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Host plant-based variation in fitness traits and major detoxifying enzymes activity in Scirtothrips dorsalis (Thysanoptera: Thripidae), an emerging sucking pest of tea

Published online by Cambridge University Press:  06 June 2016

Dhiraj Saha*
Affiliation:
Department of Zoology, Insect Biochemistry and Molecular Biology Laboratory, University of North Bengal, RajaRammohunpur, Siliguri-734013, District - Darjeeling, West Bengal, India
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Abstract

Scirtothrips dorsalis Hood is a polyphagous species and an important sucking pest of tea (Camellia sinensis) (Theaceae). The fitness traits of S. dorsalis on two alternative host plants: Capsicum annuum L. (chilli) (Solanaceae) and Ricinus communis (castor oil plant) (Euphorbiaceae) and on C. sinensis and corresponding levels of defence enzymes was studied. The study revealed that C. sinensis is the more suitable host of S. dorsalis based on faster development (13.6 days) compared to the alternative hosts, C. annuum (15.5 days) and R. communis (16.7 days), a higher fecundity (C. sinensis: 11.4 eggs; C. annuum: 9.7 eggs; R. communis: 8.6 eggs), and superior egg hatchability (C. sinensis, 92.6%; C. annuum: 82.5%; and R. communis: 74.6%). The host-based variation in the fitness traits of S. dorsalis corroborated in light of differential activity of three major detoxifying enzymes, such as the general esterases (GEs), glutathione S-transferases (GSTs), and cytochrome P450 mediated monooxygenases (CYPs). Densitometric analysis of GEs showed five esterase isozymes (EST I–V) with retardation factor (Rf) values of 0.17, 0.22, 0.27, 0.35 and 0.52, respectively. The pixel density, and accordingly the profile height, varied in different host-specific S. dorsalis. A significant variation of the quantity of these enzymes was also apparent in the insect when reared on the three hosts. A 2.4 and 2.7, 1.6 and 2.0, and 2.0 and 2.3-fold higher GEs, GSTs and CYPs activity on the two non-tea hosts possibly signify a predisposition of the species for higher tolerance to insecticides, enabling the pest to switch to tea where synthetic insecticides are routinely used.

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Research Paper
Copyright
Copyright © icipe 2016 

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References

Agosin, M. (1985) Role of microsomal oxidations in insecticide degradation, pp. 647712. In Comparative Insect Physiology, Biochemistry and Pharmacology (edited by Gilbert, L. I. and Kerkut, G. A.) Vol. 12. Pergamon, Oxford, UK.Google Scholar
Ahmad, S. (1986) Enzymatic adaptations of herbivorous insects and mites to phytochemicals. Journal of Chemical Ecology 12, 533560. doi: 10.1007/BF01020571.CrossRefGoogle ScholarPubMed
Ahmad, S., Brattsten, L. B., Mullin, C. A. and Yu, S. J. (1986) Enzymes involved in the metabolism of plant allelochemicals, pp. 73151. In Molecular Aspects of Insect–Plant Associations (edited by Brattsten, L. B. and Ahmad, S.). Plenum Press, New York, USA.CrossRefGoogle Scholar
Alonso-Pimentel, H., Korer, J. B., Nufio, C. and Papaj, D. R. (1998) Role of colour and shape stimuli in host-enhanced oogenesis in the walnut fly, Rhagoletis juglandis . Physiological Entomology 23, 97104. doi: 10.1046/j.1365-3032.1998.232076.x.CrossRefGoogle Scholar
Ananthakrishnan, T. N. (1993) Bionomics of thrips. Annual Review of Entomology 38, 7192. doi: 10.1146/annurev.en.38.010193.000443.CrossRefGoogle Scholar
Appel, H. M. and Martin, M. (1992) Significance of metabolic load in the evolution of host specificity of Manduca sexta . Ecology 73, 216228. doi: 10.2307/1938733.CrossRefGoogle Scholar
Awang, A., Muhamad, R. and Chong, K. K. (1988) Comparative merits of cocoa pod and shoot as food sources of the mirid, Helopeltis theobromae Miller. The Planter 64, 100104.Google Scholar
Awmack, C. S. and Leather, S. R. (2002) Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology 47, 817844. doi: 10.1146/annurev.ento.47.091201.145300.CrossRefGoogle ScholarPubMed
Banerjee, T. C. and Hoque, N. (1985) Influence of host plants on development, fecundity and egg hatchability of the arctiid moth Diacrisia casignetum . Entomologia Experimentalis et Applicata 37, 193198. doi: 10.1111/j.1570-7458.1985.tb03473.x.CrossRefGoogle Scholar
Berenbaum, M. R. (2002) Postgenomic chemical ecology: from genetic code to ecological interactions. Journal of Chemical Ecology 28, 873896.CrossRefGoogle ScholarPubMed
Berenbaum, M. R., Cohen, M. B. and Schuler, M. A. (1992) Cytochrome P450 monooxygenase genes in oligophagous Lepidoptera. ACS Symposium Series 505, 114124.CrossRefGoogle Scholar
Berenbaum, M. R., Zangerl, A. R. and Nitao, J. K. (1986) Constraints on chemical coevolution: wild parsnips and the parsnip webworm. Evolution 40, 12151228.CrossRefGoogle ScholarPubMed
Bernays, E. A. (1998) Evolution of feeding behavior in insect herbivores: success seen as different ways to eat without being eaten. Bioscience 48, 3544.CrossRefGoogle Scholar
Brattsten, L. B. (1979a) Ecological significance of mixed-function oxidations. Drug Metabolism Reviews 10, 3558. doi: 10.3109/03602537908993900.CrossRefGoogle ScholarPubMed
Brattsten, L. B. (1979b) Biochemical defense mechanisms in herbivores against plant allelochemicals, pp. 199270. In Herbivores: Their Interaction with Secondary Plant Metabolites (edited by Rosenthal, G. A. and Janzen, D. H.). Academic Press, New York, USA.Google Scholar
Brattsten, L. B. (1983) Cytochrome P-450 involvement in the interactions between plant terpenes and insect herbivores, pp. 173195. In Plant Resistance to Insects (edited by Hedin, P. A.). Symposium Series No. 208. American Chemical Society, Washington DC, USA.CrossRefGoogle Scholar
Brattsten, L. B., Evans, C. K., Bonetti, S. and Zalkow, L. H. (1984) Induction by carrot allelochemicals of insecticide-metabolising enzymes in the southern armyworm (Spodoptera eridania). Comparative Biochemistry and Physiology 77, 2937.Google ScholarPubMed
Brattsten, L. B., Wilkinson, C. F. and Eisner, T. (1977) Herbivore–plant interactions: mixed-function oxidases and secondary plant substances. Science 196, 13491352.CrossRefGoogle ScholarPubMed
Brogdon, W. G., McAllister, J. C. and Vulule, J. M. (1997) Heme peroxidase activity measured in single mosquitoes identifies individuals expressing an elevated oxidase for insecticide resistance. Journal of the American Mosquito Control Association 13, 233237.Google ScholarPubMed
Brough, C. N. and Dixon, A. F. G. (1990) The effects of starvation on development and reproductive potential of apterous virginoparae of vetch aphid Megoura viciae . Entomologia Experimentalis et Applicata 55, 4145.CrossRefGoogle Scholar
Castañeda, L. E., Figueroa, C. C. and Nespolo, R. F. (2010) Do insect pests perform better on highly defended plants? Costs and benefits of induced detoxification defences in the aphid Sitobion avenae . Journal of Evolutionary Biology 23, 24742483. doi: 10.1111/j.1420-9101.2010.02112.x.CrossRefGoogle ScholarPubMed
Das, G. M. (1965) Pests of tea in North-East India and their control, pp. 169173. In Tocklai Experimental Station Memorandum No. 27. Tocklai Experimental Station, Tea Research Association, Jorhat, Assam, India.Google Scholar
Després, L., David, J. P. and Gallet, C. (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends in Ecology and Evolution 22, 298307.CrossRefGoogle ScholarPubMed
Dethier, V. G. (1954) Evolution of feeding preferences in phytophagous insects. Evolution 8, 3354.CrossRefGoogle Scholar
Ehrlich, P. R. and Raven, P. H. (1964) Butterflies and plants: a study in coevolution. Evolution 18, 586608.CrossRefGoogle Scholar
Farazmand, H., Rassoulian, G. R. and Bayat-Assadi, H. (2000) Comparative notes on growth and development of red palm weevil, Rhynchophorus ferrugineus Oliv. (Col.: Curculionidae), on date palm varieties in Saravan Region. Journal of Entomological Society of Iran 19, 114.Google Scholar
Foster, S. P., Woodcock, C. M., Williamson, M. S., Devonshire, A. L., Denholm, I. and Thompson, R. (1999) Reduced alarm response by peach–potato aphids, Myzus persicae (Hemiptera, Aphididae), with knock-down resistance to insecticides (kdr) may impose a fitness cost through increased vulnerability to natural enemies. Bulletin of Entomological Research 89, 133138.CrossRefGoogle Scholar
Fraenkel, G. S. (1959) The raison d'etre of secondary plant substances. Science 129, 14661470. doi: 10.1126/science.129.3361.1466.CrossRefGoogle ScholarPubMed
Georghiou, G. P. and Pasteur, N. (1978) Electrophoretic esterase patterns in insecticide-resistant and susceptible mosquitoes. Journal of Economic Entomology 71, 201205.CrossRefGoogle ScholarPubMed
Giles, K. L., Madden, R. D., Stockland, R., Payton, M. E. and Dillwith, J. W. (2002) Host plants affect predator fitness via the nutritional value of herbivore prey: investigation of a plant–aphid–ladybeetle system. Biocontrol 47, 121.CrossRefGoogle Scholar
Gould, F. (1984) Mixed function oxidases and herbivore polyphagy: the devil's advocate position. Ecological Entomology 9, 2934. doi: 10.1111/j.1365-2311.1984.tb00695.x.Google Scholar
Govind, G., Mittapalli, O., Griebel, T., Allmann, S., Böcker, S. and Baldwin, I. T. (2010) Unbiased transcriptional comparisons of generalist and specialist herbivores feeding on progressively defenseless Nicotiana attenuata plants. PLoS One 5, e8735. doi:10.1371/journal.pone.0008735.CrossRefGoogle ScholarPubMed
Habig, W. H., Pabst, M. J. and Jakoby, W. B. (1974) Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. The 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. doi: 10.1146/annurev.ento.53.103106.093359.CrossRefGoogle ScholarPubMed
Hodgson, E. (1985) Microsomal monooxygenases, pp. 225331. In Comprehensive Insect Physiology, Biochemistry and Pharmacology (edited by Kerkut, G. A. and Gilbert, L. I.). Pergamon Press, Oxford, UK.Google Scholar
Hood, J. D. (1919) Two new genera and thirteen new species of Australian Thysanoptera. Proceedings of the Biological Society of Washington 32, 7592.Google Scholar
Iyengar, S., Arnason, J. T., Philogene, B. J. R., Werstiuk, N. H. and Morand, P. (1990) Comparative metabolism of the photoxic allelochemical α-terthienyl in three species of lepidopterans. Pesticide Biochemistry and Physiology 37, 154164.CrossRefGoogle Scholar
Ju, R.-T., Wang, F., Wan, F.-H. and Li, B. (2011) Effect of host plants on development and reproduction of Rhynchophorus ferrugineus (Olivier) (Coleoptera, Curculionidae). Journal of Pest Science 84, 3339.CrossRefGoogle Scholar
Kanno, H. and Harris, M. O. (2000) Physical features of grass leaves influence the placement of eggs within the plant by the Hessian fly. Entomologia Experimentalis et Applicata 96, 6980.CrossRefGoogle Scholar
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 (5), 12991340.CrossRefGoogle Scholar
Kennedy, G. G. (1984) 2-tridecanone, tomatoes and Heliothis zea: potential incompatibility of plant antibiosis with insecticidal control. Entomologia Experimentalis et Applicata 35, 305311. doi: 10.1111/j.1570-7458.1984.tb03396.x.CrossRefGoogle Scholar
Krieger, R. I., Feeny, P. P. and Wilkinson, C. F. (1971) Detoxication enzymes in the guts of caterpillars: an evolutionary answer to plant defenses? Science 172, 579581.CrossRefGoogle ScholarPubMed
Kumaresan, D., Regupathy, A. and Baskaran, P. (1988) Pests of Spices. Rajalakshmi Publications, Nagercoil, India. 241 pp.Google Scholar
Le, G. G. (2006) Xenobiotic response in Drosophila melanogaster: sex dependence of P450 and GST gene induction. Insect Biochemistry and Molecular Biology 36, 674682.Google Scholar
Leather, S. R. and Burnand, A. C. (1987) Factors affecting life-history parameters of the pine beauty moth, Panolis flammea (D&S): the hidden costs of reproduction. Functional Ecology 1, 331338. doi: 10.2307/2389789.CrossRefGoogle Scholar
Lee, K. (1991) Glutathione-S-transferase activities in phytophagous insects: induction and inhibition by plant phototoxins and phenols. Insect Biochemistry 21, 353361.CrossRefGoogle Scholar
Legrand, A. and Barbosa, P. (2000) Pea aphid (Homoptera, Aphididae) fecundity, rate of increase and within-plant distribution unaffected by plant morphology. Environmental Entomology 29, 987993. doi: 10.1603/0046-225X-29.5.987.CrossRefGoogle Scholar
Li, X., Berenbaum, M. R. and Schuler, M. A. (2002) Plant allelochemicals differentially regulate Helicoverpa zea cytochrome P450 genes. Insect Molecular Biology 11, 343351.CrossRefGoogle ScholarPubMed
Li, W., Schuler, M. A. and Berenbaum, M. R. (2003) Diversification of furanocoumarin-metabolizing cytochrome P450 in two papilionids: specificity and substrate encounter rate. Proceedings of the National Academy of Sciences USA 100 (Suppl. 2), 1459314598.CrossRefGoogle ScholarPubMed
Li, X., Schuler, M. A. and Berenbaum, M. R. (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology 52, 231253.CrossRefGoogle ScholarPubMed
Li, X., Zangerl, A. R., Schuler, M. A. and Berenbaum, M. R. (2000) Cross-resistance to alpha-cypermethrin after xanthotoxin ingestion in Helicoverpa zea (Lepidoptera: Noctuidae). Journal of Economic Entomology 93, 1825.CrossRefGoogle ScholarPubMed
Lindroth, R. L. (1989) Host plant alteration of detoxication activity in Papilio glaucus glaucus . Entomologia Experimentalis et Applicata 50, 2935. doi: 10.1007/BF00190125.CrossRefGoogle Scholar
Lindroth, R. L., Scriber, J. M. and Hsia, M. T. S. (1988) Chemical ecology of the tiger swallowtail: mediation of host use by phenolic glycosides. Ecology 69, 814822. doi: 10.2307/1941031.CrossRefGoogle Scholar
Lowry, O. H., Rosebrough, N. J., Farr, A. L. and Randall, R. J. (1951) Protein measurement with the folin phenol reagent. The Journal of Biological Chemistry 193, 265275.CrossRefGoogle ScholarPubMed
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
Mitter, C., Farrell, B. D. and Futuyma, D. J. (1991) Phylogenetic studies of insect/plant interactions: insights into the genesis of diversity. Trends in Ecology and Evolution 6, 290293.CrossRefGoogle ScholarPubMed
Mullin, C. A. (1986) Adaptive divergence of chewing and sucking arthropods to plant allelochemicals, pp. 175209. In Molecular Aspects of Insect–Plant Associations (edited by Brattsten, L. B. and Ahmad, S.). Plenum Press, New York, USA.CrossRefGoogle Scholar
Mullin, C. A., Croft, B. A., Strickler, K., Matsumura, F. and Miller, J. R. (1982) Detoxification enzyme differences between a herbivorous and predatory mite. Science 217, 12701272.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 & Hall, London, UK.CrossRefGoogle Scholar
Muraleedharan, N. (2007) Tea insects: ecology and control, pp. 672674. In Encyclopedia of Pest Management (edited by Pimentel, D.). CRC Press, London, UK.Google Scholar
Murphy, S. T. and Briscoe, B. R. (1999) The red palm weevil as an alien invasive: biology and the prospects for biological control as a component of IPM. Biocontrol News and Information 20, 35N–46N.Google Scholar
Neal, J. J. (1987) Metabolic costs of mixed-function oxidase induction in Heliothis zea . Entomologia Experimentalis et Applicata 43, 175179. doi: 10.1111/j.1570-7458.1987.tb03602.x.CrossRefGoogle Scholar
Nehare, S., Moharil, M. P., Ghodki, B. S., Lande, G. K., Bisane, K. D., Thakare, 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., Trejo, A., López, 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
Pffannenstiel, R. S. and Yeargan, K. V. (1998) Ovipositional preference and distribution of eggs in selected field and vegetable crops by Nabis roseipennis (Hemiptera, Nabidae). Journal of Entomological Science 33, 8289.CrossRefGoogle Scholar
Rattan, P. S. (1992) Pest and disease control in Africa in tea, pp. 331352. In Tea: Cultivation to Consumption (edited by Wilson, K. C. and Clifford, M. N.). Chapman & Hall, London, UK.CrossRefGoogle Scholar
Reilly, C. C., Gentry, C. R. and McVay, J. R. (1987) Biochemical evidence for resistance of rootstocks to the peachtree borer and species separation of peachtree borer and lesser peachtree borer (Lepidoptera, Sesiidae) on peach trees. Journal of Economic Entomology 80, 338343. doi: 10.1093/jee/80.2.338.CrossRefGoogle Scholar
Riley, D. G. and Tan, W. (2003) Host plant effects on resistance to bifenthrin in silverleaf whitefly (Homoptera: Aleyrodidae). Journal of Economic Entomology 96, 13151321.CrossRefGoogle ScholarPubMed
Rossiter, M. C. (1991a) Environmentally-based maternal effects: a hidden force in insect population dynamics? Oecologia 87, 288294. doi: 10.1007/BF00325268.CrossRefGoogle ScholarPubMed
Rossiter, M. C. (1991b) Maternal effects generate variation in life history: consequences of egg weight plasticity in the gypsy moth. Functional Ecology 5, 386393. doi: 10.2307/2389810.CrossRefGoogle Scholar
Rossiter, M. C., Cox-Foster, D. L. and Briggs, M. A. (1993) Initiation of maternal effects in Lymantria dispar: genetic and ecological components of egg provisioning. Journal of Evolutionary Biology 6, 577590.CrossRefGoogle Scholar
Saeed, R., Sayyed, A. H., Shad, S. A. and Zaka, S. M. (2010) Effect of different host plants on the fitness of diamond-back moth, Plutella xylostella (Lepidoptera: Plutellidae). Crop Protection 29, 178182.CrossRefGoogle Scholar
Saha, D. (2014) Assessment of population variability at subcellular level of some common sucking tea pests from Darjeeling Hill and its adjoining plain. PhD Thesis, University of North Bengal, Sliguri-734013, District-Darjeeling, West Bengal, India.Google Scholar
Saha, D. and Mukhopadhyay, A. (2013) Insecticide resistance mechanisms in three sucking insect pests of tea with reference to North East India: an appraisal. International Journal of Tropical Insect Science 33, 4670.CrossRefGoogle Scholar
Saha, D., Mukhopadhyay, A. and Bahadur, M. (2012a) Effect of host plants on fitness traits and detoxifying enzymes activity of Helopeltis theivora (Heteroptera, Miridae), a major sucking insect pest of tea. Phytoparasitica 40, 433444. doi: 10.1007/s12600-012-0244-2.CrossRefGoogle Scholar
Saha, D., Mukhopadhyay, A. and Bahadur, M. (2012b) Genetic diversity of Empoasca flavescens Fabricius (Homoptera: Cicadellidae), an emerging pest of tea from sub-Himalayan plantations of West Bengal, India. Proceedings of the Zoological Society 65, 126131.CrossRefGoogle Scholar
Saha, D., Roy, S. and Mukhopadhyay, A. (2012c) Seasonal incidence and enzyme-based susceptibility to synthetic insecticides in two upcoming sucking insect pests of tea. Phytoparasitica 40, 105115.CrossRefGoogle Scholar
Saha, D., Roy, S. and Mukhopadhyay, A. (2012d) Insecticide susceptibility and activity of major detoxifying enzymes in female Helopeltis theivora Waterhouse (Heteroptera: Miridae) from sub-Himalayan tea plantations of North Bengal, India. International Journal of Tropical Insect Science 32, 8593. doi: 10.1017/S1742758412000161.CrossRefGoogle Scholar
Saha, D., Mukhopadhyay, A. and Bahadur, M. (2013) Variation in the activity of three detoxifying enzymes in major sucking pest of tea, Helopeltis theivora Waterhouse (Heteroptera, Miridae) from sub-Himalayan tea plantations of West Bengal, India. Proceedings of Zoological Society 66 (2), 9299.CrossRefGoogle Scholar
Schuler, M. A. (1996) The role of cytochrome P450 monooxygenases in plant–insect interactions. Plant Physiology 112, 14111419.CrossRefGoogle ScholarPubMed
Scott, J. G., Liu, N. and Wen, Z. (1998) Insect cytochromes P450: diversity, insecticide resistance and tolerance to plant toxins. Comparative Biochemistry and Physiology - Part C: Pharmacology, Toxicology, and Endocrinology 121, 147155.Google 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
Terriere, L. C. (1984) Induction of detoxication enzymes in insects. Annual Review of Entomology 29, 7188. doi: 10.1146/annurev.en.29.010184.000443.CrossRefGoogle ScholarPubMed
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 (Hemiptera: Psyllidae). 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
Venette, R. C. and Davis, E. E.. (2004) Chilli Thrips/Yellow Tea Thrips, Scirtothrips dorsalis Hood (Thysanoptera, Thripidae) Mini Pest Risk Assessment. University of Minnesota, Saint Paul, Minnesota. 31 pp.Google Scholar
Wadleigh, R. W. and Yu, S. J. (1987) Glutathione transferase activity of fall armyworm larvae toward α, β-unsaturated carbonyl allelochemicals and its induction by allelochemicals. Insect Biochemistry 17, 759764.CrossRefGoogle Scholar
Wadleigh, R. W. and Yu, S. J. (1988) Detoxification of isocyanate allelochemicals by glutathione transferase in three lepidopterous species. Journal of Chemical Ecology 14, 12791288.CrossRefGoogle Scholar
Ward, S. A. and Dixon, A. F. G. (1982) Selective resorption of aphid embryos and habitat changes relative to life-span. Journal of Animal Ecology 51, 859864. doi: 10.2307/4010.CrossRefGoogle Scholar
Whittaker, R. H. and Feeny, P. P. (1971) Allelochemics chemical interactions between species. Science 171, 757770.CrossRefGoogle ScholarPubMed
Wink, M. (2003) Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64, 319.CrossRefGoogle ScholarPubMed
Wink, M. and Waterman, P. (1999) Chemotaxonomy in relation to molecular phylogeny of plants. Annual Plant Reviews 2, 300341.Google Scholar
Yang, X., Margolies, D. C., Zhu, K. Y. and Buschman, L. L. (2001) Host plant-induced changes in detoxyfication enzymes and susceptibility to pesticides in the twospotted spider mite (Acari: Tetranichidae). Journal of Economic Entomology 94, 381387.CrossRefGoogle Scholar
Yu, S. J. (1983) Induction of detoxifying enzymes by allelochemicals and host plants in the fall armyworm. Pesticide Biochemistry and Physiology 19, 330336.CrossRefGoogle Scholar
Yu, S. J. (1986) Host plant induction of microsomal monooxygenases in relation to organophosphate activation in fall armyworm larvae. The Florida Entomologist 69, 579587. doi: 10.2307/3495393.CrossRefGoogle Scholar
Yu, S. J. (1989) Β-glucosidase in four phytophagous Lepidoptera. Insect Biochemistry 19, 103108.CrossRefGoogle Scholar
Yu, S. J. (2008) The Toxicology and Biochemistry of Insecticides. CRC Press, Boca Raton, USA.Google Scholar
Yu, S. J. and Abo-Elghar, G. E. (2000) Allelochemicals as inhibitors of glutathione S-transferase in the fall armyworm. Pesticide Biochemistry and Physiology 68, 173183.CrossRefGoogle Scholar
Yu, S. J., Berry, R. E. and Terriere, L. C. (1979) Host plant stimulation of detoxifying enzymes in a phytophagous insect. Pesticide Biochemistry and Physiology 12, 280284.CrossRefGoogle Scholar
Yu, S. J. and Ing, R. T. (1984) Microsomal biphenyl hydroxylase of fall armyworm larvae and its induction by allelochemicals and host plants. Comparative Biochemistry and Physiology: - Part C: Comparative Pharmacology 78, 145152.CrossRefGoogle ScholarPubMed
Zeng, R. S., Zhimou, W., Goudong, N., Schular, M. A. and Berenbaum, M. (2007) Allelochemical induction of cytochrome P450 monooxygenases and amelioration of xenobiotic toxicity in Helicoverpa zea . Journal of Chemical Ecology 33, 449461.CrossRefGoogle ScholarPubMed