Detoxifying Enzyme Activities in the Common Pistachio Psylla and the Coccinellid Predator

Document Type : Original Research

Authors
1 Department of Plant Protection, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Islamic Republic of Iran.
2 Department of Plant Protection, Faculty of Agriculture, Vali-e-Asr University of Rafsanjan, Rafsanjan, Islamic Republic of Iran.
Abstract
The common pistachio psylla, Agonoscena pistaciae Burckhardt and Lauterer (Hem: Aphalaridae) is one of the main and most destructive pests of pistachio orchards in Iran. Chemical control is a widely applied method to manage this pest problem. The intensive use of insecticides has led to the development of resistant populations of the common pistachio psylla. In this research, the activities of detoxifying enzymes (general esterase, glutathione S-transferase and cytochrome P450) were assessed against two populations of the common pistachio psylla, and the coccinellid predator, Oenopia conglobata L. (Col: Coccinellidae) in Kerman Province, under treatment of three rational insecticides, namely, acetamiprid, spirotetramat, and hexaflumuron in four concentrations (control, LC25, LC50 and LC75). The results indicated that the activities of detoxifying enzymes were higher in the resistant population of psylla compared to the susceptible one. Esterase was the predominant detoxifying enzyme in the pest and its predator. Based on the results, the activity of detoxifying enzymes were higher at the higher concentrations of the pesticides. Esterase activity was greater in the psyllid populations than the coccinellid predator; which may indicate a higher sensitivity of the lady beetle to insecticides than its prey.

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Abdallah, I.S., Abou-Yousef, H.M., Fouad, E.A. and Kandil, M.A., 2016. The role of detoxifying enzymes in the resistance of the cowpea aphid (Aphis craccivora Koch) to thiamethoxam. J. Plant Prot. Res., 56(1): 67-72.
Alimohamadi, N., Samih, M.A., Izadi, H. and Shahidi-Noghabid, S., 2014. Developmental and biochemical effects of hexaflumuron and spirodiclofen on the ladybird beetle, Hippodamia variegata (Goeze) (Coleoptera: Coccinellidae). J. Crop Prot., 3(3): 335-344.
Alizadeh, A., Talebi, K., Hosseininaveh, V. and Ghadamyari, M., 2011. Metabolic resistance mechanisms to phosalone in the common pistachio psyllid, Agonoscena pistaciae (Hem.: Psyllidae). Pestic. Biochem. Physiol., 101(2): 59-64.
Amirzade, N., Izadi, H., Jalali, M.A. and Zohdi, H., 2014. Evaluation of three neonicotinoid insecticides against the common pistachio psylla, Agonoscena pistaciae, and its natural enemies. J. Insect Sci., 14(35): 1-8.
Bandaraa, K.M.U.J. and Karunaratne, S.H.P.P., 2017. Mechanisms of acaricide resistance in the cattle tick Rhipicephalus (Boophilus) microplus in Sri Lanka. Pestic. Biochem. Physiol., 139: 68-72.
Bemani, M., Moravvej, G., Izadi, H. and Sadeghi-Namaghi, H., 2018. Variation in insecticidal susceptibility of Agonoscena pistaciae Burckhardt and Lauterer (Hemiptera: Aphalaridae), and its coccinellid predator, Oenopia conglobata L. (Coleoptera: Coccinellidae). J. Kans. Entomol. Soc., 91(2): 110-118.
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. J. Am. Mosq. Control. 13: 133-137.
Bruck, E., Elbert, A., Fischer, R., Krueger, S., Kuhnhold, J., Klueken, A.M., Nauen, R., Niebes, J.F., Reckmann, U. and Schnorbach, H.J., 2009. Movento®, an innovative ambimobile insecticide for sucking insect pest control in agriculture: biological profile and field performance. Crop Prot., 28(10): 838-844.
Burckardt, D. and Lauterer, P., 1989. Systematics and biology of the Rhinocolinae (Homoptera: Psylloidea). J. Nat. Hist., 23: 643-712.
Casimiro, S., Coleman, M., Hemingway, J. and Sharp, B., 2006. Insecticide resistance in Anopheles arabiensis and Anopheles gambiae from Mozambique. J. Med. Entomol., 43: 276-282.
Cho, J.R., Kim, Y.J., Kim, H.S. and Yoo, J.K., 2002. Some biochemical evidence on the selective insecticide toxicity between the two aphids, Aphis citricola and Myzus malisuctus (Homoptera: Phididae), and their predator, Harmonia axyridis (Coleoptera: Coccinellidae). J. Asia-Pac. Entomol., 5(1): 49-53.
Claudianos, C., Ranson, H., Johnson, R.M., Biswas, S., Schuler, M.A., Berenbaum, M.R., Feyereisen, R. and Oakeshott, J.G., 2006. A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Mol Biol., 5: 615-636.
Croft, B.A., 1990. Arthropod Biological Control Agents and Pesticides. John Wiley and Sons Inc., 723 pp.
Devonshire, A.L. and Moores, G.D., 1982. A carboxylesterase with broad substrate specificity causes organophosphorus, carbamate and pyrethroid resistance in peach-potato aphids (Myzus persicae). Pestic. Biochem. Physiol., 18(2): 235-246.
Devorshak, C. and Roe, R.M., 1999. The role of esterases in insecticide resistance. Rev. Toxicol., 2(7): 501-537.
Elbert, A., Becker, B., Hartwig, J. and Erdelen, C., 1991. Imidacloprid–a new systemic insecticide. Pflanzenschutz Nachrichten Bayer, 44: 113–136.
Ferrari, J.A. and Georghiou, G.P., 1991. Quantitative genetic variation of esterase activity associated with a gene amplification in Culex quinquefasciatus. Hered., 66(Pt 2): 265-272.
Franca, S.M., Breda, M.O., Barbosa, D.R., Araujo, A.M. and Guedes, C.A., 2017. The sublethal effects of insecticides in insects. In: Shields V.D.C. (Editor), Biological Control of Pest and Vector Insects. Books on Demand, pp. 360.
Francis, S., Saavedra-Rodriguez, K., Perera, R., Paine, M., Black, W.C. and Delgoda, R., 2017. Insecticide resistance to permethrin and malathion and associated mechanisms in Aedes aegypti mosquitoes from St. Andrew Jamaica. PLos One, 12(6): https://doi.org/10.1371/journal.
Gong, Y.J., Wang, Z.H., Shi, B.C., Kang, Z.J., Zhu, L., Jin, G.H. and Wei, S.J., 2013. Correlation between pesticide resistance and enzyme activity in the diamondback moth, Plutella xylostella. J. Insect Sci., 13(135): Available online: www.insectscience.org/13.135.
Habig, W.H., Pabst, M.J. and Jakoby, W.B., 1976. Glutathione s-transferase AA form rat liver. Arch. Biochem. Biophys., 175: 710-716.
Halappa, B. and Patil, R.K., 2016. Detoxifying enzyme studies on cotton leafhopper, Amrasca biguttula biguttula (Ishida), resistance to neonicotinoid insecticides in field populations in Karnataka, India. J. Plant Prot. Res., 56(4).
Hodek, I., 1973. Biology of the Coccinellidae. Academic Publishing House of the Czechoslovak Academy of Science, Prague, 260 pp.
Kabiri Raeis Abbad, M. and Amiri Besheli, B., 2012. Bioassay of the botanical insecticide, tondexir, on two natural enemies of the common pistachio psyllid. Int. J. Agron. Plant Prod., 4(6): 1191-1196.
Kristensen, M., 2005. Glutathione S-transferase and insecticide resistance in laboratory strains and field populations of Musca domestica. J. Econ. Entomol., 98(4): 1341-1348.
Li, X., Schuler, M.A. and Berenbaum, M.R., 2007. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu. Rev. Entomol., 52: 231-253.
Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J., 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem., 193: 267-275.
Martin, P.D., Warwick, M.J., Dane, A.L., Hill, S.J., Giles, P.B., Phillips, P.J. and Lenz, E., 2003. Metabolism, excretion, and pharmacokinetics of rosuvastatin in healthy adult male volunteers. Clin. Ther., 25(11): 2822-2835.
Mehrnejad, M.R., 1998. Evaluation of the parasitoid Psyllaephagus pistaciae (Hymenoptera: Encyrtidae) as a biocontrol agent of the common pistachio psylla Agonoscena pistaciae (Hemiptera: Psylloidea), University of London, 189 pp.
Mehrnejad, M.R., 2007. Impact of predators on the spring population of the common pistachio psylla on wild pistachio trees, Proceedings of IUFRO conference, natural enemies and other multi-scale influence on forest insects, Vienna, Austria.
Mehrnejad, M.R. and Copland, M.J.W., 2005. Diapause strategy in the parasitoid Psyllaephagus pistaciae. Entomol. Exp. et Appl., 116: 109-114.
Mohammadzadeh, B., Ghadamyari, M., Sahragard, A. and Karimi-Malati, A., 2014. Sublethal effects of spinosad on some biochemical parameters of Xanthogaleruca luteola (Muller) (Coleoptera: Chrysomelidae). Plant Prot. Sci., 50(4): 199-204.
Mouches, C., Pasteur, N., Berge, J.B., Hyrien, O., Raymond, M., De Saint Vincent, B.R., De Silvestri, M. and Georghiou, G.P., 1986. Amplification of an esterase gene is responsible for insecticide resistance in a California Culex mosquito. Sci., 233: 778-781.
Mullin, C.A., Croft, B.A., Strickler, K., Matsumura, F. and Miller, J.R., 1982. Detoxification enzyme differences between an herbivorous and predatory mite. Sci., 217(4566): 1270-1272.
Nath, B.S., Suresh, A., Varma, B.M. and Kumar, R.P.S., 1997. Changes in protein metabolism in hemolymph and fat body of the silkworm, Bombyx mori (Lepidoptera: Bombycidae) in response to organophosphorus insecticides toxicity. Ecotoxicol. Environ. Saf., 36(2): 169-173.
Noorbakhsh, S., Sahramian, H., Sorush, M.J., Rezaii, V. and Fotuhi, A., 2001. The List of Pests and Diseases and Weeds of the Main Crops of Iran (The Recommended Pesticides and the Methods for Controlling Them). Ministry of Agriculture, Plant Protection Organization.
Oberlander, H. and Silhacek, D.L., 1998. New perspectives on the mode of action of benzoylphenyl urea insecticides. In: Ishaaya I. and Degheele D. (Editors), Insecticides with Novel Modes of Action. Pergamon Press, pp. 92-105.
Penilla, R.P., Rodriguez, A.D., Hemingway, J., Trejo, A., Loipez, A.D. and Rodriguez, M.H., 2007. Cytochrome P450-based resistance mechanism and pyrethroid resistance in the field Anopheles albimanus resistance management trial. Pestic. Biochem. Physiol, 89: 111-117.
Piri, F., Sahragard, A. and Ghadamyari, M., 2014. Sublethal effects of spinosad on some biochemical and biological parameters of Glyphodes pyloalis Walker (Lepidoptera: Pyralidae). Plant Prote. Sci., 50(3): 135-144.
Saha, D., 2016. Biochemical insecticide resistance in tea pests. In: Trdan S. (Editor), Agricultural and Biological Sciences "Insecticides Resistance".
Samih, M.A., Alizadeh, A. and Saberi Riseh, R., 2005. Pistachio Pests and Diseases in Iran and Their IPM. Jahad Daneshgahi Press.
Schroeder, M.E. and Flattum, R.F., 1984. The mode of action and neurotoxic properties of the nitromethylene heterocycle insecticides. Pestic Biochem Physiol., 22(2): 148-160.
Soleymanzade, A., Valizadegan, O. and Saryazdi, G.A., 2019. Biochemical mechanisms and cross resistance patterns of chlorpyrifos resistance in a laboratory-selected strain of diamondback Moth, Plutella xylostella (Lepidoptera: Plutellidae). J. Agri. Sci. Tech., 21: 1859-1870.
Suh, C.P.C., Orr, D.B. and Van Duyn, J.W., 2000. Effect of insecticides on Trichogramma exiguum (Hymenoptera: Trichogrammatidae) preimaginal development and adult survival. J. Econ. Entomol., 93: 577-583.
Tak, J., Jovel, E. and Isman, M.B., 2017. Effects of rosemary, thyme and lemongrass oils and their major constituents on detoxifying enzyme activity and insecticidal activity in Trichoplusia ni. Pestic. Biochem. Physiol., 140: 9-16.
Takada, Y., Kawamura, S. and Tanaka, T., 2001. Effects of various insecticides on the development of the egg parasitoid Trichogramma dendrolimi (Hymenoptera: Trichogrammatidae). J. Econ. Entomol., 94: 1340-1343.
Talebi, K.h., Rahmani Moghaddam, M. and Moharramipour, S., 2001. Susceptibility of different populations of pistachio psylla Agonoscena pistaciae to phosalone insecticide in Kerman province. Iran. J. Agric. Sci., 32: 495–500.
Tmimi, F.Z., Faraj, C., Bkhache, M., Mounaji, K., Failloux, A.B. and Sarih, H., 2018. Insecticide resistance and target site mutations (G119S ace-1 and L1014F kdr) of Culex pipiens in Morocco. Parasites Vectors, 11(51).
Tomberlin, J.K., Sheppard, D.C. and Joyce, J.A., 2002. Susceptibility of black soldier fly (Diptera: Stratiomyidae) larvae and adults to four insecticides. J. Econ. Entomol., 95: 598- 602.
Van-Asperen, K., 1962. A study of housefly esterase by means of a sensitive colorimetric method. J. Insect Physiol., 8: 401-416.
Van de Baan, H.E. and Croft, B.A., 1990. Factors influencing insecticide resistance in Psylla pyricola (Homoptera: Psyllidae) and susceptibility in the predator Deraeocoris brevis (Heteroptera: Miridae). Environ. Entomol., 19(5): 1223-1228.
Van Driesche, R.G. and Bellowa, J.R., 1996. Biological Control. Chapman and Hall, New York.
Willrich, M.M. and Boethel, D.J., 2001. Effects of diflubenzuron on Pseudoplusia includens (Lepidoptera : Noctuidae) and its parasitoid Copidosoma floridanum (Hymenoptera : Encyrtidae). Environ. Entomol., 30: 794-797.
Wu, G. and Miyatab, T., 2005. Susceptibilities to methamidophos and enzymatic characteristics in 18 species of pest insects and their natural enemies in crucifer vegetable crops. Pestic. Biochem. Physiol., 82: 79-93.
Xu, Z.B., Zou, X.P., Zhang, N., Feng, Q.L. and Zheng, S.C., 2015. Detoxification of insecticides, allechemicals and heavy metals by glutathione S-transferase SlGSTE1 in the gut of Spodoptera litura. Insect Sci., 22(4): 503-511.
Zhang, S., Zhang, X., Shen, J., Li, D., Wan, H., You, H. and Li, J., 2017. Cross-resistance and biochemical mechanisms of resistance to indoxacarb in the diamondback moth, Plutella xylostella. Pestic. Biochem. Physiol.
Zhou, C., Yang, H., Wang, Z., Long, G.Y. and Jin, D.C., 2019. Protective and detoxifying enzyme activity and ABCG subfamily gene expression in Sogatella furcifera under insecticide stress. Front. Physiol., 9.