Survey on bromopropylate acaricide resistance in the citrus red spider mite, Panonychus citri and the effect of three synergists on its resistance

Document Type : Research Paper

Authors

Department of Plant Protection, Faculty of Agricultural Sciences, University of Guilan, Rasht-Iran

Abstract

Biological characteristics of Panonychus citri such as life cycle, abundant progeny and arrhenotoky, have provided the pest a high potential to develop acaricidal resistance. Bromopropylate is recommended by Iranian Plant Protection Organization to control P. citri. In this study, resistance of p. citri to bromopropylate was investigated. Bioassay and synergists tests were performed with a Potter spray tower method. Results showed a resistance of 10.63 fold to bromopropylate in resistant population (RP). Pre-treatment of susceptible population (SP) of P. citri adult with the cytochrome P450 monooxygenase inhibitor, PBO, the esterase inhibitor, TPP, and glutathione-S-transferases inhibitor, DEM, increased bromopropylate toxicity by 5.58, 5.89 and 4.59-fold, respectively, while, these ratios were as 2.44, 2.51 and 2.38-fold, respectively, for RP. The overall lower synergism in RP compared with susceptible population by DEM, PBO and TPP suggests that glutathione-S-transferases, esterases and monooxygenase are not an important factor in resistance. The results of biochemical tests revealed that the activities of monoxygenase, α-naphthyl, β-naphthyl esterases and glutathione-S-transferase in the resistant population was 1.39, 1.70, 1.83, and 1.34- fold higher than that of susceptible population, respectively. Estimation of kinetic parameters showed qualitative changes in esterase and GST. The increased activities of detoxification enzymes may be caused by application of different acaricides which are used for control of this pest in citrus gardens. Therefore, other resistance mechanisms such as reduced penetration and target site insensitivity likely is involved in the resistance. Reduced bromopropylate application as well as application of acaricides with different mode of actions are necessary for avoiding resistance development. 

Keywords


Alizadeh, A., Talebi, K., Hosseininaveh, V. and Ghadamyari, M. 2011. Metabolic resistance mechanisms to phosalone in the common pistachio psyllid, Agonoscena pistaciae (Hem.: Psyllidae), Pesticide Biochemistry and Physiology 101: 59–64.
Ay, R. and Kara, F. E. 2011. Toxicity, inheritance of fenpyroximate resistance, and detoxification-enzyme levels in a laboratory-selected fenpyroximate-resistant strain of Tetranychus urticae Koch (Acari: Tetranychidae). Crop Protection 30: 605-611.
Ay, R. and Yorulmaz-Salman, S. 2010. Inheritance and detoxification enzyme levels in Tetranychus urticae Koch (Acari: Tetranychidae) strain selected with Chlorpyrifos. Journal of Pest Science 83: 85–93.
Behdad, A. 2009. Primary Entomology and Plant Pests of Iran. Memorial Publication, 840 p. (in Farsi).
Brogdon, W. G., McAllister, J. C. and Vulule, J. 1997. Heme peroxidase activity measured in single mosquitoes identifies individuals expressing an elevated oxidase for insecticide resistance. Journal of American Mosquito Control Association 13 (3): 233-237.
Chen, Z. Y., Ran, C., Zhang, L., Dou, W. and Wang, J. J. 2009. Susceptibility and esterase activity in citrus red mite Panonychus citri (McGregor) (Acari: Tetranychidae) after selection with Phoxim. International Journal of Acarology 35: 33–40.
Dekeyser, M. 2005.Acaricides mode of action. Pest Management Science 61: 103–110.
Doker, I. and Kazak. C. 2012. Detecting acaricides resistance in Turkish populations of Panonychus citri McGregor (Acari: Tetranychidae). Systematic and Applied Acarology 17(4): 368–377.
Feng, R. and Isman, M. B. 1995. Selection for resistance to azadirachtin in the green peach aphid, Myzus persicae. Cellular and Molecular Life Sciences 51: 831-833.
Gerson, U. and Cohen, E. 1989. Resurgences of spider mites (Acari: Tetranychidae) induced by synthetic Pyrethroid. Experimental and Applied Acarology 6: 29–46.
Habig, W. H., Pabst, M. J. and Jakoby, W. B. 1974. Glutathione S- transferase, the first step in mercapturic acid formation. Journal of Biological Chemistry 249: 7130-7139.
Hu, J., Wang, C., Wang, J., You, Y. and Chen, F. 2010. Monitoring of resistance to Spirodiclofen and five other acaricides in Panonychus citri collected from Chinese citrus orchards. Pest Management Science 66(9): 1025-1030.
Kasap, I. 2009. The biology and fecundity of the citrus red mite Panonychus citri (McGregor) (Acari: Tetranychidae) at different temperatures under laboratory conditions. Turkish Journal of Agriculture and Forestry 33(6): 593-600.
Khajehali, J., Van Leeuwen, T., Grispou, M., Morou, E., Alout, H., Weill, M., Tirry, L., Vontasc, J. and Tsagkarakou, A.  2010. Acetylcholinesterase point mutations in European strains of Tetranychus urticae (Acari: Tetranychidae) resistant to organophosphates. Pest Management Science 66: 220- 228.
Kim, Y. J., Park. H. M., Cho, J. R. and Ahn, y. j. 2006. Multiple resistance and biochemical mechanisms of pyridaben resistance in Tetranychus urticae (Acari: Tetranychidae). Journal of Economic Entomology 99(3): 954-958.
Kim, Y. J., Si-Hyeock, L., Si-Woo, L. and Ahn, Y. J. 2004. Fenpyroximate resistance in Tetranychus urticae (Acari: Tetranychidae) cross-resistance and biochemical resistance mechanisms. Pest Management Science 60: 1001- 1006.
Kumral, N. A. and Kovanci, B. 2007. Susceptibility of female populations of Panonychus ulmi (Koch) (Acari: Tetranychidae) to some acaricides in apple orchards. Journal of Pesticide Science 80:131–137.
LeOra Software, 2003. In: Robertson, J. L., Preisler, H.K., Russel, R. M. (Eds.), Polo Plus Probit and Logit Analysis, User’s Guide. Berkeley, p. 36.
Liao, C. Y., Xia, W. K., Feng, Y. C., Li, G., Liu. H., Dou, W. and Wang, J. J. 2015. Characterization and functional analysis of a novel Glutathione-S-transferases gene potentially associated with the abamectin resistance in Panonychus citri (McGregor). Pesticide Biochemistry and Physiology 132: 72-80.
Lin, H., Chuan-Hua, X., Jin-Jun, W., Ming, L., Wen-Cai, L. and Zhi-Mo, Z. 2009. Resistance selection and biochemical mechanism of resistance to two acaricides in Tetranychus cinnabarinus (Boiduval). Pesticide Biochemistry and Physiology 93: 47-52.
Liu, Y. H., Jiang, H. B., Yuan, M. L., Fan, F. H., Yang, L. H., Chen, J. and Wang, J. J. 2010. Resistance monitoring and synergism on four acaricides against Panonychus citri. Journal of Fruit Science 27(4): 570-574.
Luo, Y. J., Yang, Z. G., Xie, D. Y., Ding, W., Da, A. S., Ni, J., Chai, J. P., Huang, P., Jiang, X. J.  and Li, S. X. 2014.Molecular cloning and expression of Glutathione-S-transferases involved in propargite resistance 396 of the carmine spider mite, Tetranychus cinnabarinus (Boisduval). Pesticide Biochemistry and Physiology 114: 44-51.
Memarizadeh, N., Ghadamyari, M., Sajedi, R. H. and Jalali Sendi, J. 2011. Resistance mechanisms of Tetranychus urticae Koch (Acari: Tetranychidae) to abamectin. Journal of Plant Protection Sciences 42(1): 75-83. (in Farsi).
Meng, H. S., Wang, K. Y. and Jiang, X. Y. 2002. Studies on resistance selection by abamectin and Fenpropathrin and activity change of DE toxicant enzymes in Panonychus citri, Acta Entomological Sinica 45: 58–62.
Meng, H. S., Wang, K. Y., Jiang, X. Y. and Yi, M. Q. 2000. Studies on the resistance of Panonychus citri to several acaricides. Pesticides 39: 26–28.
Niu, J. Z., Liu, G. Y., Dou, W. and Wang, J. J. 2011. Susceptibility and activity of Glutathione-S-transferases in nine field populations of Panonychus citri (Acari: Tetranychidae) to Pyridabine and azocyclotin. Florida Entomologist 94: 321–329.
Norbakhsh, S. 2017. List of Important Pests, Diseases and Weeds of Major Agricultural Products, Recommended Methods and Pesticides for Their Control. Plant Protection Organization of Iran. 206 pp.
Ouyang, Y., Montez, G. H., Liu. L. and GraftonCardwell, E. E. 2012. Spirodiclofen and Spirotetramat bioassays for monitoring resistance in citrus red mite, Panonychus citri (Acari: Tetranychidae). Pest Management Science 68(5): 781-787.
Ran, C., Chen, Y. and Wang, J. J. 2009. Susceptibility and carboxylesterase activity of five field populations of Panonychus citri (McGregor) (Acari: Tetranychidae) to four acaricides. International Journal of Acarology 35: 115–121.
Rauch, N. and R. Nauen. 2003. Spirodiclofen resistance risk assessment in Tetranychus urticae (Acari: Tetranychidae): a biochemical approach. Pesticide Biochemistry and Physiology 74: 91–101.
Rodrigues, A. R. S., Torres, J. B., Siqueira, H. A. A. and Lacerda, D. P. A. 2013. Inheritance of lambda-cyhalothrin resistance in the predator lady beetle Eriopis connexa (Germar) (Coleoptera: Coccinellidae). Biological Control 64: 217– 224.
SAS Institute. 2001. SAS users guide: Statistics, version 8.2. SAS Institute, Cary, NC.
Sato, M. E., Silvs, M. Z. D., Raga, A. and Filo, M. F. D. S. 2005. Abamectin resistance in Tetranychus urticae Koch (Acari: Tetranychidae): selection, cross-resistance and stability of resistance. Neotropical Entomology 34(6): 991-998.
Sterk, G. and Versmissen, C. 1992. Recent developments with pyridaben for mite control on top fruit. Mededelingen van de Faculteit Landbouwwetenschappen, Rijksuniversiteit Gent 44: 941– 943.
Stumpf, N. and Nauen, R. 2001. Cross-resistance, inheritance, and biochemistry of mitochondrial electron transport inhibitor-acaricides resistance in Tetranychus urticae (Acari: Tetranychidae). Entomological Society of America 94(6): 1577-1583.
Talebi Jahromi, Kh. 2011. Toxicology of Pesticides. Tehran University Press. 507 p.
Tsagkarakou, A., van Leeuwen, T., Khajehali, J., Ilias, A., Grispou, M., Williamson, S., Tirry, L. and Vontas, J. 2009. Identification of Pyrethroid resistance associated mutations in the para sodium channel of the two spotted spider mite Tetranychus urticae (Acari: Tetranychidae). Insect Molecular Biology 18(5): 583-593.
Van Asperen, K. 1962. A study of housefly esterases by means of a sensitive colorimetric method. Journal of Insect Physiology 8: 401-416.
Van Leeuwen, T., Van Nieuwenhuyse, P., Vanholme, B., Dermauw, W., Nauen, R. and Tirry, L. 2011. Parallel evolution of cytochrome b mediated bifenazate resistance in the citrus red mite Panonychus citri. Insect Biochemistry and Molecular Biology 20: 135–140.
Van Pottelberge, S., Van Leeuwen, T., Nauen, R. and Tirry, L. 2009. Resistance mechanisms to mitochondrial electron transport inhibitors in a field-collected strain of Tetranychus urticae Koch (Acari: Tetranychidae). Bulletin of Entomological Research 99: 23-31.
Villanueva, R. T. and Walgenbach, J. F. 2006. Acaricidal properties of spinosad against Tetranychus urticae and Panonychus ulmi (Acari: Tetranychidae). Journal of Economic Entomology 99(3): 843-849.
 Yamamoto, A., Yoneda, H., Hatano, R. and Asada, M. 1995. Laboratory selections of populations in the citrus red mite, Panonychus citri (McGregor), with Hexythiazox and their cross resistance spectrum. Journal of Pesticide Science 20: 493-501.
Yang, X., Lawrent, L., Buschman, 1., Zhu, K. Y. and Margolies, D. C. 2002. Susceptibility and detoxifying enzyme activity in two spider mite species (Acari: Tetranychidae) after selection with three insecticides. Journal of Economic Entomology 95(2): 399-406.
Yorulmaz-Salman, S. and Ay, R. 2014. Determination of the inheritance, cross resistance and detoxifying enzyme levels of a laboratory-selected, spiromesifen-resistant population of the predatory mite Neoseiulus californicus (Acari: Phytoseiidae), Pest Management Science 94(6): 1577-1583.
Yu, D. Y., Wang, C. F., Yu, Y., Huang, Y. Q., Yao, J. A. and Hu, J. F. 2011. Laboratory selection for spirodiclofen resistance and cross-resistance in Panonychus citri. African Journal of Biotechnology 10(17): 3424-3429.