Document Type : Original Article


1 Department of Plant Protection, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran.

2 Departmant of Plant Protection, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran

3 Iranian Research Institute of Plant Protection, Tehran, Iran

4 Department of Plant Protection, University of Tehran, Karaj, Iran



Tomato leafminer, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) is one of the most destructive pests of tomato in many parts of the world including Iran. The toxicity of emamectin benzoate alone and combined with acetamiprid, eforia (thiamethoxam + lambda-cyhalotrin) and hexaflumuron was evaluated against 2nd instar larvae of Tuta absoluta (Meyrick) under 25 ± 1 °C, the relative humidity of 75 ± 5% and a photoperiod of 16:8 (L:D). Also the mixtures of tested insecticides with emamectin benzoate at LC15:LC15 ratio were evaluated on the activity of general esterase enzyme and total protein content of 2nd instar larvae. After 96 hour, emamectin benzoate had the highest toxicity (LC50 = 0.52 mg A.I./L), followed by acetamiprid (LC50 = 56.39 mg A.I./L) and eforia (LC50 = 312.01 mg A.I./L). Hexaflumuron showed no toxicity against larvae. The combination of emamectin benzoate with acetamiprid at LC50:LC50 ratio produced synergistic effects and all of the other ratios showed additive effects. The emamectin benzoate combined with either eforia or hexaflumuron at all of the ratios produced additive and antagonistic effects, respectively. Esterase activity of larvae increased when emamectin benzoate was mixed with either acetamiprid or eforia, but no significant differences were seen between emamectin benzoate alone and its mixture with hexaflumuron. The combination of emamectin benzoate with tested insecticides significantly reduced the total protein content of larvae. According to the results of this study, the mixtures of acetamiprid and eforia with emamectin benzoate showed higher negative impacts against 2nd instar larvae than emamectin benzoate alone


Abbas, N, Crickmore, N, Shad, SA. (2015). Efficacy of insecticide mixtures against a resistant strain of housefly (Diptera: Muscidae) collected from a poultry farm. Int. J. Trop. Insect Sci., 35:48-53.
Abbott, WS. (1925). A method of computing the effectiveness of an insecticide. J. Econom. Entomol., 18:265–267.
Abdel-Mageed, AEM, Shalaby, SEM. (2011). Toxicity and biochemical impacts of some new insecticide mixtures on cotton leafworm Spodoptera littoralis (Boisd.). Plant Protect. Sci., 47(4):166–175.
All, JN, Ali, M, Hornyak, EP, Weaver, JB. (1977). Joint action of two pyrethroids with methyl-parathion, methomyl, and chlorpyrifos on Heliothiszea and H. virescens in the laboratory and in cotton and sweetcorn. J. Econom. Entomol., 70:813–817.
AL-Kherb, (2011). Field efficacy of some neonicotinoid Insecticides on whitefly Bemiciatabaci (Homoptera: Aleyrodidae) and its natural enemies in cucumber and tomato plants in Al-qassim region, KSA. J. Entomol., 8(5):429-439.
Asher, KRS, Eliyahu, M, Ishaaya, I, Zur, M, Ben-Moshe, E. (1986). Synergism of pyrethroid–organophosphorus insecticide mixtures in insects and their toxicity against Spodoptera littoralis larvae. Phytoparasitica, 14:101–110.
Assar, AA, Abo El-Mahasen, MM, Dahi, HF, Amin, HS. (2016). Biochemical effects of some insect growth regulators and bioinsecticides against cotton leafworm, Spodoptera littoralis (Boisd.)(Lepidoptera: Noctuidae). J. Biosci. Appl. Res., 2(8):587-594.
Badawy, MEI, Nasr, HM, Rabea, EI. (2015). Toxicity and biochemical changes in the honey bee Apis mellifera exposed to four insecticides under laboratory conditions. Apidologie, 46:177–193.
Belzunces, L, Tchamitchian, S, Brunet, JL. (2012). Neural effects of insecticides in the honey bee. Apidologie, 43:348–370.
Bielza, P, Fernández, E, Graválos, C, Albellán, J. (2009). Carbamates synergize the toxicity of acrinathrin in resistant western flower thrips (Thysanoptera: Thripidae). J. Econom. Entomol., 102:393–397.
Bradford, MM. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal. Biochem., 72:248-254.
Braham, M, Hajji, L. (2011).Management of Tuta absoluta (Lepidoptera, Gelechiidae) with Insecticides on Tomatoes. Insecticides– Pest Engineering, 333-354.
Bryne, FJ, Devonshire, AL. (1991). In vivo inhibition of esterase and acetylcholinesterase activities by profenofos treatment in the tobacco whitefly Bemisia tabaci (Genn) implications for routine biochemical monitoring of these enzymes. Pest. Biochem. Physiol., 40:198–204.
Campos, MR, Rodrigues, ARS, Silva, WM, Silva, TBM, Silva, VRF, Guedes, RNC, Siqueira, HAA. (2014). Spinosad and the tomato borer Tuta absoluta: A bioinsecticide, an invasive pest threat, and high insecticide resistance. PLOS ONE, 9:e103235.
Corbett, JR. (1974). The Biochemical Mode of Action of Pesticides. New York: Academic Press.
Desneux, N, Wajnberg, E, Wyskhuys, KAG, Burgio, G, Arpaia, S, NarváezVazquez, CA, Gonzalez-Cabrera, J, Catalán Ruescas, D, Tabone, E, Frandon, J, Pizzol, J, Poncet, C, Cabello, T, Urbaneja, A  (2010). Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J. Pest Sci., 83:197-215.
Duchovskienė, L. (2016). The efficancy of different insecticides for control of Lepidopteran pests on cabbage in Lithuania. Sodin. stėir Daržinink., 35(3/4):65-75.
EPPO, (2005). Data sheets on quarantine pests: Tuta absoluta: 2005 OEPP/EPPO, European and Mediterranean Plant Protection Organization. Bulletin OEPP/EPPO, 35:434-435.
Gacemi, A, Guenaoui, Y. (2012). Efficacy of emamectin benzoate on Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) infesting a protected tomato crop in Algeria. Academic J. Entomol., 5(1):37-40.
Galdino, TVS, Picanço, MC, Morais, EGF, Silva, NR, Silva, GAR, Lopes, MC. (2011).  Bioassay method for toxicity studies of insecticide formulations to Tuta absoluta (MEYRICK, 1917). Sci. Agrotechnol., 35(5):869-877.
Gamil, WE, Mariy, FM, Youssef, LA, Abdel Halim, SM. (2011). Effect of indoxacarb on some biological and biochemical aspects of Spodoptera littoralis (Boisd.) larvae. Ann. Agricul. Sci., 56(2):121–126.
Ghoneim, YF, Singab, M, Abou-Yousef, HM, Abd-El-Hai, NS. (2012). Efficacy of certain insecticides and their mixtures with the tested IGRs against a field strain of the cotton leaf worm, Spodoptera littoralis (Boisd.) under laboratory conditions. Austral. J. Basic Appl. Sci., 6(6):300-304.
Guedes, RNC, Siqueira, HAA. (2012). The tomato borer Tuta absoluta: insecticide resistance and control failure. CAB Rev., 7 (055). (CAB Reviews Perspectives in Agriculture Veterinary Science Nutrition and Natural Resources 7(055):1)
Hemingway, J, Karunatne, SHP. (1998). Mosquito carboxylesterases: A review of the molecularbiology and biochemistry of a major insecticide resistance mechanism. Med. Veter. Entomol., 12:1-12.
Ishaaya, I. (2001). Biochemical processes related to insecticide action: An overview. In: Ishaaya, I., Eds. Biochemical sites of insecticides action and resistance. Berlin: Springer, pp. 1–16.
Ishaaya, I, Mendelson, Z, Ascher, KRS, Casida, JE. (1985). Mixtures of synthetic pyrethroids and organophosphorus compounds for controlling the whitefly, Bemisia tabaci, Phytoparasitica, 13:76–77.
Khan, HAA, Akram, W, Shad, SA, Lee, JJ. (2013). Insecticide mixtures could enhance the toxicity of insecticides in a resistant dairy population of Musca domestica L. PLOS ONE, 8(4):e60929.
Koppenhofer, AM, Kaya, HK. (1996). Additive and synergistic interaction between entomopathogenic nematodes and Bacillus thuringiensis for scarab grub control. Biol. Control, 8:131–137.
López, JD, Latheef, MA, Hoffman, WC. (2010). Effect of emamectin benzoate on mortality, proboscis extension, gustation and reproduction of the corn earworm Helicoverpa zea. J. Insect Sci., 10:89. available online:
Mahmoud, MM, Soliman, ASH, Abdel-Moniem, B, Abdel-Raheem, MA. (2013). Impact of some insecticides and their mixtures on the population of tomato borers, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) and Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) intomato crop at Upper Egypt. Arch. Phytopathol. Plant Protect., 47(14).
Mahmoud, MM, Soliman, ASH, Abdel-Moniem, B, Abdel-Raheem, MA. (2014).  Effect of certain low toxicity insecticides against tomato leaf miner, Tuta absoluta (Lepidoptera: Gelechiidae) with reference to their residues in harvested tomato fruits. Int. J. Agricul. Res., 9(4 ):210-218.
Manal, AR, Abdel-Mageed, AR. (2018). Toxicity of traditional, novel and bio-insecticides and theirmixtures against house fly Musca domestica in relation to somebiochemical activities. Res. J. Environ. Toxicol., 12(1):1-10.
Martin, T, Ochou, OG, Vaissayre, M, Fournier, D. (2003). Organophosphorus insecticides synergisepyrethroids in the resistant strain of cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae) from West Africa. J. Econ. Entomol., 92:468–474.
Metayi, MHA, Ibrahiem, MAM, El-Deeb, DA. (2015). Toxicity and Some Biological Effects of Emamectin Benzoate, Novaluron and Diflubenzuron against Cotton Leafworm. Alex. Sci. Exchange J., 36(4):350-357.
Nath, BS, Suresh, ., Varma, BM, Kumar, RPS. (1997). Bombyx mori (Lepidoptera: Bombycidae) in response to organophosphorus insecticides toxicity. Ecotoxicol. Environ. Safety, 36(2):169–173.
Nozad-Bonab, Z, Hejazi, MJ, Iranipour, S, Arzanlou, M. (2017). Lethal and sublethal effects of some chemicaland biological insecticides on Tuta absoluta (Lepidoptera: Gelechiidae) eggs and neonates. J. Econ. Entomol., 110(3):1138-1144.
Reyes, M, Rocha, K, Alarcón, L, Siegwart , M, Sauphanor, B. (2012). Metabolic mechanisms involved in the resistance of field populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) to spinosad. Pest. Biochem. Physiol., 102:45-50.
Reyes, M, Franck, P, Charmillot, PJ, Ioriatti, C, Olivares, J, Pasqualini, E, Sauphanor, B. (2007). Diversity of insecticide resistance mechanisms and spectrum in European populations of the codling moth, Cydia pomonella. Pest Manag. Sci., 63:890–902.
Roditakis, E, Skarmoutsou, C, Staurakaki, M. (2013). Toxicity of insecticides to populations of tomato borer Tuta absoluta (Meyrick) from Greece. Pest Manag. Sci., 69:834-840.
Saddiq, B, Ejaz, M, Shad, SA, Aslam, M. (2017). Assessing the combined toxicity of conventional and newer insecticides on the cotton mealybug Phenacoccus solenopsis. Ecotoxicology, 26:1240–1249.
Siqueira, HAA, Guedes, RNC, Picanco, MC. (2000). Cartap resistance and synergism in populations of Tuta absoluta (Lep.,Gelechiidae). J. Appl. Entomol., 124:233–238.
Siqueira, HAA, Guedes, RNC, Fragoso, DB, Magalhaes, LC. (2001). Abamectin resistance and synergism in Brazilian populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Int. J. Pest Manag., 47:247–251.
Sun, YP. (1950). Toxicity index-An improved method of comparing the relative toxicity of insecticides. J. Econ. Entomol., 43:45–53.
Torres, JB, Faria, C, Evangelista, WSJ, Pratissoli, D. (2001).Within-plantdistribution of the leaf miner Tuta absoluta (Meyrick) immatures in processing tomatoes, with notes on plant phenology. Int. J. Pest Manag., 47(3):173-178.
vanAsperen, K. (1962). Study of housefly esterases by means of sensitive colorimetric method. J. Insect Physiol., 8:401-416.
Vanhaelen, N, Haubruge, E, Lognay, G, Francis, F. (2001). Housefly glutathione S-transferase and effect of Brassicaceae secondary metabolites. Pest. Biochem. Physiol., 71:170-177.
Wakil, W, Ashfaq, M, Ghazanfar, MU. (2009). Integrated management of Helicoverpa armigera in chickpea in rainfed areas of Punjab, Pakistan. Phytoparasitica, 37:415–420.
Wilde, J., Fraczek, R. J., Siudaa, M., Bak, B., Hatjina, F. and Miszczak, A. (2016). The influence of sublethal doses of imidacloprid on protein content and proteolytic activity in honey bees (Apis mellifera L.). Journal of Apicultural Research, 55(2): 212–220.
Wing, KD, Sacher, M, Kagaya, Y, Tsurubuchi, Y, Mulderig, L, Connair, M, Schnee, M. (2000). Bioactivation and mode of action of the oxadiazineindoxacarb in insects. Crop Protect., 19:537–545.
Wolfenbarger, DA, Cantu, E. (1975). Enhanced toxicity of carbaryl when combined with synergists against larvae of the bollworm, Heliothis zea and the tobacco budworm, Heliothis virescens. Flor. Entomol., 58:103-104.
Yankova, V, Ganeva, D. (2013). Possibilities for control of tomato leaf miner Tuta absoluta (Meyrick) by application of insecticides in tomato greenhouse growing. Bulgar. J. Agricul. Sci., 19(4):728-731
Zibaee, I, Bandani, AR, Sabahi, GH. (2016). The expression profile of detoxifying enzyme of tomato leaf miner,Tuta absoluta Meyrik (Lepidoptera: Gelechiidae) to chlorpyrifos. Arthropods, 5(2):77-86.