Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-26T18:08:19.978Z Has data issue: false hasContentIssue false

Insecticide susceptibility and activity of major detoxifying enzymes in female Helopeltis theivora (Heteroptera: Miridae) from sub-Himalayan tea plantations of North Bengal, India

Published online by Cambridge University Press:  08 June 2012

Dhiraj Saha*
Affiliation:
Entomology Research Unit, Department of Zoology, University of North Bengal, Siliguri, Darjeeling734013, WB, India
Somnath Roy
Affiliation:
Entomology Research Unit, Department of Zoology, University of North Bengal, Siliguri, Darjeeling734013, WB, India
Ananda Mukhopadhyay
Affiliation:
Entomology Research Unit, Department of Zoology, University of North Bengal, Siliguri, Darjeeling734013, WB, India
Get access

Abstract

Despite the continuous use of synthetic insecticides during the last two decades, the tea mosquito bug Helopeltis theivora Waterhouse still exists as the most destructive pest of tea in North East India. The susceptibility levels of the female sucking bug collected from conventional (synthetic insecticide treated: Terai and Dooars plain regions) and organic (synthetic insecticide untreated: low-altitude Darjeeling region) tea plantations of the northern part of West Bengal to two synthetic insecticides, quinalphos and cypermethrin, and the activity of three principal detoxifying enzymes were assayed. Compared with the susceptible Darjeeling population, the Terai and Dooars populations showed a resistance factor at the lethal concentrations for 50% level ranging from 547- to 2680.87-fold and from 3810- to 7480-fold for quinalphos and cypermethrin, respectively. General esterases (GEs), glutathione S-transferases (GSTs) and cytochrome P450-mediated mono-oxygenases (CYPs) also showed an increased activity in the Terai and Dooars populations compared with those from Darjeeling. Defence enzyme activity was enhanced by 15.4- and 17.6-fold for GEs, 1.8- and 1.9-fold for GSTs and 2.1- and 2.4-fold for CYPs in the synthetic insecticide-treated H. theivora populations when compared with the untreated Darjeeling populations. Electrophoretic analysis for GEs showed a higher level of expression for esterase I–VI isozymes in the Terai and Dooars populations when compared with that in the Darjeeling populations. This study reveals a reduced efficacy of quinalphos and cypermethrin against field populations of H. theivora, possibly due to enhanced activities of GEs, GSTs and CYPs. The findings may be used in developing integrated resistance management strategies that can help in the effective control of this major tea pest.

Type
Research Paper
Copyright
Copyright © ICIPE 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abbott, W. S. (1925) A method of computing the effectiveness of an insecticide. Journal of Economic Entomology 18, 265267.CrossRefGoogle Scholar
Anonymous (1990) Proposed insecticide/acaricide susceptibility tests. IRAC method no. 7. Bulletin of the European Plant Protection Organization 20, 399400.Google Scholar
Bora, S., Sarmah, M., Rahaman, A. and Gurusubramanian, G. (2007) Relative toxicity of pyrethroid and nonpyrethroid insecticides against male and female tea mosquito bug Helopeltis theivora Waterhouse (Darjeeling strain). Journal of Entomological Research 31, 3741.Google Scholar
Brogdon, W. G., McAllister, J. C. and Vulule, J. M. (1997) Association of heme peroxidase activity measured in single mosquitoes identifies individuals expressing elevated oxidases for insecticide resistance. Journal of American Mosquito Control Association 13, 233237.Google Scholar
Brown, T. M. and Brogdon, W. G. (1987) Improved detection of insecticide resistance through conventional and molecular techniques. Annual Review of Entomology 32, 145162.CrossRefGoogle ScholarPubMed
Buès, R., Bouvier, J. C. and Boudinhon, L. (2005) Insecticide resistance and mechanisms of resistance to selected strains of Helicoverpa armigera (Lepidoptera: Noctuidae) in the south of France. Crop Protection 24, 814820.CrossRefGoogle Scholar
Cai, Q., Han, Y., Cao, Y., Hu, Y., Zhao, X. and Bi, J. (2009) Insecticide resistance and mechanisms of resistance to selected strains of Helicoverpa armigera (Lepidoptera: Noctuidae) in the south of France. Journal of Chemical Ecology 35, 320325.CrossRefGoogle Scholar
Campos, F., Dybas, R. A. and Kruba, D. A. (1995) Susceptibility of two-spotted spider mite (Acari: Tetranychidae) populations in California to abamectin. Journal of Economic Entomology 88, 225231.CrossRefGoogle Scholar
Cao, C. W., Zhang, J., Gao, X. W., Liang, P. and Guo, H. L. (2008) Overexpression of carboxylesterase gene associated with organophosphorous insecticide resistance in cotton aphids, Aphis gossypii (Glover). Pesticide Biochemistry and Physiology 90, 175180.CrossRefGoogle Scholar
Chaudhuri, T. C. (1999) Pesticide residues in tea, pp. 369378. In Global Advances in Tea Science (edited by Jain, N. K.). Aravali Books, New Delhi.Google Scholar
Chen, Z. M. and Chen, X. F. (1989) An analysis of world tea fauna. Journal of Tea Science 9, 7388.Google Scholar
Cheng, E. Y., Kao, C. H., Lin, D. F. and Trai, T. C. (1983) Insecticide resistance study in Plutella xylostella Lin. The specificity of oxidative detoxification mechanism in larval stage. Journal of Agriculture Research China 35, 375386.Google Scholar
Chen, S., Yang, Y. and Wu, Y. (2005) Correlation between fenvalerate resistance and cytochrome P450 mediated O-demethylation activity in Helicoverpa armigera (Lepidoptera: Noctuidae). Journal of Economic Entomology 98, 943946.CrossRefGoogle ScholarPubMed
Cranham, J. E. (1966) Tea pests and their control. Annual Review of Entomology 11, 491514.CrossRefGoogle Scholar
Das, G. M. (1965) Pests of Tea in North East India and their Control. Memorandom No. 27, pp. 169173. Tocklai Assam, India Experimental Station, Tea Research Association, Jorhat.Google Scholar
Devonshire, A. L. (1977) The properties of a carboxylesterase from the peach potato aphid, Myzus persicae (Sulz.), and its role in conferring insecticide resistance. Biochemistry Journal 167, 675683.CrossRefGoogle ScholarPubMed
Devonshire, A. L. and Field, L. M. (1991) Gene amplification and insecticide resistance. Annual Review of Entomology 36, 123.CrossRefGoogle ScholarPubMed
Ferrari, J. A., Morse, J. G., Georghiou, G. P. and Sun, Y. (1993) Elevated esterase activity and acetylcholinesterase insensitivity in citrus thrips (Thysanoptera: Thripidae) populations from the San Joaquin valley of California. Journal of Economic Entomology 86, 16451650.CrossRefGoogle Scholar
Feyereisen, R. (1995) Molecular biology of insecticide resistance. Toxicology Letters 82 and 83, 8390.CrossRefGoogle ScholarPubMed
Feyereisen, R. (1999) Insect P450 enzymes. Annual Review of Entomology 44, 507533.CrossRefGoogle ScholarPubMed
Finney, D. J. (1973) Probit Analysis (3rd edn).Cambridge University Press, London.Google Scholar
Georghiou, G. P. (1972) The evolution of resistance to pesticides. Annual Review of Ecology and Systematics 3, 133168.CrossRefGoogle Scholar
Georghiou, G. P. and Pasteur, N. (1978) Electrophoretic esterase pattern in insecticide resistant and susceptible mosquitoes. Journal of Economic Entomology 71, 201205.CrossRefGoogle ScholarPubMed
Gurusubramanian, G. and Bora, S. (2007) Relative toxicity of some commonly used insecticides against adults of Helopeltis theivora Waterhouse (Hemiptera: Miridae) collected from Jorhat area tea plantations, South Assam, India. Resistance Pest Management Newsletter 17, 812.Google Scholar
Gurusubramanian, G., Rahman, A., Sarmah, M., Roy, S. and Bora, S. (2008) Pesticide usage pattern in tea ecosystem, their retrospects and alternative measures. Journal of Environmental Biology 29, 813826.Google ScholarPubMed
Habig, W. H., Pabst, M. J. and Jakoby, W. B. (1974) Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry 249, 71307139.CrossRefGoogle ScholarPubMed
Hazarika, L. K., Bhuyan, M. and Hazarika, B. N. (2009) Insect pests of tea and their management. Annual Review of Entomology 54, 267284.CrossRefGoogle ScholarPubMed
Hemingway, J., Hawkes, N. J., McCarroll, L. and Ranson, H. (2004) The molecular basis of insecticide resistance in mosquitoes. Insect Biochemistry and Molecular Biology 34, 653665.CrossRefGoogle ScholarPubMed
Hodgson, E. and Kulkarni, A. P. (1983) Characterization of cytochrome P450 in studies of insecticide resistance, pp. 207228. In Pest Resistance to Pesticides (edited by Georghiou, G. P. and Saito, T.). Plenum Press, New York.CrossRefGoogle Scholar
Hsu, J. C., Feng, H. T. and Wu, W. J. (2004) Resistance and synergistic effects of insecticides in Bactrocera dorsalis (Diptera: Tephritidae) in Taiwan. Journal of Economic Entomology 97, 16821688.CrossRefGoogle ScholarPubMed
Kao, C. H., Hung, C. F. and Sun, C. N. (1989) Parathion and methyl parathion resistance in diamondback moth (Lepidoptera: Plutellidae) larvae. Journal of Economic Entomology 82, 12991304.CrossRefGoogle Scholar
Kawai, A. (1997) Prospect for integrated pest management in tea cultivation in Japan. Japan Agricultural Research Quarterly 31, 213217.Google Scholar
Komagata, O., Kasai, S. and Tomita, T. (2010) Overexpression of cytochrome P450 genes in pyrethroid-resistant Culex quinquefasciatus. Insect Biochemistry and Molecular Biology 40, 146152.CrossRefGoogle ScholarPubMed
Limoee, M., Enayati, A. A., Ladonni, H., Vatandoost, H., Baseri, H. and Oshaghi, M. A. (2007) Various mechanisms responsible for permithrin metabolic resistance in seven field collected strains of the German cockroach from Iran, Blattella germanica (L.) (Dictyoptera: Blattellidae). Pesticide Biochemistry and Physiology 87, 138146.CrossRefGoogle Scholar
Lowry, O. H., Rosebrough, N. J., Farr, A. L. and Randall, R. J. (1951) Protein measurement with the folin phenol reagent. Journal of Biological Chemistry 193, 265275.CrossRefGoogle ScholarPubMed
Markussaen, M. D. K. and Kristensen, M. (2010) Cytochrome P450 monooxygenase-mediated neonicotinoid resistance in the house fly Musca domestica L. Pesticide Biochemistry and Physiology 98, 5058.CrossRefGoogle Scholar
Martin, T., Chandre, F., Ochou, O. G., Vaissayre, M. and Fournier, D. (2002) Pyrethroid resistance mechanisms in the cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae) from West Africa. Pesticide Biochemistry and Physiology 74, 1726.CrossRefGoogle Scholar
Maymo, A. C., Cervera, A., Sarabia, R., Martínez-Pardo, R. and Garcera, M. D. (2002) Evaluation of metabolic detoxifying enzyme activities and insecticide resistance in Frankliniella occidentalis. Pest Management Science 58, 928934.CrossRefGoogle ScholarPubMed
Muraleedharan, N. (1992) Pest control in Asia, pp. 375412. In Tea: Cultivation to Consumption (edited by Wilson, K. C. and Clifford, M. N.). Chapman and Hall, London.CrossRefGoogle Scholar
Muraleedharan, N. (2007) Tea insects: ecology and control, pp. 672674. In Encyclopedia of Pest Management, Vol. II (edited by Pimentel, D.). CRC Press, London.Google Scholar
Nehare, S., Moharil, M. P., Ghodki, B. S., Lande, G. K., Bisane, K. D., Thakre, A. S. and Barkhade, U. P. (2010) Biochemical analysis and synergistic suppression of indoxacarb resistance in Plutella xylostella L. Journal of Asia Pacific Entomology 13, 9195.CrossRefGoogle Scholar
Penilla, R. P., Rodriguez, A. D., Hemingway, J., Trezo, A., Lopez, A. D. and Rodriguez, M. H. (2007) Cytochrome P450-based resistance mechanism and pyrethroid resistance in the field Anopheles albimanus resistance management trial. Pesticide Biochemistry and Physiology 89, 111117.CrossRefGoogle Scholar
Perera, M. D. B., Hemingway, J. and Karunaratne, S. H. P. P. (2008) Multiple insecticide resistance mechanisms involving metabolic changes and insensitive target sites selected in anopheline vectors of malaria in Sri Lanka. Malaria Journal 7, 168.CrossRefGoogle ScholarPubMed
Rattan, P. S. (1992) Pest and disease control in Africa, pp. 331352. In Tea: Cultivation to Consumption (edited by Wilson, K. C. and Clifford, M. N.). Chapman and Hall, London.CrossRefGoogle Scholar
Roy, S., Gurusubramanian, G. and Mukhopadhyay, A. (2008 a) Insecticide persistence and residual toxicity monitoring in tea mosquito bug Helopeltis theivora Waterhouse (Heteroptera: Hemiptera: Miridae) in Dooars, West Bengal. Resistant Pest Management Newsletter 17, 915.Google Scholar
Roy, S., Mukhopadhyay, A. and Gurusubramanian, G. (2008 b) Use pattern of insecticides in tea estates of the Dooars in North Bengal, India. North Bengal University Journal of Animal Science 2, 3540.Google Scholar
Roy, S., Mukhopadhyay, A. and Gurusubramanian, G. (2009) The synergistic action of piperonyl butoxide on toxicity of certain insecticides applied against Helopeltis theivora Waterhouse (Heteroptera: Miridae) in the Dooars tea plantations of North Bengal India. Journal of Plant Protection Research 49, 226229.CrossRefGoogle Scholar
Roy, S., Gurusubramanian, G. and Mukhopadhyay, A. (2010 a) Neem-based integrated approaches for the management of tea mosquito bug, Helopeltis theivora Waterhouse (Miridae: Heteroptera) in tea. Journal of Pest Science 83, 143148.CrossRefGoogle Scholar
Roy, S., Mukhopadhyay, A. and Gurusubramanian, G. (2010 b) Development of resistance to endosulphan in populations of the tea mosquito bug Helopeltis theivora (Heteroptera: Miridae) from organic and conventional tea plantations in India. International Journal of Tropical Insect Science 30, 6166.CrossRefGoogle Scholar
Sannigrahi, S. and Talukdar, T. (2003) Pesticide use patterns in Dooars tea industry. Two and a Bud 50, 3538.Google Scholar
Sarker, M. and Mukhopadhyay, A. (2003) Expression of esterases in different tissues of the tea pest, Helopeltis theivora exposed and unexposed to synthetic pesticide sprays from Darjeeling foothills and plains. Two and a Bud 50, 2830.Google Scholar
Sarker, M. and Mukhopadhyay, A. (2006) Studies on some enzymes related to insecticide resistance in Helopeltis theivora Waterhouse (Insecta: Heteroptera: Miridae) from Darjeeling foothills and plains. Journal of Plantation Crops 34, 423428.Google Scholar
Sarker, M., Bhattacharyya, I. K., Borkotoki, A., Goswami, D., Rabha, B., Baruah, I. and Srivastava, R. B. (2009) Insecticide resistance and detoxifying enzyme activity in principal bancroftian filariasis vector, Culex quinquefasciatus, in northeastern India. Medical and Veterinary Entomology 23, 122131.CrossRefGoogle Scholar
Scharf, M. E., Neal, J. J. and Bennett, W. G. (1998) Changes of insecticide resistance levels and detoxifying enzymes following insecticide selection in the German cockroach, Blattella germanica L. Pesticide Biochemistry and Physiology 59, 6779.CrossRefGoogle Scholar
Shono, T., Ohsawa, K. and Casida, J. E. (1979) Metabolism of trans and cis-permithrin, trans and cis-cypermethrin and deltamethrin by microsomal enzymes. Journal of Agricultural and Food Chemistry 27, 316325.CrossRefGoogle ScholarPubMed
Sivapalan, P. (1999) Pest management in tea, pp. 625646. In Global Advances in Tea Science (edited by Jain, N. K.). Aravali Books, New Delhi.Google Scholar
Soderlund, D. M. and Bloomquist, J. R. (1990) Molecular mechanisms of insecticide resistance, pp. 5896. In Pesticide Resistance in Arthropods (edited by Roush, R. T. and Tabashnik, B. E.). Chapman and Hall, New York/London.CrossRefGoogle Scholar
Sundaraju, D. and Sundara Babu, P. C. (1999) Helopeltis spp. (Heteroptera: Miridae) and their management in plantation and horticultural crops of India. Journal of Plantation Crops 27, 155174.Google Scholar
Tiwari, S., Pelz-Stelinski, K., Mann, R. S. and Stelinski, L. L. (2011) Glutathione-S-transferase and cytochrome P450 activity levels in Candidatus Liberibacter asiaticus-infected and uninfected Asian citrus psyllid, Diaphorina citri. Annals of the Entomological Society of America 104, 297305.CrossRefGoogle Scholar
van Asperen, K. (1962) A study of housefly esterases by means of a sensitive colorimetric method. Journal of Insect Physiology 8, 401416.CrossRefGoogle Scholar
van Asperen, K. and Oppenoorth, F. J. (1959) Organophosphate resistance and esterase activity in houseflies. Entomologia Experimentalis et Applicata 2, 4857.CrossRefGoogle Scholar
van Asperen, K. and Oppenoorth, F. J. (1960) The interaction between organophosphorus insecticides and esterases in homogenates of organophosphate susceptible and resistant houseflies. Entomologia Experimentalis et Applicata 3, 6883.CrossRefGoogle Scholar
Wu, G., Jiang, S. and Miyata, T. (2004) Seasonal changes of methamidophos susceptibility and biochemical properties in Plutella xylostella (Lepidoptera: Yponomeutidae) and its parasitoid, Cotesia plutellae (Hymenoptera: Braconidae). Journal of Economic Entomology 97, 16891698.CrossRefGoogle ScholarPubMed
Wu, S., Yang, Y., Yuan, G., Cambell, P. M. and Teese, M. G. (2011) Overexpressed esterases in a fenvalerate resistant strain of the cotton bollworm, Helicoverpa armigera. Insect Biochemistry and Molecular Biology 41, 1421.CrossRefGoogle Scholar
Yang, Y., Wu, Y., Chen, S., Devine, G. J., Denholm, I., Jewess, P. and Moores, G. D. (2004) The involvement of microsomal oxidases in pyrethroid resistance in Helicoverpa armigera from Asia. Insect Biochemistry and Molecular Biology 34, 763773.CrossRefGoogle ScholarPubMed
Yu, S. J. (1996) Insect glutathione S-transferases. Zoological Studies 35, 919.Google Scholar
Yu, S. J. (2008) The Toxicology and Biochemistry of Insecticides. CRC Press & Taylor and Francis Group, Boca Raton, FL.Google Scholar
Yu, S. J. and Nguyen, S. N. (1992) Detection and biochemical characterization of resistance in diamondback moth. Pesticide Biochemistry and Physiology 44, 7481.CrossRefGoogle Scholar
Yu, S. J., Nguyen, S. N. and Abo-Elghar, G. E. (2003) Biochemical characteristics of insecticide resistance in the fall armyworm, Spodoptera frugiperda (J.E. Smith). Pesticide Biochemistry and Physiology 77, 111.CrossRefGoogle Scholar
Zhu, Y. C., West, S., Snodgrass, G. and Luttrell, R. (2011) Variability in resistance-related enzyme activities in field populations of the tarnished plant bug, Lygus lineolaris. Pesticide Biochemistry and Physiology 99, 265273.CrossRefGoogle Scholar