Abstract
Mosquito responds to various insecticides in the presence of environmental factors which is very important to consider in vector management as these factors affect both mosquito behavior and efficacy of insecticides. The current study aims to examine the impact of high temperatures and Bti insecticide on the biochemical profile of Aedes aegypti and Aedes albopictus mosquitoes. Late third instar larvae of Aedes aegypti and Aedes albopictus were exposed to varying temperatures (39 °C and 40 °C) and Bti concentrations (1 ppm and 1.5 ppm). After exposure, detoxifying enzymes such as Esterase (α and β), Glutathione S-transferase (GST), Cytochrome P450 monooxygenase and total protein level were analyzed. It was observed that both temperature and Bti significantly influenced the level of protein and enzyme activities in both mosquito species. Aedes aegypti and Aedes albopictus exhibited a significant increase in total protein in response to temperature exposure at 40 °C and a decline of total protein in response to Bti exposure. Thermally pre-exposed (40 °C) larvae exhibited an increase in total protein content after Bti exposure. The activity of esterase decreased significantly in thermally exposed mosquitoes while Bti exposure increased the level of esterase significantly. The result of the current study also showed a significant increase in GSTs and monooxygenase after exposure to temperature and Bti in both mosquitoes. Thermally pre-exposed larvae of both mosquito species exhibited increased activities of GSTs and monooxygenase in response to Bti exposure. A significant interaction between temperature and Bti for activities of GSTs and monooxygenase was also observed. Current results showed most of the enzymes were highly expressed in Ae. aegypti than Ae. albopictus. Our results suggest that consideration of environmental factors like temperature is crucial while evaluating the efficacy of Bti that may help to make accurate prediction of Bti effect on Aedes mosquitoes.
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References
Achari TS, Acharya UR, Barik TK (2017) Impact of thermal stress on survival and induced cross-tolerance to toxins of Bacillus thuringiensis in wild Aedes aegypti. Int J Biosci 11:156–164. https://doi.org/10.12692/ijb/11.1.156-164
Achari TS, Barik TK (2019) Assessment of Temperature-induced Cross-tolerance to Bacillus thuringiensis subsp. israelensis on Field-collected Aedes albopictus. Biopestic Int 15:97–104
Araujo AP, Araujo Diniz DF, Helvecio E, de Barros RA, de Oliveira CM, Ayres CF, de Melo-Santos MA, Regis LN, Silva-Filha MH (2013) The susceptibility of Aedes aegypti populations displaying temephos resistance to Bacillus thuringiensis israelensis: a basis for management. Parasite Vector 6:297. https://doi.org/10.1186/1756-3305-6-297
Bayoh MN, Lindsay SW (2004) Temperature-related duration of aquatic stages of the Afrotropical malaria vector mosquito Anopheles gambiae in the laboratory. Med Vet Entomol 18:174–179. https://doi.org/10.1111/j.0269-283X.2004.00495.x
Benoit JB, Lopez-Martinez G, Patrick KR, Phillips ZP, Krause TB, Denlinger DL (2011) Drinking a hot blood meal elicits a protective heat shock response in mosquitoes. PNAS 108:8026–8029. https://doi.org/10.1073/pnas.1105195108
Beyger L, Orrego R, Guchardi J, Holdway D (2012) The acute and chronic effects of endosulfan pulse-exposure on Jordanella floridae (Florida flagfish) over one complete life-cycle. Ecotoxicol Environ Saf 76:71–78. https://doi.org/10.1016/j.ecoenv.2011.09.015
Boyer S, David JP, Rey D, Lemperiere G, Ravanel P (2006) Response of Aedes aegypti (Diptera: Culicidae) larvae to three xenobiotic exposures: larval tolerance and detoxifying enzyme activities. Environ Toxicol Chem 25:470–476. https://doi.org/10.1897/05-267r2.1
Boyer S, Tilquin M, Ravanel P (2007) Differential sensitivity to Bacillus thuringiensis var. israelensis and temephos in field mosquito populations of Ochlerotatus cataphylla (diptera: culicidae): toward resistance? Environ Toxicol Chem 26:157. https://doi.org/10.1897/06-205R.1
Brogdan WG, McAllister JC (1998) Insecticide resistance and vector control. Emerg Infect Dis 4:605–613. https://doi.org/10.3201/eid0404.980410
Diffenbaugh NS, Pal JS, Trapp RJ, Giorgi F (2005) Fine-scale processes regulate the response of extreme events to global climate change. Proc Natl Acad Sci USA 102:15774–15778. https://doi.org/10.1073/pnas.0506042102
Dixit V, Gupta AK, Kataria O, Prasad GBKS (2002) Population dynamics of Culex quinquefasciatus filaria vector in Raipur City of Chhattisgarh State. J Commun Dis 34:193–202
Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modeling, and impacts. Science 28:2068–2074. https://doi.org/10.1126/science.289.5487.2068
Githeko AK, Lindsay SW, Confalonieri UE, Patz JA (2000) Climate change and vector-borne diseases: a regional analysis. Bull World Health Organ 78:1136–1147
Gubler DJ (1998) Dengue and dengue hemorrhagic fever. Clin Microbiol Rev 11:480–496
Helinski MEH, Parker AG, Knols BGJ (2009) Radiation biology of mosquitoes. Malar J 8:S6. https://doi.org/10.1186/1475-2875-8-S2-S6
Intergovernmental Panel on Climate, Change Working Group II. Climate Change (2014) Impacts. Adaptation and Vulnerability. Cambridge University Press; New York, NY, USA
Juliano SA, Lounibos LP (2005) Ecology of invasive mosquitoes: effects on resident species and on human health. Ecol Lett 8:558–574. https://doi.org/10.1111/j.1461-0248.2005.00755
Kang ZW, Tian HG, Liu FH, Liu X, Jing XF, Liu TX (2017) Identification and expression analysis of chemosensory receptor genes in an aphid endoparasitoid Aphidius gifuensis. Sci Rep 7:3939. https://doi.org/10.1038/s41598-017-03988-z
Kaur M, Atif F, Ansari RA, Ahmad F, Raisuddin S (2011) The interactive effect of elevated temperature on deltamethrin-induced biochemical stress responses in Channa punctata Bloch. Chem Biol Interact 193:216–224. https://doi.org/10.1016/j.cbi.2011.06.011
Koodalingam A, Mullainadhan P, Rajalakshmi A, Deepalakshmi R, Ammu M (2012) Effect of a Bt-based product (Vectobar) on esterases and phosphatases from larvae of the mosquito Aedes aegypti. Pestic Biochem Phys 104:267–272. https://doi.org/10.1016/j.pestbp.2012.09.008
Lacey LA (2007) Bacillus thuringiensis serovariety israelensis and Bacillus sphaericus for mosquito control. J Am Mosquito Contr Assoc 23:133–163. https://doi.org/10.2987/8756-971X(2007)23[133:BTSIAB]2.0.CO;2
Laurence D, Christophe L, Roger F (2011) Using the Bio-Insecticide Bacillus thuringiensis israelensis in Mosquito Control. Pesticides in the Modern World - Pests Control and Pesticides Exposure and Toxicity Assessment
Meehl GA, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 30:994–997. https://doi.org/10.1126/science.1098704
Morris ON (1983) Protection of Bacillus thuringiensis from inactivation from sunlight. Can Entomol 115:1215–1227. https://doi.org/10.4039/Ent1151215-9
Mulla MS, Federici BA, Darwazeh HA (1982) Larvicidal efficacy of Bacillus thuringiensis serotype H-14 against stagnant-water mosquitoes and its effects on non-target organisms. Environ Entomol 11:788–795. https://doi.org/10.1093/ee/11.4.788
Muthusamy R, Ramkumar G, Karthi S, Shivakumar MS (2014) Biochemical mechanisms of insecticide resistance in field population of Dengue vector Aedes aegypti (Diptera: Culicidae). Int J Mosq Res 1:1–4
Oliver SV, Brooke BD (2017) The effect of elevated temperatures on the life history and insecticide resistance phenotype of the major malaria vector Anopheles arabiensis (Diptera: Culicidae). Malar J 16:73. https://doi.org/10.1186/s12936-017-1720-4
Patil NS, Lole KS, Deobagkar DN (1996) Adaptive larval thermotolerance and induced cross-tolerance to propoxur insecticide in mosquitoes Anopheles stephensi and Aedes aegypti. Med Vet Entomol 10:277–282. https://doi.org/10.1111/j.1365-2915.1996.tb00743.x
Penilla RP, Rodríguez AD, Hemingway J, Torres JL, Arredondo-Jiménez JI, Rodríguez MH (1998) Resistance management strategies in malaria vector mosquito control. Baseline data for a large-scale field trial against Anopheles albimanus in Mexico. Med Vet Entomol 12:217–233. https://doi.org/10.1046/j.1365-2915.1998.00123.x
Pickett CB, Lu AY (1989) Glutathione S-transferases: gene structure, regulation, and biological function. Annu Rev Biochem 58:743–764. https://doi.org/10.1146/annurev.bi.58.070189.003523
Raghavendra K, Barik TK, Adak T (2010) Development of larval thermotolerance and its impact on adult susceptibility to malathion insecticide and Plasmodium vivax infection in Anopheles stephensi. Parasitol Res 107:1291–1297. https://doi.org/10.1007/s00436-010-2001-0
Rahmstorf S, Coumou D (2011) Increase of extreme events in a warming world. Proc Natl Acad Sci USA 108:17905–17909. https://doi.org/10.1073/pnas.1101766108
Rohr JR, Schotthoefer AM, Raffel TR, Carrick HJ, Halstead N, Hoverman JT, Johnson CM, Johnson LB, Lieske C, Piwoni MD, Schoff PK, Beasley VR (2008) Agrochemicals increase trematode infections in a declining amphibian species. Nature 455:1235–1239. https://doi.org/10.1038/nature07281
Sandland GJ, Carmosini N (2006) Combined effects of a herbicide (atrazine) and predation on the life history of a pond snail, Physa gyrina. Environ Toxicol Chem 25:2216–2220. https://doi.org/10.1897/05-596R.1
Smirle MJ, Zurowski CL, Lowery DT, Foottit RG (2010) Relationship of insecticide tolerance to esterase enzyme activity in Aphis pomi and Aphis spiraecola. J Econ Entomol 103:374–378. https://doi.org/10.1603/EC09275
Swain V, Seth RK, Mohanty SS, Raghavendra K (2008) Effect of temperature on development, eclosion, longevity and survivorship of malathion-resistant and malathion-susceptible strain of Culex quinquefasciatus. Parasitol Res 103:299–303. https://doi.org/10.1007/s00436-008-0969-5
Swain V, Seth RK, Raghavendra K, Mohanty SS (2009) Characterization of biochemical based insecticide resistance mechanism by thermal bioassay and the variation of esterase activity in Culex quinquefasciatus. Parasitol Res 104:1307‐1313. https://doi.org/10.1007/s00436-008-1326-4
Van Munster, M, Préfontaine G, Meunier L, Elias M, Mazza A, Brousseau R, Masson L, (2007) Altered gene expression in Choristoneura fumiferana and Manduca sexta in response to sublethal intoxication by Bacillus thuringiensis Cry1Ab toxin. Insect Mol Biol 16:25–35. https://doi.org/10.1111/j.1365-2583.2006.00692.x
Vontas JG, Small GJ, Hemingway J (2001) Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens. Biochem J 357:65–72. https://doi.org/10.1042/0264-6021:3570065
Weis JS, Smith G, Zhou T, Santiago-Bass C, Weis P (2001) Effects of contaminants on behavior: Biochemical mechanisms and ecological consequences. Bioscience 513:209–217. https://doi.org/10.1641/0006-3568(2001)051[0209:EOCOBB]2.0.CO;2
World Health Organization (1988) Test Procedures for Insecticide Resistance Monitoring in Malaria Vectors, Bio-efficacy and Persistence of Insecticide on Treated Surfaces, World Health Organization, Geneva, Switzerland
World Health Organization (1998) Recommended classification of pesticides by hazard, and guidelines to classification, 1998–1999. International Program on Chemical safety. WHO document, WHO/PSC/98.21
World Health Organization (2006) Guidelines for testing mosquito adulticides for indoor residual spraying and treatment of mosquito nets
World Health Organization (2020) Vector borne disease factsheet. https://www.who.int/news-room/fact-sheets/detail/vector-borne-diseases
Zhang H, Zhao M, Liu Y, Zhou Z, Guo J (2018) Identification of cytochrome P450 monooxygenase genes and their expression in response to high temperature in the alligator weed flea beetle Agasicles hygrophila (Coleoptera: Chrysomelidae). Sci Rep 8:17847. https://doi.org/10.1038/s41598-018-35993-1
Zhu G, Xue M, Luo Y, Ji G, Liu F, Zhao H, Sun X (2017) Effects of short-term heat shock and physiological responses to heat stress in two Bradysia adults, Bradysia odoriphaga and Bradysia difformis. Sci Rep 7:13381. https://doi.org/10.1038/s41598-017-13560-4
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Authors are thankful to the Head, Post Graduate Department of Zoology, Post Graduate Department of Chemistry, Berhampur University, Berhampur, Odisha, for providing necessary facilities and encouragement.
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Achari, T.S., Panda, C. & Barik, T.K. Biochemical response of Aedes aegypti and Aedes albopictus mosquitoes after exposure to thermal stress and toxin of Bacillus thuringiensis israelensis. Int J Trop Insect Sci 42, 651–660 (2022). https://doi.org/10.1007/s42690-021-00587-4
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DOI: https://doi.org/10.1007/s42690-021-00587-4