Inhibition of antennal response of the tomato leaf miner males, Tuta absoluta (Lepidoptera: Gelechiidae) to its sex pheromone under the influence of three insecticides in an electrophysiological study

Document Type : Paper, Persian

Authors

1 Department of Plant Protection, College of Agriculture, Shahid Chamran University of Ahwaz, Iran.

2 Department of Plant Protection, College of Agriculture, Zanjan University, Zanjan, Iran.

3 Department of Chemical Ecology, Fondazione Edmund Mach, Research and Innovation Centre, San Michele all’Adige, TN, Italy

Abstract

The tomato leaf miner moth Tuta absoluta Meyrick is an invasive pest of tomato which damages this crop economically in greenhouse and field conditions. Due to the endophytic feeding habits of larvae and the high fecundity, the resistant populations has developed. Based on the effect of chemical pesticides on the mating disruption efficacy, it is therefore possible to exploit novel approaches on the use of insecticides against this pest. In this study, the efficacy of 3 insecticides, imidaclopride, indoxacarb and NeemAzal, with different mode of action, in 4 concentrations (0, 1, 10, 100 μg/ml) were assayed on Electroantennogram response of antennal receptors of 2-3 days old males to sex pheromone. The antennal responses rate to sex pheromone were measured during 6 time intervals, after insecticide spray and were calculated as inhibitory percentage in comparison to the response rate before spray and the data was analysis by repeated measure method. The results showed a significant difference between different concentrations of each insecticides compared to the control, the time of EAG assay and also the interaction effects of these factors, while, there was no significantly difference between tested pesticides. All insecticides were inhibited the antennal response in range of 18-20%. There was a dose- dependent relationship between concentration levels of each insecticides and the highest inhibition percentage was calculated in 100 μg/ml. The results confirmed the inhibitory effect of the tested insecticides on the antennal receptors leading to disruption of their response to sex pheromone.

Keywords

References

Ahmad, S., Ansari, M. S. & Muslim, M. (2015) Toxic effects of neem based insecticides on the fitness of Helicoverpa armigera (Hübner). Crop Protection 68, 72-78.
Anjum, S. I., Yousf, M. J., Ayaz, S. & Siddiqui, B. S. (2010) Toxicological Evaluation of chlorpyrifos and neem extract (Biosal B) against 3rd instars larvae of Drosophila melanogaster. The Journal of Animal & Plant Sciences 20, 9-12.
Ansebo, L., Coracini, M. D. A., Bengtsson, M., Liblikas, I., Ramirez, M., Borg-Karlson, A. K., Tasin, M. & Witzgall, P. (2004) Antennal and behavioural response of codling moth Cydia pomonella to plant volatiles. Journal of Applied Entomology 128, 488–493.
Anton, S. & Gadenne, C. (1999) Effect of juvenile hormone on the central nervous processing of sex pheromone in an insect. Proceedings of the National Academy of Sciences USA 96, 5764-5767.
Barrett, B. A. (2008) Assessment of methoxyfenozide exposure on the sexual attractiveness and responsiveness of adult codling moth, Cydia pomonella (L.), in small orchard blocks. Pest Management Science 64, 916–922.
Barrett, B. A. (2010) Exposure to methoxyfenozide-treated surfaces reduces the responsiveness of adult male codling moth (Lepidoptera: Tortricidae) to codlemone and pear ester lures in a wind tunnel. Journal of Economic Entomology 103, 1704–1710.
Batista-Pereira, L. G., Fernandes, J. B., Corrêa, A. G., Da Silva, M. F. G. F. & Vieira, P. C. (2006) Electrophysiological responses of eucalyptus brown looper Thyrinteina arnobia to essential oils of seven Eucalyptus species. Journal of Brazilian Chemical Society 17, 555-561.
Bawin, T., Collard, F., De Backer, L., Yarou, B. B, Compére, P., Francis, F. & Verheggen, F. J. (2017) Structure and distribution of the sensilla on the antennae of Tuta absoluta (Lepidoptera: Gelechiidae). Micron 96, 16-28.
Beck, J. J., Light, D. M. & Gee, S. W. (2014) Electrophysiological responses of male and female Amyelois transitella antennae to pistachio and almond host plant volatiles. Entomologia Experimentalis et Applicata 153, 217–230.
Cardé, T. R & Millar, G. J. (2004) Advances in insect chemical ecology. 275pp. Cambridge University Press, New York.
Chaudhary, S., Kanwar, R. K., Sehgal, A., Cahill, D. M., Barrow, C. J., Sehgal, R. & Kanwar, J. R. (2017) Progress on Azadirachta indica based biopesticides in replacing synthetic toxic pesticides. Frontiers in Plant Science 8, 1-13.
Chertemps, T., François, A., Durand, N., Roseel, G., Dekker, T., Lucas, Ph. & Maȉbèche-Coisne, M. (2012) A carboxylesterase, esterase 6. Modulates sensory physiological and behavioral response dynamics to pheromone in Drosophila. BMC. Biology 10, 1-12.
Clark, D. C. & Haynes, K. F. (1992) Sublethal effects of Cypermethrin on chemical communication, courtship, and oviposition in the Cabbage looper (Lepidoptera: Noctuidae). Journal of Economic Entomology 85, 1771-1778.
Delpuech, J. M., Legallet, B. & Fouillet, P. (2001) Partial compensation of the sublethal effect of detamethrin on the sex pheromonal communication of Trichogramma brassicae. Chemosphere 42, 985–991.
Desneux, N., Decourtye, A., & Delpuech, J. M. (2007) The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology 52, 81–106.
Dominguez, A., Puigmart, M., Bosch, M. P., Rosell, G., Crehuet, R., Ortiz, A., Quero, C. & Guerrero, A. (2016) Synthesis, functional assays, electrophysiological activity, and field tests of pheromone antagonists of the tomato leaf miner, Tuta absoluta. Journal of Agricultural and Food Chemistry 64, 3523-3532.
Durand, N., Carot-Sans, G., Bozzolan, F., Rosell, G., Siaussat, D., Debermard, S., Chertemps, T. & Maibèch-Coisne, M. (2011) Degradation of pheromone and plant volatile compounds by some odorant degrading enzyme in Spodoptera litteralis. PLos ONE 6, 12. e 29147.
El-Sayed, A. M., Byers, J. A., Manning, L. M., Jürgens, A., Mitchell, J. V. & Suckling, D. M. (2008) Floral scent Canada thistle and its potential as a generic insect attractant. Journal of Economic Entomology 101, 720-727.
EPPO: European and Mediterranean Plant Protection Organization. (2005) Data sheets on quarantine pests: Tuta absoluta. EPPO Bulletin 35, 434–435.
Floyd, M. A., Evans, D. A. & Howse, Ph. E. (1976) Electrophysiological and behavioural studies on naturally occurring repellents to Reticulitermes lucifugus. Journal of Insect Physiology 22, 697-701.
Fraser, A. M., Mechaber, W. L. & Hildebrand, J. G. (2003) Electroantennographic and behavioral responses of the sphinx moth Manduca sexta to host plant headspace volatiles. Journal of Chemical Ecology 29, 1813-1833.
Germinara, G. S., De Cristofaro, A. & Rotundo, G. (2016) Electrophysiological and behavioral responses of Theocolax elegans (Westwood) (Hymenoptera: Pteromalidae) to cereal grain volatiles. BioMed Research International 2016, 1-8.
Giner, M., Sans, A., Riba, M., Bosch, D., Gago, R., Rayo, J., Rosell, G. & Guerrero, A. (2009) Development and biological activity of a new antagonist of the pheromone of the codling moth. Journal of Agricultural & Food Chemistry 57, 8514-8519.
Gunasekaran, K., Vijayakumar, T. & Kalyanasundaram, M. (2009) Larvicide and emergence inhibitory activities of NeemAzal T/S 1.2 per cent EC against vectors of malaria, filariasis and dengue. Indian Journal of Medical Research 130, 138-145.
Hansson, B. S. (1995) Olfaction in Lepidoptera. Experientia 51, 1003-1027.
Haynes, K. F. (1988) Sublethal effects of neurotoxic insecticides on insect behavior. Annual Review of Entomology 33, 149-168.
IBM SPSS Statistics for Windows, Version 21.0. (2012) Armonk, NY: IBM Corp. Command Syntax Reference, Chicago, Illinois: SPSS Inc. 
Jactel, H., Birgersson, G., Andersson, S. & Schlyter, F. (2011) Non-host volatiles mediate associational resistance to the pine processionary moth. Oecologia 166, 703–711.
Kaissling, K. E. (1987) R. H. Wright lectures on insect olfaction. Burnaby, B. C., Canada: Simon Fraser University.
Lietti, M. M. M., Botto, E. & Alzogaray, R. A. (2005) Insecticide Resistance in Argentine Populations of Tuta absoluta (Lepidoptera: Gelechiidae). Neotropical Entomology 34, 113-19.
Lòpez, S., Quero, C., Iturrondobeitia, J. C., Guerrero, A. & Goldarazena, A. (2013) Electrophysiological and behavioural responses of Pityophthorus pubescens (Coleoptera: Scolytinae) to (E,E)-α-farnesene, (R) (+)-limonene and (S)-(−)-verbenone in Pinus radiata (Pinaceae) stands in northern Spain. Pest Management Science 69, 40-47. 
Lucas, P. & Renou, M. (1992) Electrophysiological study of the effects of deltamethrin, bioresmethrin, and DDT on the activity of pheromone receptor neurons in 2 moth species. Pesticide Biochemistry and Physiology43, 103–115.
Malo, E. A., Rojas, J. C., Gago, F. & Guerrero, A. (2013) Inhibition of the responses to sex pheromone of the fall armyworm, Spodoptera frugiperda. Journal of Insect Science 13, 1-14. 
Megido, R. C., Haubruge, E. & Verheggen, F. J. (2013) Pheromone-based management strategies to control the tomato leaf miner, Tuta absoluta (Lepidoptera: Gelechiidae). A review. Biotechnology, Agronomy, Society & Environment Journal 17, 475-82.
Moore, R. F. (1988) Inhibition of chemical communication between male and female bollworms (Lepidoptera, Noctuidae) by sublethal amounts of permethrin. Journal of Economic Entomology 81, 78–82.
Nathan, S. S, Choia, M. Y., Seoa, Y.H., Paika, H. C., Kalaivani, K. & Kima, J. D. (2008) Effect of azadirachtin on acetylcholinesterase (AChE) activity and histology of the brown planthopper Nilaparvata lugens (Stål). Ecotoxicology and Environmental Safety 70, 244–250.
Nauen, R., Ebbinghaus-Kintscher, U., & Schmuck, R. (2001) Toxicity and nicotinic acetylcholine receptor interaction of imidacloprid and its metabolites in Apis mellifera (Hymenoptera: Apidae). Pest Management Science 57, 577–586.
Oliveira, E. E., Schleicher, S., Buschges, A., Schmidt, J., Kloppenburg, P. & Salgado, V. L. (2011) Desensitization of nicotinic acetylcholine receptors in central nervous system neurons of the stick insect (Carausius morosus) by imidacloprid and sulfoximine insecticides. Insect Biochemistry & Molecular Biology 41, 872–880.
Paduraru, P. M., Popoff, R. T. W., Nair, R., Gries, R., Gries, G. & Plettner, E. (2008) Synthesis of substituted alkoxy benzene minilibraries, for the discovery of new insect olfaction or gustation inhibitors. Journal of Combinatorial Chemistry 10, 123-134.
Pandey, J. P. & Tiwari, R. K. (2011) Neem based insecticides intraction with development and fecundity of Red Cotton Bug, Dysdercus cingulatus Fab. International Journal of Agricultural Research 6, 335-346.
Pandey, J. P. & Tiwari, R. K. (2011) Neem based insecticides intraction with development and fecundity of Red Cotton Bug, Dysdercus cingulatus Fab. International Journal of Agricultural Research 6, 335-346.
Party, V., Hanot, Ch., Said, I, Rochat, D. & Renou, M. (2009) Plant terpenes affect intensity and temporal parameters of pheromone detection in a moth. Chemical Senses 34, 763-774.
Pophof, B., Gebauer, T. & Ziegelberger G. (2000) Decyl thio-trifluoropropane, a competitive inhibitor of moth pheromone receptor. Journal of Comparative Physiology 186, 315-323.
Prestwich, G. D. & Streinz L. (1988) Haloacetate analogs of pheromones: effects on catabolism and electrophysiology in Plutella xylostella. Journal of Chemical Ecology 14, 1003–1021.
Puigmarti, M., Bosch, M. P. & Guerrero, A. (2015) An improved and convenient new synthesis of the pheromone components of the tomato leafminer Tuta absoluta. Synthesis 47, 961-968.
Rabhi, K. K., Deisig, N., Demondion, E., Le Corre, J., Robert, G., Tricoire-Leignel, H., Lucas, P. Gadenne, C. & Anton, A. (2016) Low doses of a neonicotinoid insecticide modify pheromone response thresholds of central but not peripheral olfactory neurons in a pest insect. Proceedings Biological Sciences Royal Society of London B 283, 1-7.
Rabhi, K. K., Esancy, K., Voisin, A., Crespin, L., Le Corre, J., Tricoire-Leignel, H., Anton, S. & Gadenne, C. (2014) Unexpected effect of low doses of a neonicotinoid insecticide on behavioral responses to sex pheromone in a pest insect. PLoS ONE. DOI:10.1371/journal.pone.0114411
Rana, H., Farhanullah Khan, M., Akbar, M. F., Tahir, H. F., Sohail khan, M. & Ahmed, Z. (2015) Cholinsterase inhibition effects of Azadirachta indica A. Just fresh leave extract and its effects on Musca domestica L., larval mortality, pupation, adult emergence, fecundity and fertility. International Journal of Agriculture & Applied Sciences 7, 28-36.
Reddy, G. R., Madhusudhana, L., Shafeek, A. & Chetty, C. S. (2001) Azadirachtin and cypermethrin induced alterations in electrophysiological properties of sensory and interneurons in the cockroach, Periplaneta americana. Bulletin of Environmental Contamination and Toxicology 67, 828–833.
Reddy, G. V. & Guerrero, A. (2010) New pheromones and insect control strategies. Volume 83. Edited by Litwek, G. 20. Pheromones (Vitamins and Hormones).
Reinke, M. D. & Barrett, B. A. (2007) Sublethal exposure to methoxyfenozide-treated surfaces reduces the attractiveness and responsiveness in adult oriental fruit moth (Lepidoptera: Tortricidae). Journal of Economic Entomology 100, 72–78.
Sannino L. & Espinosa, B. (2010) Tuta absoluta. Guida alla conoscenza e recenti acquisizioni per una corretta difesa. 113pp. Edited by L’Informatore Agrario, Verona, Supplemento 1 al n. 46.
Santos da Silva, R. C.,  Milet-Pinheiro, P., Bezerra da Silva, P. C., Gomes da Silva, A., Vanusa da Silva, M., Navarro, M. A. F. & Henrique da Silva, N. (2015) (E)-caryophyllene and α-humulene: Aedes aegypti oviposition deterrents elucidated by gas chromatography-Electrophysiological assay of Commiphora leptophloeos leaf oil. PLoS ONE 10, 1-14.
Scott, R. H., O’Brien, K., Roberts, L., Mordue, M. & Mordue Luntz, L. (1999) Extracellular and intracellular actions of azadirachtin on the electrophysiological properties of cultured rat DRG neurons. Comparative Biochemistry and Physiology- Part C: Toxicology & Pharmacology 123, 85-93.
Shafeek, A., Prasanthi, R. P. J., Reddy, G. H., Chetty, C. S. & Reddy, G. R. (2004) Alterations in acetylcholinesterase and electrical activity in the nervous system of cockroach exposed to the neem derivative, azadirachtin. Ecotoxicology & Enviromental Safety 59, 205-208.
Siqueira, H. A. A., Guedes, R. N. C. & Picanço, M. C. (2000) Insecticide resistance in populations of Tuta absoluta (Lepidoptera: Gelechiidae). Journal of Agricultural & Forest Entomology 2, 147-153.
Tan, J., Galligan, J. J. & Hollingworth, R. M. (2007) Agonist actions of neonicotinoids on nicotinic acetylcholine receptors expressed by cockroach neurons. NeuroToxicology 28, 829-842.
Tricoire-Leignel, H., Thany, S. H., Gadenne, C. & Anton, S. (2012) Pest insect olfaction in an insecticide contamination environment: info-distruption or hormesis effect. Frontiers in Physiology 3, 1-6.
Vacas, S., Alfaro, C., Primo, J. & Navarro-Liopis, V. (2011) Studies on the development of a mating disruption system to control the tomato leafminer, Tuta absoluta Povolny (Lepidoptera: Gelechiidae). Pest Management Science 67, 1473-1480.
Wang, G., Huang, X., Wei, H. & Fadamiro, H. Y. (2011) Sublethal effects of larval exposure to indoxacarb on reproductive activities of the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae). Pesticide Biochemistry and Physiology 101, 227–231.
Wei, H. & Du, J. (2004) Sublethal effects of larval treatment with deltamethrin on moth sex pheromone communication system of the Asian corn borer, Ostrinia furnacalis. Pesticicid Biochemistry & Physiology 80, 12–20.
Xu, P., Atkinson, R., Jones, D. N. & Smith, D. P. (2005) Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45, 193–200.
Yang, Z. H. & Du, J. (2003) Effects of sublethal deltamethrin on the chemical communication system and PBAN activity of Asian corn borer, Ostrinia furnacalis (Guenee). Journal of Chemical Ecology 29, 1611–1619.
Zhou, H., Du, J. & Huang, Y. (2005) Effects of sublethal doses of malathion on responses to sex pheromones by male Asian corn borer moths, Ostrinia furnacalis (Guenée). Journal of Chemical Ecology 31, 1645–1656.

Files

Share

How to cite

Statistics