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Thiamethoxam-mediated alteration in multi-biomarkers of a model organism, Galleria mellonella L. (Lepidoptera: Pyralidae)

  • Tamer KayisEmail author
  • Murat Altun
  • Mustafa Coskun
Research Article

Abstract

Thiamethoxam (TMX), a second-generation neonicotinoid, is extensively used to control numerous pests that infest crops. We investigated the effects of TMX (10, 20, 30, 40, and 50 μg/mL for 24, 48, 72, and 96 h) on biomarkers such as antioxidant enzymes (superoxide dismutase (SOD) and catalase (CAT)); malondialdehyde (MDA), protein, lipid, and carbohydrate levels; micronucleus formation; and total hemocyte count in a model organism, Galleria mellonella L. SOD and CAT activities significantly decreased after 72 and 96 h of treatment at all TMX concentrations compared with control. MDA level increased following treatment with all TMX doses, with the exception of that following treatment with the lowest dose (10 μg/mL) at all tested treatment durations. Lipid and carbohydrate levels significantly decreased following treatment with high doses of TMX (40 and 50 μg/mL) after 48, 72, and 96 h. Micronucleated cell number significantly increased following treatment with all TMX doses at all tested treatment durations, except with 10 μg/mL of TMX for 24 h, when compared with control. During the first 72 h, total hemocyte count significantly decreased following treatment with 20-, 30-, 40-, and 50-μg/mL TMX; however, it was significantly reduced at all doses of TMX after 96 h. These results suggest that TMX can induce immunotoxicity, oxidative stress, and genotoxicity in a potential target and also in the model organism, G. mellonella. In addition, our study provides additional information regarding the prospective toxic effects of TMX.

Keywords

Antioxidant enzymes MDA Micronucleus Total hemocyte count Thiamethoxam Insects 

Notes

Acknowledgments

We thank Dr. Yusuf Sevgiler and Dr. Muhsin Aydin for helpful comments and edits of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126.  https://doi.org/10.1016/S0076-6879(84)05016-3 CrossRefGoogle Scholar
  2. Al-Barty AMF (2014) Laboratory evaluation of superoxide dismutase (SOD) of methylamine avermectin control of the rice red weevil (Sitophilus oryzae L.) in stored wheat grains. J Chem Pharm Res 6(4):979–983Google Scholar
  3. Ansoar-Rodriguez Y, Christofoletti C, Marcato A, Correia J, Bueno O, Malaspina O, Fontanetti C (2015) Genotoxic potential of the insecticide imidacloprid in a non-target organism (Oreochromis niloticus- Pisces). J Environ Protect 6(12):1360–1367.  https://doi.org/10.4236/jep.2015.612118 CrossRefGoogle Scholar
  4. Aslanturk A, Kalender S, Uzunhisarcikli M, Kalender Y (2011) Effects of methidathion on antioxidant enzyme activities and malondialdehyde level in midgut tissues of Lymantria dispar (Lepidoptera) larvae. J Entomol Res Soc 13(3):27–38Google Scholar
  5. Bagnyukova TV, Chahrak OL, Lushchak VI (2006) Coordinated response of goldfish antioxidant defenses to environmental stress. Aquatic Toxicol 78(4):325–331.  https://doi.org/10.1016/j.aquatox.2006.04.005 CrossRefGoogle Scholar
  6. Bar-Or D, Rael LT, Lau EP, Rao NKR, Thomas GW, Winkler JV, Yukl RL, Kingston RG, Curtis CG (2001) An analog of the human albumin N-terminus (Asp-Ala-His-Lys) prevents formation of copper induced reactive oxygen species. Biochem Biophys Res Commun 284(3):856–862.  https://doi.org/10.1006/bbrc.2001.5042 CrossRefGoogle Scholar
  7. Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O (2012) Oxidative stress and antioxidant defense. WAO J 5(1):9–19Google Scholar
  8. Bolognesi C, Creus A, Ostrosky-Wegman P, Marcos R (2011) Micronuclei and pesticide exposure. Mutagenesis 26(1):19–26.  https://doi.org/10.1093/mutage/geq070 CrossRefGoogle Scholar
  9. Brandt A, Goreflo A, Siede R, Meixner M, Büchler R (2017) The neonicotinoids thiacloprid, imidacloprid, and clothianidin affect the immunocompetence of honey bees (Apis mellifera L.). J Insect Physiol 86:40–47.  https://doi.org/10.1016/j.jinsphys.2016.01.001 CrossRefGoogle Scholar
  10. Bronskill JK (1961) A cage to simplify the rearing of greater wax moth, Galleria mellonella (Pyralidae). J Lepid Soc 15(2):102–104Google Scholar
  11. Buyukguzel K (2006) Malathion-induced oxidative stress in a parasitoid wasp: effect on adult emergence, longevity and oxidative and antioxidative response of Pimpla turionellae (Hymenoptera: Ichneumonidae). J Econ Entomol 99(4):1225–1234.  https://doi.org/10.1093/jee/99.4.1225 CrossRefGoogle Scholar
  12. Buyukguzel E (2009) Evidence of oxidative and antioxidative responses by Galleria mellonella larvae to malathion. J Econ Entomol 120(1):152–159.  https://doi.org/10.1603/029.102.0122 CrossRefGoogle Scholar
  13. Calderón-Segura ME, Gómez-Arroyo S, Villalobos-Pietrini R, Martínez-Valenzuela C, Carbajal-Carbajal-López Y, Calderón-Ezquerro MC, Cortés-Eslava J, García-Martínez R, Flores-Ramírez D, Rodríguez-Romero MI, Méndez-Pérez P, Bañuelos-Ruíz E (2012) Evaluation of genotoxic and cytotoxic effects in human peripheral blood lymphocytes exposed in vitro to neonicotinoid insecticides news. J Toxicol 1(11).  https://doi.org/10.1155/2012/612647 CrossRefGoogle Scholar
  14. Calderón-Segura ME, Rojas JAM, Brito MGM, TecCab M, Calderón-Ezquerro MC, Gómez-Arroyo S (2015) Genotoxicity of the neonicotinoid insecticide poncho (clothianidin) on CD1 mice based on alkaline comet and micronucleus assays. In: Larramendy ML, Soloneski S (eds) Toxicity and hazard of agrochemicals, Croatia, pp 113–125Google Scholar
  15. Casida JE, Durkin HA (2013) Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Ann Rev Entomol 58:99–117. https://doi.org/.  https://doi.org/10.1146/annurev-ento-120811-153645 CrossRefGoogle Scholar
  16. Catae AF, Roat TC, Oliveira RA, Nocelli RE, Malaspina O (2014) Cytotoxic effects of thiamethoxam in the midgut and malpighian tubules of Africanized Apis mellifera (Hymenoptera: Apidae). Microsc Res Tech 77(4):274–281.  https://doi.org/10.1002/jemt.22339 CrossRefGoogle Scholar
  17. Catae AF, Roat TC, Pratavieira M, Silva Menegasso ARD, Palma MS, Malaspina O (2018) Exposure to a sublethal concentration of imidacloprid and the side effects on target and nontarget organs of Apis mellifera (Hymenoptera, Apidae). Ecotoxicology 27(2):109–121.  https://doi.org/10.1007/s10646-017-1874-4 CrossRefGoogle Scholar
  18. Cavas T, Cinkilic N, Vatan O, Yılmaz D (2014) Effects of fullerenol nanoparticles on acetamiprid induced cytoxicity and genotoxicity in cultured human lung fibroblasts. Pest Biochem Physiol 114:1–7.  https://doi.org/10.1016/j.pestbp.2014.07.008 CrossRefGoogle Scholar
  19. Cheung CCC, Zheng GJ, Li AMY, Richardson BJ, Lam PKS (2001) Relationship between tissue concentrations of polycylic aromatic hydrocarbons and antioxidative responses of marine mussels, Perna viridis. Aquatic Toxicol 52(3-4):189–203.  https://doi.org/10.1016/S0166-445X(00)00145-4 CrossRefGoogle Scholar
  20. Dimitrova MST, Tsinova V, Velcheva V (1994) Combined effect of zinc and lead on the hepatic superoxide dismutase-catalase system in carp (Cyprinus carpio). Comp Biochem Physiol C Toxicol Pharmacol 108(1):43–46.  https://doi.org/10.1016/1367-8280(94)90087-6 CrossRefGoogle Scholar
  21. Ellis JD, Graham JR, Mortensen A (2013) Standard methods for wax moth research. J Apic Res 52(1):1–17.  https://doi.org/10.3896/IBRA.1.52.1.10 CrossRefGoogle Scholar
  22. Emre I, Kayis T, Coskun M, Dursun O, Cogun HY (2013) Changes in antioxidative enzyme activity, glycogen, lipid, protein, and malondialdehyde content in cadmium-treated Galleria mellonella larvae. Ann Entomol Soc Am 106(3):371–377.  https://doi.org/10.1603/AN12137 CrossRefGoogle Scholar
  23. European Commission (2013) Bee health: EU-wide restrictions on pesticide use to enter into force. European Commission, BrusselsGoogle Scholar
  24. Finney DJ (1971) Probit analysis, 3rd edn. Cambridge University Press, CambridgeGoogle Scholar
  25. Fotouhi K, Fazel MM, Kavaousi A (2015) Effects of pyriproxyfen on bioenergetic resources of Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae). Turk Entomol Derg 39(1):11–22.  https://doi.org/10.16970/ted.14717 CrossRefGoogle Scholar
  26. Gad AF, Radwan MA, EL-Gendy KS, Eshra EH, Seehy MA, Khamis A (2016) Genotoxic potential of some pollutants in Theba pisana snails using the micronucleus test. IJZI 2(2):197–205Google Scholar
  27. Ge WL, Yan SH, Wang JH, Zhu LS, Chen AM, Wang J (2015) Oxidative stress and DNA damage induced by imidacloprid in zebrafish (Danio rerio). J Agric Food Chem 63(6):1856–1862.  https://doi.org/10.1021/jf504895h CrossRefGoogle Scholar
  28. Gregorc A, Ellis JD (2011) Cell death localization in situ in laboratory reared honey bee (Apis mellifera L.) larvae treated with pesticides. Pest Biochem Physiol 99(2):200–207.  https://doi.org/10.1016/j.pestbp.2010.12.005 CrossRefGoogle Scholar
  29. Gul ST, Khan A, Farooq M, Niaz S, Ahmad M, Khatoon A, Hussain R, Saleemi MK, Hassan MF (2017) Effect of sub lethal doses of thiamethoxam (a pesticide) on hemato-biochemical values in cockerels. Pak Vet J 37(2):135–138Google Scholar
  30. Gultekin F, Ozturk M, Akdogan M (2000) The effect of organophosphate insecticide chlorpyrifos-ethyl on lipid peroxidation and antioxidant enzymes (in vitro). Arch Toxicol 74(9):533–538.  https://doi.org/10.1007/s002040000167 CrossRefGoogle Scholar
  31. Guo J, Shi R, Cao Y, Luan Y, Zhou Y, Gao Y, Tian Y (2018) Genotoxic effects of imidacloprid in human lymphoblastoid TK6 cells. Drug Chem Toxicol 13:1–5.  https://doi.org/10.1080/01480545.2018.1497048 CrossRefGoogle Scholar
  32. Han YN, Liu T, Wang JH, Wang J, Zhang C, Zhu LS (2016) Genotoxicity and oxidative stress induced by the fungicide azoxystrobin in zebrafish (Danio rerio) livers. Pest Biochem Physiol 133:13–19.  https://doi.org/10.1016/j.pestbp.2016.03.011 CrossRefGoogle Scholar
  33. Hertner T (1995) CGA 293343 tech.—Micronucleus test, mouse (OECD conform). Ciba-Geigy Ltd, Genetic Toxicology, Basel, Switzerland. Unpublished report No. 952018, 15 December 1995. Submitted to WHO by Syngenta Crop Protection AGGoogle Scholar
  34. Hogervorst PAM, Wäckers FL, Romeis J (2007) Effect of honeydew sugar composition on the longevity of Aphidius ervi. Entomol Exp Appl 122(3):223–232.  https://doi.org/10.1111/j.1570-7458.2006.00505.x CrossRefGoogle Scholar
  35. Ighodaro OM, Akinloye OA (2018) First line defense antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defense grid. Alexandria J Med 54(4):287–293.  https://doi.org/10.1016/j.ajme.2017.09.001 CrossRefGoogle Scholar
  36. Jones JC (1962) Current concepts concerning insect hemocytes. Amer Zool 2:209–246CrossRefGoogle Scholar
  37. Juhel G, Bayen S, Goh C, Lee WK, Kelly BC (2017) Use of a suite of biomarkers to assess the effects of carbamazepine, bisphenol A, atrazine and their mixture on green mussels, Perna viridis. Environ Toxicol Chem 36(2):429–441.  https://doi.org/10.1002/etc.3556 CrossRefGoogle Scholar
  38. Kalita MK, Haloi K, Devi D (2016) Larval exposure to Chlorpyrifos affects nutritional physiology and induces genotoxicity in silkworm Philosamia ricini (Lepidoptera: Saturniidae). Front Physiol 7:535.  https://doi.org/10.3389/fphys.2016.00535 CrossRefGoogle Scholar
  39. Kanbur M, Liman BC, Eraslan G, Altinordulu S (2008) Effects of cypermethrin, propetamphos, and combination involving cypermethrin and propetamphos on lipid peroxidation in mice. Environ Toxicol 23(4):473–479.  https://doi.org/10.1002/tox.20360 CrossRefGoogle Scholar
  40. Karabay NU, Oguz MN (2005) Cytogenetic and genotoxic effects of the insecticides, imidacloprid and methamidophos. Genet Mol Res 4(4):653–662Google Scholar
  41. Kataria SK, Chhillar AK, Kumar A, Tomar M, Malik V (2016) Cytogenetic and hematological alterations induced by acute oral exposure of imidacloprid in female mice. Drug Chem Toxicol 39(1):59–65.  https://doi.org/10.3109/01480545.2015.1026972 CrossRefGoogle Scholar
  42. Kavanagh K, Reeves PE (2007) Insects and mammalian innate immune responses are much alike. Microbe 2(12):596–599Google Scholar
  43. Kayis T, Coskun M, Dursun O, Emre I (2015) Alterations in antioxidant enzyme activity, lipid peroxidation and ion balance induced by Dichlorvos in Galleria mellonella L. Ann Entomol Soc Am 108(4):570–574.  https://doi.org/10.1093/aesa/sav038 CrossRefGoogle Scholar
  44. Keshta AT, Hataba AA, Mead HMI, El-Shafey NM (2016) Oxidative stress and biochemical changes induced by thiamethoxam and acetamiprid insecticides in rats. Pharm Sci Pharmacol 5(6):44–60.  https://doi.org/10.20959/wjpps20166-6837 CrossRefGoogle Scholar
  45. Kissoum N, Soltani N (2016) Spiromesifen, an insecticide inhibitor of lipid synthesis, affects the amounts of carbohydrates, glycogen and the activity of lactate dehydrogenase in Drosophila melanogaster. J Entomol Zool Stud 4(1):452–456Google Scholar
  46. Kocaman AY, Topaktas M (2007) In vitro evaluation of the genotoxicity of acetamiprid in human peripheral blood lymphocytes. Environ Mol Mutagen 48(6):483–490.  https://doi.org/10.1002/em.20309 CrossRefGoogle Scholar
  47. Kurt D, Kayis T (2015) Effects of the pyrethroid insecticide deltamethrin on the hemocytes of Galleria mellonella. Turk J Zool 39:452–457.  https://doi.org/10.3906/zoo-1405-66 CrossRefGoogle Scholar
  48. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193(1):265–275Google Scholar
  49. Lushchak VI (2016) Contaminant-induced oxidative stress in fish: a mechanistic approach. Fish Physiol Biochem 42(2):711–747.  https://doi.org/10.1007/s10695-015-0171-5 CrossRefGoogle Scholar
  50. Maryanski M, Kramarz P, Laskowski R, Niklinska M (2002) Decreased energetic reserves, morphological changes and accumulation of metals in Carabid Beetles (Poecilus cupreus L.) exposed to zinc or cadmium contaminated food. Ecotoxicology 11(2):127–139.  https://doi.org/10.1023/A:1014425113481 CrossRefGoogle Scholar
  51. Mathews CM, Summers CB, Felton GW (1997) Ascorbate peroxidase: a novel antioxidant enzyme in insects. Arch Insect Biochem Physiol 34:57–68.  https://doi.org/10.1002/(SICI)1520-6327(1997)34:1<57::AID-ARCH5>3.0.CO;2-T CrossRefGoogle Scholar
  52. Muthusamy R, Rajakumar S (2016) Antioxidative response in a silkworm, Bombyx mori larvae to dichlorvos insecticide. Free Rad Biol Antioxid 6(1):58–63.  https://doi.org/10.5530/fra.2016.1.7 CrossRefGoogle Scholar
  53. Nordberg J, Arnér ESJ (2001) Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Rad Biol Med 31(11):1287–1312.  https://doi.org/10.1016/S0891-5849(01)00724-9 CrossRefGoogle Scholar
  54. Noshy MM, Saad-Hussein A, Shahy EM, El-Shorbagy HM, Taha MM, Abdel-Shafy EA (2017) Assessment of anticholinesterase toxicity, oxidative stress and antioxidant status in carbamate and organophosphorus pesticides-exposed agricultural workers. Int J Pharm Clin Res 9(3):205–209.  https://doi.org/10.25258/ijpcr.v9i3.8319 CrossRefGoogle Scholar
  55. Oliveira RA, Roat TC, Carvalho SM, Malaspina O (2013) Side-effects of thiamethoxam on the brain and midgut of the Africanized honeybee Apis mellifera (Hymenopptera: Apidae). Environ Toxicol 29(10):1122–1133.  https://doi.org/10.1002/tox.21842 CrossRefGoogle Scholar
  56. Olson DM, Fadamiro H, Lundgren JG, Heimpel GE (2000) Effects of sugar feeding on carbohydrate and lipid metabolism in a parasitoid wasp. Physiol Entomol 25(1):17–25.  https://doi.org/10.1046/j.1365-3032.2000.00155.x CrossRefGoogle Scholar
  57. Parakash M (2008) Insect physiology. In: Encyclopedia of Entomology, 3nd edn. Discovery Pub. House Pvt. Ltd., New Delhi, pp 216–257Google Scholar
  58. Perveen N, Ahmad M (2017) Toxicity of some insecticides to the haemocytes of giant honeybee, Apis dorsata F. under laboratory conditions. Saudi J Biol Sci 24(5):1016–1022.  https://doi.org/10.1016/j.sjbs.2016.12.011 CrossRefGoogle Scholar
  59. Raj SJ, Joseph B (2015) Impact of acetamiprid toxicity on biochemical biomarkers (protein and carbohydrate) in some tissues of the fish Oreochromis mossambicus. Int J Zool Res 11(5):222–227.  https://doi.org/10.3923/ijzr.2015.222.227 CrossRefGoogle Scholar
  60. Rajak P, Dutta M, Roy S (2015) Altered differential hemocyte count in 3rd instar larvae of Drosophila melanogaster as a response to chronic exposure of Acephate. Interdiscip Toxicol 8(2):84–88.  https://doi.org/10.1515/intox-2015-0013 CrossRefGoogle Scholar
  61. Rashwan M (2013) Biochemical impacts of rynaxypyr (Coragen) and spinetoram (Radiant) on Spodoptera littoralis (Boisd.). J Nat Sci 11(8):40–47Google Scholar
  62. Sak O, Uckan F, Ergin E (2006) Effects of cypermetrin on total body weight, glycogen, protein, and lipid contents of Pimpla turionellae (L.) (Hymenoptera: Ichneumonidae). Belgian J Zool 136(1):53–58Google Scholar
  63. Saleem MA, Shakoori AR, Mantle D (1998) Macromolecular and enzymatic abnormalities induced by a synthetic pyrethroid, Ripcord (cypermethrin) in adult beetles of stored grain pests, Tribolium castaneum (Herbst.) (Col. Tenebrionidae). Arch Insect Biochem Physiol 39:144–154.  https://doi.org/10.1002/(SICI)1520-6327(1998)39:4<144::AID-ARCH2>3.0.CO;2-6 CrossRefGoogle Scholar
  64. Salema LH, Alwan MJ, Afaf AY (2014) Antioxidative and antigenotoxic effects against cytotoxicity of thiamethoxam on mice. Int J Adv Res 2(10):507–511Google Scholar
  65. Senyildiz M, Kilinc A, Ozden S (2018) Investigation of the genotoxic and cytotoxic effects of widely used neonicotinoid insecticides in HepG2 and SH-SY5Y cells. Toxicol Ind Health 34(6):375–383.  https://doi.org/10.1177/0748233718762609 CrossRefGoogle Scholar
  66. Shimizu N (2011) Molecular mechanisms of the origin of micronuclei from extrachromosomal elements. Mutagenesis 26(1):119–123.  https://doi.org/10.1093/mutage/geq053 CrossRefGoogle Scholar
  67. Shuklaa S, Jhamtania RC, Dahiyab MS, Agarwal R (2017) Oxidative injury caused by individual and combined exposure of neonicotinoid, organophosphate and herbicide in zebrafish. Toxicol Rep 4:240–244.  https://doi.org/10.1016/j.toxrep.2017.05.002 CrossRefGoogle Scholar
  68. Sinha S, Thaker AM (2013) Sub-acute genotoxicity studies of thiamethoxam in mice. Indian Vet J 90(9):42–44Google Scholar
  69. Stivaktakis P, Vlastos D, Giannakopoulos E, Matthopoulos DP (2010) Differential micronuclei induction in human lymphocyte cultures by imidacloprid in the presence of potassium nitrate. Sci World J 10:80–89.  https://doi.org/10.1100/tsw.2010.9 CrossRefGoogle Scholar
  70. Summers CB, Felton GW (1993) Antioxidant role of dehydroascorbic acid reductase in insects. Biochim Biophys Acta 1156(2):235–238.  https://doi.org/10.1016/0304-4165(93)90142-U CrossRefGoogle Scholar
  71. Sun Y, Oberley LW, Li Y (1988) A simple method for clinical assay of superoxide dismutase. Clin Chem 34(3):497–500Google Scholar
  72. Tauber OE, Yeager JF (1936) On the total hemolymph (blood) cell counts of insects II. Neuroptera, Coleoptera, Lepidoptera, and Hymenoptera. Ann Entomol Soc Am 29(1):112–118CrossRefGoogle Scholar
  73. Tomizawa M, Casida JE (2003) Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotinic receptors. Annu Rev Entomol 48:339–364.  https://doi.org/10.1146/annurev.ento.48.091801.112731 CrossRefGoogle Scholar
  74. Tomizawa M, Lee DL, Casida JE (2000) Neonicotinoid insecticides: molecular features conferring selectivity for insect versus mammalian nicotinic receptors. J Agric Food Chem 48(12):6016–6024.  https://doi.org/10.1021/jf000873c CrossRefGoogle Scholar
  75. Toroser D, Orr WC, Sohal RS (2007) Carbonylation of mitochondrial proteins in Drosophila melanogaster during aging. Biochem Biophys Res Commun 363(2):418–524.  https://doi.org/10.1016/j.bbrc.2007.08.193 CrossRefGoogle Scholar
  76. Tsai CJ, Loh JM, Proft T (2016) Galleria mellonella infection models for the study of bacterial diseases and for antimicrobial drug testing. Virulence 7(3):214–229.  https://doi.org/10.1080/21505594.2015.1135289 CrossRefGoogle Scholar
  77. Uckan F, Sak O (2010) Cytotoxic effect of cypermethrin on Pimpla turionellae (Hymenoptera: Ichneumonidae) larval hemocytes. Ekoloji 19(75):20–26.  https://doi.org/10.5053/ekoloji.2010.753 CrossRefGoogle Scholar
  78. Van Handel E (1985a) Rapid determination of glycogen and sugar in mosquitoes. J Am Mosq Control Assoc 1(3):299–301Google Scholar
  79. Van Handel E (1985b) Rapid determination of total lipids in mosquitoes. J Am Mosq Control Assoc 1(3):302–304Google Scholar
  80. Velisek J, Stara A (2018) Effect of thiacloprid on early life stages of common carp (Cyprinus carpio). Chemosphere 194:481–487.  https://doi.org/10.1016/j.chemosphere.2017.11.176 CrossRefGoogle Scholar
  81. Venier P, Maron S, Canova S (1997) Detection of micronuclei in gill cells and haemocytes of mussels exposed to benzo(a)pyrene. Mutat Res 390(1–2):33–44.  https://doi.org/10.1016/S0165-1218(96)00162-0 CrossRefGoogle Scholar
  82. Wickens PA (2001) Ageing and the free radical theory. Respir Physiol 128(3):379–391.  https://doi.org/10.1016/S0034-5687(01)00313-9 CrossRefGoogle Scholar
  83. Wu YY, Zhou T, Wang Q, Dai PL, Xu SF, Jia HR, Wang X (2015) Programmed cell death in the honey bee (Apis mellifera) (Hymenoptera: Apidae) worker brain induced by imidacloprid. J Econ Entomol 108(4):1486–1494.  https://doi.org/10.1093/jee/tov146 CrossRefGoogle Scholar
  84. Yan SH, Wang JH, Zhu LS, Chen AM, Wang J (2016) Thiamethoxam induces oxidative stress and antioxidant response in zebrafish (Danio Rerio) livers. Environ Toxicol 31(12):2006–2015.  https://doi.org/10.1002/tox.22201 CrossRefGoogle Scholar
  85. Yonar ME (2013) Protective effect of lycopene on oxidative stress and antioxidant status in Cyprinus carpio during cypermethrin exposure. Environ Toxicol 28(11):609–616.  https://doi.org/10.1002/tox.20757 CrossRefGoogle Scholar
  86. Yucel MS, Kayis T (2019) Imidacloprid induced alterations in oxidative stress, biochemical, genotoxic, and immunotoxic biomarkers in non-mammalian model organism Galleria mellonella L. (Lepidoptera: Pyralidae). J Environ Sci Health B 54(1):27–34.  https://doi.org/10.1080/03601234.2018.1530545 CrossRefGoogle Scholar
  87. Zhang Q, Zhan B, Wang C (2014) Ecotoxicological effects on the earthworm Eisenia fetida following exposure to contaminated with imidacloprid. Environ Sci Pollut Res 21(21):12345–12353.  https://doi.org/10.1007/s11356-014-3178-z CrossRefGoogle Scholar
  88. Zhang P, Sun H, Ren C, Min L, Zhang H (2018) Sorption mechanisms of neonicotinoids on biochars and the impact of deashing treatments on biochar structure and neonicotinoids sorption. Environ Pollut 234:812–820.  https://doi.org/10.1016/j.envpol.2017.12.013 CrossRefGoogle Scholar
  89. Zhu Q, He Y, Yao J, Liu Y, Tao L, Huang Q (2012) Effects of sublethal concentrations of the chitin synthesis inhibitor, hexaflumuron, on the development and hemolymph physiology of the cutworm, Spodoptera litura. J Insect Sci 12(27):1–13.  https://doi.org/10.1673/031.012.2701 CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Faculty of Science and Letters, Department of BiologyAdiyaman UniversityAdiyamanTurkey
  2. 2.Institutes of Natural and Applied SciencesAdiyaman UniversityAdiyamanTurkey

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