Neonicotinoid resistance in adults and nymphs of Bemisia tabaci (Genn., 1889) (Hemiptera: Aleyrodidae) populations in tomato fields from Tokat, Turkey

Yıl 2020, Cilt: 44 Sayı: 3, 319 - 331, 01.09.2020

Tarık Balkan Kenan Kara

https://doi.org/10.16970/entoted.650742

Cited By: 2

Öz

Bemisia tabaci (Genn., 1889) (Hemiptera: Aleyrodidae) is one of the most important agricultural pests in Turkey and in the world. This polyphagous pest is a highly efficient vectors of plant viruses and has the ability to rapidly develop resistance to diverse range of insecticides, hence controlling this pest is problematic. In this study, bioassays and biochemical tests were conducted to determine resistance to neonicotinoid in B. tabaci populations collected in 2017-2018 from Tokat (Turkey). According to the adult test results, resistance ratios for acetamiprid, imidacloprid and thiamethoxam were 5.64-16.8, 10.0-30.9 and 4.01-14.9, respectively. The highest resistance ratio for acetamiprid and thiamethoxam in the Pazar population were 16.8 and 14.9, respectively. The highest resistance ratio to imidacloprid was 30.9 in the TOGU campus population. According to the nymph test results, resistance ratios for acetamiprid, imidacloprid and thiamethoxam were 2.96-8.60; 4.29-8.74 and 2.48-4.88, respectively. Enzyme analysis revealed statistically higher metabolic resistance. Maximum enzyme activities were 4.37 and 3.79 pmol/min/mg protein for cytochrome P450 monooxygenase in TOGU campus and Pazar populations, respectively.

Anahtar Kelimeler

Acetamiprid, Bemisia tabaci, imidacloprid, insecticide resistance, thiamethoxam

Destekleyen Kurum

Tokat Gaziosmanpasa University Scientific Research Projects Coordination Unit

Proje Numarası

2016/45

Teşekkür

We are grateful to Tokat Gaziosmanpaşa University Scientific Research Projects Coordination Unit (project number 2016/45) for financial aid.

Tokat (Türkiye) domates alanlarındaki Bemisia tabaci (Genn., 1889) (Hemiptera: Aleyrodidae) ergin ve nimf popülasyonlarında neonikotinoid direnci

Öz

Bemisia tabaci (Genn., 1889) (Hemiptera: Aleyrodidae) Türkiye ve dünyadaki en önemli tarım zararlılarından biridir. Bu polifag zararlı oldukça etkili bir bitki virüs vektörüdür ve çeşitli insektisitlere karşı hızla direnç geliştirme kabiliyetine sahiptir, bu yüzden zararlıyı kontrol etmek zordur. Bu çalışma 2017-2018 yıllarında Tokat (Türkiye)'tan toplanan farklı B. tabaci popülasyonlarının neonikotinoid grubu insektisitlere karşı direnç durumunu biyoassay ve biyokimyasal yöntemlerle belirlemek amacıyla yapılmıştır. Ergin testlerinde ortaya çıkan sonuçlara göre acetamiprid, imidacloprid ve thiamethoxam için direnç oranları, sırasıyla 5.64-16.8; 10.0-30.9 ve 4.01-14.9 arasındadır. Acetamiprid ve thiamethoxam için en yüksek direnç oranı, Pazar popülasyonunda sırasıyla 16.8 ve 14.9 ’dur. Imidacloprid’e en yüksek direnç ise TOGU kampüs popülasyonunda 30.9’dur. Nimf testlerinde ortaya çıkan sonuçlara göre acetamiprid, imidacloprid ve thiamethoxam için direnç oranları, sırasıyla 2.96-8.60; 4.29-8.74 ve 2.48-4.88 arasındadır. Enzim analizi istatistiki anlamda yüksek metabolik direnci ortaya çıkarmıştır. Her üç insektisit içinde, TOGU kampüs ve Pazar popülasyonlarında en yüksek monooksigenaz P450 enzim aktivitesi sırasıyla 4.37 ve 3.79 pmol/dk/mg protein bulunmuştur.

Anahtar Kelimeler

Acetamiprid, Bemisia tabaci, imidacloprid, insektisit direnci, thiamethoxam

Proje Numarası

2016/45

Kaynakça

• Anonymous, 2019a. Bemisia tabaci. (Web page: https://gd.eppo.int/taxon/BEMITA/distribution) (Data accessed: January 2019).
• Anonymous, 2019b. Neonicotinoids. (Web page: http://www.pan-uk.org/about_neonicotinoids) (Data accessed: December 2019).
• Anonymous, 2019c. Tomato production in Tokat. (Web page: http://www.oka.org.tr/Documents/TOKAT_Tarim_ve_ Kirsal_Kalkinma_Eylem_Plani.pdf) (Data accessed: May 2019).
• APRD, 2019. Bemisia tabaci. (Web page: https://www.pesticideresistance.org/ display.php?page=species&arId=505) (Data accessed: August 2019).
• Bahşi, Ş. Ü., F. Dağlı, C. İkten & H. Göçmen, 2012. Antalya ve ilçelerinden toplanan Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) populasyonlarının Acetamiprid, Chlorpyrifos-ethyl ve Cypermethrin’e karşı duyarlılık düzeyleri. Akdeniz Üniversitesi Ziraat Fakültesi Dergisi, 25 (1): 17-22.
• Basij, M., K. Talebi, M. Ghadamyari, V. Hosseininaveh & S. A. Salami, 2017. Status of resistance of Bemisia tabaci (Hemiptera: Aleyrodidae) toneonicotinoids in Iran and detoxification by cytochrome P450-dependent monooxygenases. Neotropical Entomology, 46 (1):115-124.
• Basit, M., S. Saeed, M. A. Saleem, I. Denholm & M. Shah, 2013. Detection of resistance, cross-resistance, and stability of resistance to new chemistry insecticides in Bemisia tabaci (Homoptera: Aleyrodidae). Entomological Society of America, 106 (3): 1414-1422.
• Bass, C., I. Denholm, M. S. Williamson & R. Nauen. 2015. The global status of insect resistance to neonicotinoid insecticides. Pesticide Biochemistry and Physiology, 121: 78-87.
• Bayhan, E., M. R. Ulusoy & J. K. Brown, 2006. Host range, distribution, and natural enemies of Bemisia tabaci ‘B biotype’ (Hemiptera: Aleyrodidae) in Turkey. Journal of Pest Science, 79 (4): 233-240.
• Bedford, I. D., R. W. Briddon, J. K. Brown, R. C. Rosell & P. G. Markham, 1994. Geminivirus transmission and biological characterisation of Bemisia tabaci (Gennadius) biotypes from different geographic regions. Annals of Applied Biology, 125 (2): 311-325.
• Bedford, I. D., R. W. Briddon, P. G. Markham, J. K. Brown & R. C. Rossell, 1993. A new species of Bemisia or biotype of Bemisia tabaci (Gennadius), as a future pest of European agriculture. Plant Health and the European Single Market, BCPC Monograph, 54: 381-386.
• Boykin, L. M., 2014. Bemisia tabaci nomenclature: lessons learned. Pest Management Science, 70 (10): 1454-1459.
• Bradford, M. M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry, 72 (1-2): 248-254.
• Byrne, F. J., S. Castle, N. Prabhaker & N. C. Toscano, 2003. Biochemical study of resistance to imidacloprid in B biotype Bemisia tabaci from Guatemala. Pest Management Science, 59 (3): 347-352.
• Cahill, M., K. Gorman, S. Day & I. Denholm. 1996. Baseline determination and detection of resistance to imidacloprid in Bemisia tabaci (Homoptera: Aleyrodidae). Bulletin of Entomological Research, 86 (4): 343-349.
• Castle, S. J. & N. Prabhaker, 2013. Monitoring changes in Bemisia tabaci (Hemiptera: Aleyrodidae) susceptibility to neonicotinoid insecticides in Arizona and California. Journal of Economic Entomology, 106 (3): 1404‐1413.
• Denholm, I., M. Cahill, T. Dennehy & A. R. Horowitz, 1998. Challenges with managing insecticide resistance in agricultural pests, exemplified by the whitefly Bemisia tabaci. Philosophical Transactions of the Royal Society B, 353 (1376): 1757-1767.
• Elbert, N. & R. Nauen, 2000. Resistance of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides in southern Spain with special reference to neonicotinoids. Pest Management Science, 56 (1): 60-64.
• Feng, Y., Q. Wu, S. Wang, X. Chang, W. Xie, B. Xu, & Y. Zhang, 2010. Cross-resistance study and biochemical mechanisms of thiamethoxam resistance in B-biotype Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Management Science, 66 (3): 313-318.
• Gilbertson, R. L., O. Batuman, C. G. Webster & S. Adkins, 2015. Role of the insect supervectors Bemisia tabaci and Frankliniella occidentalis in the emergence and global spread of plant viruses. Annual Review of Virology, 2 (1): 67-93.
• Gnankiné, O., L. Mouton, A. Savadogo, T. Martin , A. Sanon , R. K. Dabire, F. Vavre & F. Fleury, 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 (2): 95-102.
• Hajjar, M. J., I. Almarzouk, & K. Alhudaib, 2020. Biotype and status of insecticide resistance of whitefly Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) in Alhassa oasis, Eastern Province of Saudi Arabia. Entomological Research, 50 (2): 74-81.
• Horowitz, A. R., S. Kontsedalov & I. Ishaaya, 2004. Dynamics of Resistance to the Neonicotinoids Acetamiprid and Thiamethoxam in Bemisia tabaci (Homoptera: Aleyrodidae). Journal of Economic Entomology, 97 (6): 2051-2056.
• IRAC, 2016a. Bemisia tabaci adult biyoassay method. (Web page: http://www.irac-online.org/methods/bemisia-tabaci-adults) (Data accessed: February 2019).
• IRAC, 2016b. Bemisia tabaci nymphs biyoassay method. (Web page: http://www.irac-online.org/methods/trialeurodes-vaporariorum-bemisia-tabaci-nymphs) (Data accessed: February 2019). IRAC, 2020. Mode of Action Classification Scheme, Version 9.4. (Web page: https://www.irac-online.org/ documents /moaclassification) (Data accessed: March 2020).
• Jeschke, P. & R. Nauen, 2005. “Neonicotinoid Insecticides, 53-105”. In: Comprehensive Molecular Insect Science (Eds. L. I. Gilbert, L. Iatrou & S. S. Gill). Elsevier, Oxford, UK, 459 pp.
• Jeschke, P., R. Nauen, M. Schindler & A. Elbert, 2011. Overview of the status and global strategy for neonicotinoids, Journal of Agricultural and Food Chemistry, 59 (7): 2897-2908.
• Jones, C. M., M. Daniels, M. Andrews, R. Slater, R. J. Lind, K. Gorman, M. S. Williamson & I. Denholm, 2011. Age-specific expression of a P450 monooxygenase (CYP6CM1) correlates with neonicotinoid resistance in Bemisia tabaci. Pesticide Biochemistry and Physiology, 101 (1): 53-58.
• Karunker, I., B. Juergen, L. Bettina, P. Tanja, R. Nauen, R. Emmanouil, V. John, G. Kevin, D. Ian & M. Shai, 2008. Overexpression 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 (6): 634-644.
• Karut, K., M. Kaydan, S. Castle, C. Kazak & M. Ulusoy, 2014. Çukurova'da pamukta bulunan Bemisia tabaci (Gennadius, 1889) (Hemiptera: Aleyrodidae)'nin tür kompleksi üzerine çalışmalar. Turkish Journal of Entomology, 38 (1): 43-50.
• Karut, K., A. Malik, C. Kazak, M. Kamberoğlu & M. Ulusoy, 2012. Determination of biotypes of Bemisia tabaci Gennadius 1889 (Hemiptera: Aleyrodidae) on different host plant in Adana (Balcalı) by using two different molecular methods. Turkish Journal of Entomology, 36 (1): 93-100.
• Luo, C., C. M. Jones, G. Devine, F. Zhang, I. Denholm & K. Gorman, 2010. Insecticide resistance in Bemisia tabaci biotype Q (Hemiptera: Aleyrodidae) from China. Crop Protection, 29 (5): 429-434.
• Markham, P. G., I. D. Bedford, S. Liu & M. S. Pinner, 1994. The transmission of geminiviruses by Bemisia tabaci. Pesticide Science, 42 (2): 123-128.
• Martin, J. H., D. Mifsud & C. Rapisarda, 2000. The whiteflies (Hemiptera: Aleyrodidae) of Europe and the Mediterranean Basin. Bulletin of Entomological Research, 90 (5): 407-448.
• Naranjo, S. E. & P. C. Ellsworth, 2009. Fifty years of the integrated control concept: Moving the model and implementation forward in Arizona. Pest Management Science, 65 (12): 1267-1286.
• Nauen, R., P. Bielza, I. Denholm & K. Gorman, 2008. Age-specific expression of resistance to a neonicotinoid insecticide in the whitefly Bemisia tabaci. Pest Management Science, 64 (11): 1106-1110.
• Nauen, R., N. Stumpf & A. Elbert, 2002. Toxicological and mechanistic studies on neonicotinoid cross resistance in Q-type Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Management Science, 58 (9): 868-875.
• Nauen R., K. Wolfel, B. Lueke, A. Myridakis, D. Tsakireli, E. Roditakis, A. Tsagkarakou, E. Stephanou & J. Vontas, 2015. Development of a lateral flow test to detect metabolic resistance in Bemisia tabaci mediated by CYP6CM1, a cytochrome P450 with broad spectrum catalytic efficiency. Pesticide Biochemistry and Physiology, 121: 3-11.
• Naveen, N. C., R. Chaubey, D. Kumar, K. B. Rebijith, R. Rajagopal, B. Subrahmanyam & S. Subramanian, 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 (Nature Publisher Group), 7: 40634.
• Paul, J. B., L. Shu-Sheng, M. B. Laura & B. D. Adam, 2011. Bemisia tabaci: A statement of species status. Annual Review of Entomology, 56 (1): 1-19. Rao, Q., Y. Xu, C. Luo, H. Zhang, C. M. Jones, G. J. Devine, K. Gorman & I. Denholm, 2012. Characterisation of Neonicotinoid and Pymetrozine Resistance in Strains of Bemisia tabaci (Hemiptera: Aleyrodidae) from China, Journal of Integrative Agriculture, 11 (2): 321-326.
• Rauch, N. & R. Nauen, 2003. Identification of biochemical markers linked to neonicotinoid cross resistance in Bemisia tabaci (Hemiptera: Aleyrodidae). Archives of Insect Biochemistry and Physiology, 54 (4): 165-176.
• Roditakis, E., N. E. Roditakis & A. Tsagkarakou, 2005. Insecticide resistance in Bemisisa tabaci (Homoptera: Aleyrodidae) populations from Crete. Pest Management Science, 61 (6): 577-582.
• Roditakis, E., M. Grispou, E. Morou, J. B. Kristoffersen, N. Roditakis, R. Nauen, J. Vontas & A. Tsagkarakou, 2009. Current status of insecticide resistance in Q biotype Bemisia tabaci populations from Crete. Pest Management Science, 65 (3): 313-322.
• Roditakis, E., E. Morou, A. Tsagkarakou, M. Riga, R. Nauen, M. Paine & J. Vontas, 2011. Assessment of the Bemisia tabaci CYP6CM1vQ transcript and protein levels in laboratory and field-derived imidacloprid resistant insects and cross-metabolism potential of the recombinant enzyme. Insect Science, 18 (1): 23-29.
• Şahin, İ. & C. İkten, 2017. Neonicotinoid resistance in Bemisia tabaci (Genn., 1889) (Hemiptera: Aleyrodidae) populations from Antalya, Turkey. Turkish Journal of Entomology, 41 (2): 169-175.
• Satar, G. & M. R. Ulusoy, 2016. Akdeniz Bölgesi’nden toplanan Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) popülasyonlarının biyotiplerinin belirlenmesi. Türkiye Entomoloji Bülteni, 6 (3): 205-212.
• Satar, G., M. R. Ulusoy, R. Nauen & K. Dong, 2018. Neonicotinoid insecticide resistance among populations of Bemisia tabaci in the Mediterranean region of Turkey. Bulletin of Insectology, 71 (2): 171-177.
• Schuster, D. J., R. S. Mann, M. Toapanta, R. Cordero, S. Thompson, S. Cyman, A. Shurtleff & R. F. II. Morris, 2010. Monitoring neonicotinoid resistance in biotype B of Bemisia tabaci in Florida. Pest Management Science, 66 (2): 186-195.
• Schuster, D. J., R. S. Mann, M. Toapanta, R. Cordero, S. Thompson & R. F. Morris, 2006. Monitoring of imidacloprid resistance in biotype B of Bemisia tabaci. Florida Fourth International Bemisia Workshop International Whitefly Genomics Workshop. Journal of Insect Science, 8 (4): 41-42.
• Smith, H. A. & C. A. Nagle, 2014. “Susceptibility of Bemisia tabaci to Group 4 Insecticides, 27-28”. The Florida Tomato Proceedings (3 September 2014, Florida, USA), 60 pp.
• Stumpf, N. & R. Nauen, 2002. Biochemical markers linked to abamectin resistance in Tetranychus urticae (Acari: Tetranychidae). Pesticide Biochemistry and Physiology, 72 (2): 111-121.
• Taquet, A., H. Delatte, B. Barrès, C. Simiand, M. Grondin & H. Jourdan-Pineau, 2020. Insecticide resistance and fitness cost in Bemisia tabaci (Hemiptera: Aleyrodidae) invasive and resident species in La Réunion Island. Pest Management Science, 76 (4): 1235-1244.
• Taylor, J. E., 2011. The Distribution of Relationship Between, and Factors Influencing the Abundance of Bemisia tabaci and the Incidence of Tomato Yellow Leaf Curl Virus in Southern Florida Tomato. University of Florida (Unpublished) Phd Thesis, 206 pp.
• Thomas, M. P., 2001. The Bemisia tabaci species complex. Crop Protection, 20 (9): 725-737.
• Topakcı, N. & H. Göçmen, 2011. A research on the morphological characters of B and Q biotypes of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) using scanning electron microscopy. Turkish Journal of Entomology, 35 (3): 495-508.
• Ulusoy, M. R., 2001. Türkiye Beyazsinek Faunası. Baki Kitabevi Yayımları, Adana, 98 s.
• Ulusoy, M. R., K. Karut, M. A. Kanberoğlu & Z. Akdağcık, 2007. Doğu Akdeniz Bölgesi’nde Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) Biyotiplerinin Belirlenmesi: Biyotiplerin Biyolojileri, Doğal Düşmanları, Konukçu Bitki Tercihleri ile Virüs Vektör Özelliklerinin Araştırılması. TÜBİTAK-TOVAG, 105O173 Nolu Proje Raporu, 46 s.
• Ulusoy, M. R., A. Sarı, C. Can & N. Uygun, 1996. “Pamuk beyazsineği, Bemisia tabaci (Gennadius)'nin farklı kültür bitkileri üzerindeki gelişmesinin saptanması, 186-191”. Türkiye 3. Entomoloji Kongresi (24-28 Eylül 1996, Ankara) Bildirileri, 716 pp.
• Vontas, J. G., A. A. Enayati, G. J. Small & J. Hemingway, 2000. A simple biochemical assay for glutathione S-transferase activity and its possible field application for screening glutathione S-transferase-based insecticide resistance. Pesticide Biochemistry and Physiology, 68 (3): 184-192.
• Wang, Z., H. Yan, Y. Yang & Y. Wu, 2010. Biotype and insecticide resistance status of the whitefly Bemisia tabaci from China. Pest Management Science, 66 (12): 1360-1366.
• Wang, R., H. Zheng, C. Qu, Z. Wang, Z. Kong & C. Luo, 2016. Lethal and sublethal effects of a novel cis-nitromethylene neonicotinoid insecticide, cycloxaprid, on Bemisia tabaci. Crop Protection, 83: 15-19.
• Wang, Z., M. Yao & Y. Wu, 2009. Cross-resistance, inheritance and biochemical mechanisms of imidacloprid resistance in B-biotype Bemisia tabaci. Pest Managment Science, 65 (11): 1189-1194.