Skip to main content Accessibility help

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

  • Dhiraj Saha (a1), Somnath Roy (a1) and Ananda Mukhopadhyay (a1)


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.


Corresponding author


Hide All
Abbott, W. S. (1925) A method of computing the effectiveness of an insecticide. Journal of Economic Entomology 18, 265267.
Anonymous (1990) Proposed insecticide/acaricide susceptibility tests. IRAC method no. 7. Bulletin of the European Plant Protection Organization 20, 399400.
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.
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.
Brown, T. M. and Brogdon, W. G. (1987) Improved detection of insecticide resistance through conventional and molecular techniques. Annual Review of Entomology 32, 145162.
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.
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.
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.
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.
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.
Chen, Z. M. and Chen, X. F. (1989) An analysis of world tea fauna. Journal of Tea Science 9, 7388.
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.
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.
Cranham, J. E. (1966) Tea pests and their control. Annual Review of Entomology 11, 491514.
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.
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.
Devonshire, A. L. and Field, L. M. (1991) Gene amplification and insecticide resistance. Annual Review of Entomology 36, 123.
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.
Feyereisen, R. (1995) Molecular biology of insecticide resistance. Toxicology Letters 82 and 83, 8390.
Feyereisen, R. (1999) Insect P450 enzymes. Annual Review of Entomology 44, 507533.
Finney, D. J. (1973) Probit Analysis (3rd edn).Cambridge University Press, London.
Georghiou, G. P. (1972) The evolution of resistance to pesticides. Annual Review of Ecology and Systematics 3, 133168.
Georghiou, G. P. and Pasteur, N. (1978) Electrophoretic esterase pattern in insecticide resistant and susceptible mosquitoes. Journal of Economic Entomology 71, 201205.
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.
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.
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.
Hazarika, L. K., Bhuyan, M. and Hazarika, B. N. (2009) Insect pests of tea and their management. Annual Review of Entomology 54, 267284.
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.
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.
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.
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.
Kawai, A. (1997) Prospect for integrated pest management in tea cultivation in Japan. Japan Agricultural Research Quarterly 31, 213217.
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.
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.
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.
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.
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.
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.
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.
Muraleedharan, N. (2007) Tea insects: ecology and control, pp. 672674. In Encyclopedia of Pest Management, Vol. II (edited by Pimentel, D.). CRC Press, London.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Sannigrahi, S. and Talukdar, T. (2003) Pesticide use patterns in Dooars tea industry. Two and a Bud 50, 3538.
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.
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.
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.
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.
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.
Sivapalan, P. (1999) Pest management in tea, pp. 625646. In Global Advances in Tea Science (edited by Jain, N. K.). Aravali Books, New Delhi.
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.
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.
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.
van Asperen, K. (1962) A study of housefly esterases by means of a sensitive colorimetric method. Journal of Insect Physiology 8, 401416.
van Asperen, K. and Oppenoorth, F. J. (1959) Organophosphate resistance and esterase activity in houseflies. Entomologia Experimentalis et Applicata 2, 4857.
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.
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.
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.
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.
Yu, S. J. (1996) Insect glutathione S-transferases. Zoological Studies 35, 919.
Yu, S. J. (2008) The Toxicology and Biochemistry of Insecticides. CRC Press & Taylor and Francis Group, Boca Raton, FL.
Yu, S. J. and Nguyen, S. N. (1992) Detection and biochemical characterization of resistance in diamondback moth. Pesticide Biochemistry and Physiology 44, 7481.
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.
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.


Related content

Powered by UNSILO

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

  • Dhiraj Saha (a1), Somnath Roy (a1) and Ananda Mukhopadhyay (a1)


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.