B. K. (2019). Tomato yellow leaf curl virus (TYLCV) strains and epidemiological role of Bemisia tabaci (Hemiptera: Aleyrodidae) biotypes on tomato agroecology in Turkey. Applied Ecology and Environmental Research, 17, 9131–9144. https://doi.org/10.15666/aeer/1704_91319144.

    Article  Google Scholar 

  • Fogné, D. S., Ahmed, C. Y., Rahim, R., Mahamoudou, B., & Olivier, G. (2019). Biochemical resistance to insecticide in Bemisia tabaci field population from Burkina Faso, West Africa. Phytoparasitica, 47, 671–681. https://doi.org/10.1007/s12600-019-00765-8.

    Article  CAS  Google Scholar 

  • Games, P. A., & Howell, J. F. (1976). Pair wise multiple comparison procedures with unequal n's and/or variances. Journal of Educational Statistics, 1, 13–125. https://doi.org/10.2307/1164979.

    Article  Google Scholar 

  • Georghiou, G. P., & Taylor, C. E. (1986). Factors influencing the evolution of resistance. In National Academy of Sciences (Ed.), Pesticide resistance: Strategies and tactics for management (pp. 157–169). Washington, DC: National Academy Press. https://doi.org/10.17226/619.

    Chapter  Google Scholar 

  • Ghanim, M., & Kontsedalov, S. (2009). Susceptibility to insecticides in the Q biotype of Bemisia tabaci is correlated with bacterial symbiont densities. Pest Management Science, 65, 939–942. https://doi.org/10.1002/ps.1795.

    Article  CAS  PubMed  Google Scholar 

  • Gnankinéa, O., Moutonb, L., Savadogoc, A., Martind, T., Sanona, A., Dabire, R. K., Vavre, F., & Fleury, F. (2013). Biotype status and resistance to neonicotinoids and carbosulfan in Bemisia tabaci (Hemiptera: Aleyrodidae) in Burkina Faso, West Africa. International Journal of Pest Management, 59, 95–102. https://doi.org/10.1080/09670874.2013.771806.

    Article  CAS  Google Scholar 

  • Gore, I., Cook, D., Catchot, A., Leonard, B. R., Stewart, S. D., Lorenz, G., Kerns, D., Gorman, K., Denholm, I., & Morin, S. (2013). Cotton aphid (Heteroptera: Aphididae) susceptibility to commercial and experimental insecticides in the southern United States. Journal of Economic Entomology, 106, 1430–1439. https://doi.org/10.1603/ec13116.

    Article  CAS  PubMed  Google Scholar 

  • Gorman, K., Slater, R., Blande, J. D., Clarke, A., Wren, J., McCaffery, A., & Denholm, I. (2010). Cross-resistance relationships between neonicotinoids and pymetrozine in Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Management Science, 66, 1186–1190. https://doi.org/10.1002/ps.1989.

    Article  CAS  PubMed  Google Scholar 

  • Gottlieb, Y., Ghanim, E., Chiel, D., Gerling, V., Portnoy, S., Steinberg, Z., Tzuri, A. R., Horowitz, E., Belausov, N., Mozes-Daube, N., Kontsedalov, S., Gershon, M., Gal, S., Katzir, N., & Zchori-Fein, E. (2006). Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). Applied and Environmental Microbiology, 72, 3646–3652. https://doi.org/10.1128/aem.72.5.3646-3652.2006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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, 2051–2056. https://doi.org/10.1603/0022-0493-97.6.2051.

    Article  CAS  PubMed  Google Scholar 

  • Jahel, M. K., Halawa, S. M., Hafez, A. A., Abd El-Zahar, T. R., & Elgizawy, K. K. (2017). Comparative efficacy of different insecticides against whitefly, Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) on Tomato Plants. Middle East Journal of Applied Sciences, 07, 786–793.

    Google Scholar 

  • Jiang, Z. F., Xia, F., Johnson, K. W., Brown, C. D., Bartom, E., Tuteja, J. H., Stevens, R., Grossman, R. L., Brumin, M., White, K. P., & Ghanim, M. (2013). Comparison of the genome sequences of “Candidatus Portiera aleyrodidarum” primary endosymbionts of the whitefly Bemisia tabaci B and Q biotypes. Applied and Environmental Microbiology, 79, 1757–1759. https://doi.org/10.1128/aem.02976-12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karunker, I., Benting, J., Lueke, B., Ponge, T., Nauen, R., Roditakis, E., Vontas, J., Gorman, K., Denholm, I., & Morin, S. (2008). Over-expression of cytochrome P450 CYP6CM1 is associated with high resistance to imidacloprid in the B and Q biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae). Insect Biochemistry and Molecular Biology, 38, 634–644. https://doi.org/10.1016/j.ibmb.2008.03.008.

    Article  CAS  PubMed  Google Scholar 

  • Karut, K., & Tok, B. (2014). Secondary endosymbionts of Turkish Bemisia tabaci (Gennadius) populations. Phytoparasitica, 42, 413–419. https://doi.org/10.1007/s12600-013-0378-x.

    Article  Google Scholar 

  • Karut, K., Kazak, C., Döker, İ., & Malik, A. A. Y. (2012). Natural parasitism of Bemisia tabaci (Hemiptera: Aleyrodidae) by native Aphelinidae (Hymenoptera) parasitoids in tomato greenhouses in Mersin, Turkey. IOBC-WPRS Bulletin, 80, 69–74.

    Google Scholar 

  • Karut, K., Kaydan, M. B., Castle, S. J., Kazak, C., & Ulusoy, M. R. (2014). Study on species composition of Bemisia tabaci (Gennadius, 1889) (Hemiptera: Aleyrodidae) on cotton in Çukurova plain, Turkey. Turkish Journal of Entomology, 38, 43–50. https://doi.org/10.16970/ted.41111.

    Article  Google Scholar 

  • Karut, K., Karaca, M. M., Döker, İ., & Kazak, C. (2017). Analysis of species, subgroups, and endosymbionts of Bemisia tabaci (Hemiptera: Aleyrodidae) from southwestern cotton fields in Turkey. Environmental Entomology, 46, 1035–1040. https://doi.org/10.1093/ee/nvx093.

    Article  PubMed  Google Scholar 

  • Kikuchi, Y., Hayatsu, M., Hosokawa, T., Nagayama, A., Tago, K., & Fukatsu, T. (2012). Symbiont-mediated insecticide resistance. Proceedings of the National Academy of Sciences (PNAS), 109, 8618–8622. https://doi.org/10.1073/pnas.1200231109.

    Article  Google Scholar 

  • Kim, Y. J., Lee, Y. J., & Kim, G. H. (1999). Toxicity of tebufenpyrad to Tetranychus urticae (Acari: Tetranychidae) and Amblyseius wormersleyi (Acari: Phytoseiidae) under laboratory and field conditions. Journal of Economic Entomology, 92, 187–192. https://doi.org/10.1093/jee/92.1.187.

    Article  CAS  Google Scholar 

  • Kim, S. I., Chae, S. H., Youn, H. S., Yeon, S. H., & Ahn, Y. J. (2011). Contact and fumigant toxicity of plant essential oils and efficacy of spray formulations containing the oils against B-and Q-biotypes of Bemisia tabaci. Pest Management Science, 67, 1093–1099. https://doi.org/10.1002/ps.2152.

    Article  CAS  PubMed  Google Scholar 

  • Kontsedalov, S., Zchori-Fein, E., Chiel, E., Gottlieb, Y., Inbar, M., & Ghanim, M. (2008). The presence of Rickettsia is associated with increased susceptibility of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides. Pest Management Science, 64, 789–792. https://doi.org/10.1002/ps.1595.

    Article  CAS  PubMed  Google Scholar 

  • Kontsedalov, S., Abu-Moch, F., Lebedev, G., Czosnek, H., Horowitz, A. R., & Ghanim, M. (2012). Bemisia tabaci biotype dynamics and resistance to insecticides in Israel during the years 2008–2010. Journal of Integrative Agriculture, 11, 312–320. https://doi.org/10.1016/S2095-3119(12)60015-X.

    Article  CAS  Google Scholar 

  • Kumar, V., Kakkar, G., Cindy, L. M., & Osborne, L. S. (2017). Effect of foliar application of Xxpire on Bemisia tabaci (MED whitefly) and Amblyseius swirskii. Arthropod Management Tests, 42, 1–2. https://doi.org/10.1093/amt/tsx077.

    Article  Google Scholar 

  • Langfield, K. L., Woolley, L. K., Learmonth, S., & Herron, G. A. (2018). Spinetoram resistance detected in western flower thrips 'Frankliniella occidentalis' (pergande) following a control failure. General and Applied Entomology: The Journal of the Entomological Society of New South Wales, 46, 43–45.

    Google Scholar 

  • Lebedev, G., Abo-Moch, F., Gafni, G., Ben-Yakir, D., & Ghanim, M. (2013). High-level of resistance to spinosad, emamectin benzoate and carbosulfan in populations Thrips tabaci collected in Israel. Pest Management Science, 69, 274–277. https://doi.org/10.1002/ps.3385.

    Article  CAS  PubMed  Google Scholar 

  • Longhurst, C., Babcock, J. M., Denholm, I., Gorman, K., Thomas, J. D., & Sparks, T. C. (2013). Cross-resistance relationships of the sulfoximine insecticide sulfoxaflor with neonicotinoids and other insecticides in the whiteflies Bemisia tabaci and Trialeurodes vaporaiorum. Pest Management Science, 69, 809–813. https://doi.org/10.1002/ps.3439.

    Article  CAS  PubMed  Google Scholar 

  • Luo, C., Jones, C. M., Devine, G. D., Zhang, F., Denholm, I., & Gorman, K. (2010). Insecticide resistance in Bemisia tabaci biotype Q (Hemiptera: Aleyrodidae) from China. Crop Protection, 29, 429–434. https://doi.org/10.1016/j.cropro.2009.10.001.

    Article  CAS  Google Scholar 

  • Ma, D., Gorman, K., Devine, G. D., Luo, W. C., & Denholm, I. (2007). The biotype and insecticide-resistance status of whiteflies, Bemisia tabaci (Hemiptera: Aleyrodidae), invading cropping systems in Xinjiang Uygur autonomous region, northwestern China. Crop Protection, 26, 612–617. https://doi.org/10.1016/j.cropro.2006.04.027.

    Article  CAS  Google Scholar 

  • Nauen, R., Stumpf, N., & Elbert, A. (2002). Toxicological and mechanistic studies on neonicotinoid cross resistance in Q-type Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Management Science, 58, 868–875. https://doi.org/10.1002/ps.557.

    Article  CAS  PubMed  Google Scholar 

  • Naveen, N. C., Chaubey, R., Kumar, D., Rebijith, K. B., Rajagopal, R., Subrahmanyam, B., & Subramanian, S. (2017). Insecticide resistance status in the whitefly, Bemisia tabaci genetic groups Asia-I, Asia-II-1 and Asia-II-7 on the Indian subcontinent. Scientific Reports, 7, 40634. https://doi.org/10.1038/srep40634.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palumbo, J. C., Horowitz, A. R., & Prabhaker, N. (2001). Insecticidal control and resistance management for Bemisia tabaci. Crop Protection, 20, 739–765. https://doi.org/10.1016/S0261-2194(01)00117-X.

    Article  CAS  Google Scholar 

  • Pan, H. P., Chu, D., Liu, B. M., Xie, W., Wang, S. L., Wu, Q. J., Xu, B. Y., & Zhang, Y. J. (2013). Relative amount of Symbionts in insect hosts changes with host-plant adaptation and insecticide resistance. Environmental Entomology, 42, 74–78. https://doi.org/10.1603/en12114.

    Article  CAS  PubMed  Google Scholar 

  • Pietri, J. E., & Liang, D. (2018). The links between insect symbionts and insecticide resistance: Causal relationships and evolutionary tradeoffs. Annals of the Entomological Society of America, 111, 92–97.

    Article  CAS  Google Scholar 

  • Prabhaker, N., Castle, S., Henneberry, T. J., & Toscano, N. C. (2005). Assessment of cross-resistance potential to neonicotinoid insecticides in Bemisia tabaci (Hemiptera: Aleyrodidae). Bulletin of Entomological Research, 95, 535–543. https://doi.org/10.1079/ber2005385.

    Article  CAS  PubMed  Google Scholar 

  • Rao, Q., Xu, Y., Luo, C., Zhang, H., Jones, C. M., Devine, G. J., Gorman, K., & Denholm, I. (2012). Characterisation of neonicotinoid and pymetrozine resistance in strains of Bemisia tabaci (Hemiptera: Aleyrodidae) from China. Journal of Integrative Agriculture, 11, 321–326. https://doi.org/10.1016/s2095-3119(12)60016-1.

    Article  CAS  Google Scholar 

  • Şahin, I., & Ikten, C. (2017). Neonicotinoid resistance in Bemisia tabaci (Genn., 1889) (Hemiptera: Aleyrodidae) populations from Antalya, Turkey. Turkish Journal of Entomology, 41, 169–175. https://doi.org/10.16970/ted.76729.

    Article  Google Scholar 

  • Santos-Garcia, D., Farnier, P. A., Beitia, F., Zchori-Fein, E., Vavre, F., Mouton, L., Moya, A., Latorre, A., & Silva, F. J. (2012). Complete genome sequence of "Candidatus Portiera aleyrodidarum" BT-QVLC, an obligate symbiont that supplies amino acids and carotenoids to Bemisia tabaci. Journal of Bacteriology, 194, 6654–6655. https://doi.org/10.1128/jb.01793-12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Satar, G., Nauen, R., Ulusoy, M. R., & Dong, K. (2018). Neonicotinoid insecticide resistance among populations of Bemisia tabaci in the Mediterranean region of Turkey. Bulletin of Insectology, 71, 171–177.

    Google Scholar 

  • Siebert, M. W., Nolting, S., Dripps, J. E., Walton, L. C., Cook, D. R., Stewart, S., Gore, J., Catchot, A. L., Lorenz, G., Leonard, B. R., & Herbert, A. (2016). Efficacy of Spinetoram against Thrips (Thysanoptera: Thripidae) in seedling cotton, Gossypium hirsutum L. The Journal of Cotton Science, 20, 309–319.

    CAS  Google Scholar 

  • Sparks, T. C., Gerald, B., Watson, G. B., Loso, M. R., Geng, C., Babcock, J. M., & Thomas, J. D. (2013). Sulfoxaflor and the sulfoximine insecticides: Chemistry, mode of action and basis for efficacy on resistant insects. Pesticide Biochemistry and Physiology, 107, 1–7. https://doi.org/10.1016/j.pestbp.2013.05.014.

    Article  CAS  PubMed  Google Scholar 

  • Stansly, P. A., & Naranjo, S. E. (2010). Introduction, XV-XVIII. In P. A. Stansly & S. E. Naranjo (Eds.), Bemisia: Bionomics and management of a global pest (p. 540). New York: Springer. https://doi.org/10.1007/978-90-481-2460-2.

    Chapter  Google Scholar 

  • Su, Q., Oliver, K. M., Pan, H., Jiao, X., Liu, B., Xie, W., Wang, S., Wu, Q., Xu, B., White, J. A., Zhou, X., & Zhang, Y. (2013). Facultative symbiont Hamiltonella confers benefits to Bemisia tabaci (Hemiptera: Aleyrodidae), an invasive agricultural pest worldwide. Environmental Entomology, 42, 1265–1271. https://doi.org/10.1603/en13182.

    Article  PubMed  Google Scholar 

  • Topçu, İ., Karaca, M. M., & Karut, K. (2020). Dominance of Bemisia tabaci MEAM1 species over MED (Hemiptera: Aleyrodidae) in greenhouse vegetables in Mersin, Turkey. Phytoparasitica, 48, 159–166. https://doi.org/10.1007/s12600-020-00794-8.

    Article  Google Scholar 

  • Ulusoy, M. R., & Bayhan, E. (2003). A new whitefly species on vegetable fields in the East Mediterranean region of Turkey: Silverleaf whitefly, Bemisia argentifolii bellows and Perring (Homoptera: Aleyrodidae). Turkish Journal of Entomology, 27, 51–60.

    Google Scholar 

  • Van Leeuwen, T., Van de Veire, M., Dermauw, W., & Tirry, L. (2006). Systemic toxicity of Spinosad to the greenhouse whitefly Trialeurodes vaporariorum and to the cotton leaf worm Spodoptera littoralis. Phytoparasitica, 34, 102–108. https://doi.org/10.1007/bf02981345.

    Article  Google Scholar 

  • Vassiliou, V., Emmanouilidou, M., Perrakis, A., Morou, E., Vontas, J., Tsagkarakou, A., & Roditakis, E. (2011). Insecticide resistance in Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) from Cyprus. Insect Sci., 18, 30–39. https://doi.org/10.1111/j.1744-7917.2010.01387.x.

    Article  CAS  Google Scholar 

  • Wang, Z., Yan, H., Yang, Y., & Wu, Y. (2010). Biotype and insecticide resistance status of the whitefly Bemisia tabaci from China. Pest Management Science, 66, 1360–1366.

    Article  CAS  Google Scholar 

  • Wang, S., Zhang, Y., Yang, X., Xie, W., & Wu, Q. (2017a). Resistance monitoring for eight insecticides on the sweet potato whitefly (Hemiptera: Aleyrodidae). Journal of Economic Entomology, 110, 660–666. https://doi.org/10.1093/jee/tox040.

    Article  PubMed  Google Scholar 

  • Wang, W., Wang, S., Han, G., Du, Y., & Wang, J. (2017b). Lack of cross-resistance between neonicotinoids and sulfoxaflor in field strains of Qbiotype of whitefly, Bemisia tabaci, from eastern China. Pesticide Biochemistry and Physiology, 136, 46–51. https://doi.org/10.1016/j.pestbp.2016.08.005.

    Article  CAS  PubMed  Google Scholar 

  • Wheeler, M. W., Park, R. M., & Bailer, A. J. (2006). Comparing median lethal concentration values using confidence interval overlap or ratio tests. Environmental Toxicology and Chemistry, 25, 1441–1444. https://doi.org/10.1897/05-320r.1.

    Article  CAS  PubMed  Google Scholar 

  • WHO. (2016). Test procedures for insecticide resistance monitoring in malaria vector mosquitoes, 2nd edn. Rersouce document, World Health Organization. https://apps.who.int/iris/handle/10665/250677. Accessed Apr 2017.

  • Xia, X., Sun, B., Gurr, G.M., Vasseur, L,, Xue, M. & You, M. (2018). Gut microbiota mediate insecticide resistance in the diamondback moth, Plutella xylostella (L.). Front Microbiology, 9, 25. https://doi.org/10.3389/fmicb.2018.00025.

  • Yao, F. L., Zheng, Y., Huang, X. Y., Dıng, X. L., Zhao, J. W., Desneux, N., He, Y. X., & Wenıg, Q. Y. (2017). Dynamics of Bemisia tabaci biotypes and insecticide resistance in Fujian province in China during 2005-2014. Scientific Reports, 7, 40803.

    Article  CAS  Google Scholar 

  • Zhao, D., Hoffmann, A. A., Zhang, Z., Niu, H., & Guo, H. (2018). Interactions between facultative Symbionts Hamiltonella and Cardinium in Bemisia tabaci (Hemiptera: Aleyrodidea): Cooperation or conflict? Journal of Economic Entomology, 111, 2660–2666. https://doi.org/10.1093/jee/toy261.

    Article  PubMed  Google Scholar 

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Acknowledgments

This paper is produced from Ph.D. thesis of the senior author that was supported by Scientific Research Foundation of Cukurova University, project number: FDK-2018-10555.

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Authors and Affiliations

  1. Department of Plant Protection, Faculty of Agriculture, Cukurova University, 01330, Adana, Turkey

    Mohammed A. Mohammed, M. Mete Karaca, İsmail Döker & Kamil Karut

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  1. Mohammed A. Mohammed
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  2. M. Mete Karaca
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  3. İsmail Döker
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  4. Kamil Karut
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Kamil Karut, İsmail Döker and Mohammed A. Mohammed conceived research. Kamil Karut secured funding. Mohammed A. Mohammed and M. Mete Karaca conducted experiments. Kamil Karut contributed material. Kamil Karut, İsmail Döker and Mohammed A. Mohammed analysed data and conducted statistical analyses. Mohammed A. Mohammed wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Mohammed A. Mohammed.

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Mohammed, M.A., Karaca, M.M., Döker, İ. et al. Monitoring insecticide resistance and endosymbiont composition in greenhouse populations of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) from Mersin, Turkey. Phytoparasitica 48, 659–672 (2020). https://doi.org/10.1007/s12600-020-00812-9

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