Lethal and sublethal effects of the pyrethroid insecticide tau-fluvalinate on the non-target organism Gammarus roeseli: A study of acute toxicity, genotoxicity and locomotor activity
DOI:
https://doi.org/10.2298/ABS220930033SKeywords:
Gammarus roeseli, tau-fluvalinate, DNA damage, non-target organism, locomotor activity, comet assayAbstract
Paper description:
- Pesticides are used extensively in agricultural activities to control pests. However, they can affect both target and non-target organisms.
- Lethal and sublethal effects of tau-fluvalinate on the non-target organism roeseli were investigated for the first time.
- The 96-h median lethal concentration (LC50) was found to be 17.29 µg/L. Tau-fluvalinate caused a significant increase in DNA damage and a significant reduction in locomotor activity at sublethal concentrations.
- The use of tau-fluvalinate in agricultural activities should be reconsidered to minimize the risk of exposure.
Abstract: Aquatic ecosystems are recipients of various contaminants including pesticides. For many years, pyrethroid insecticides (e.g., tau-fluvalinate) have been used extensively in agricultural activities to control pests. However, they can affect not only target organisms but also non-target organisms. This study was conducted to investigate the lethal and sublethal effects of tau-fluvalinate on the non-target organism Gammarus roeseli. To this end, acute toxicity of tau-fluvalinate was determined using a toxicity test with a 96-h exposure period, and the genotoxic effects of different sublethal concentrations on hemocytes of the test organism were assessed at 24-, 96-, and 240-h exposure periods using the comet assay. Alterations in locomotor activity of the test organism in response to exposure to sublethal concentrations were evaluated at 120- and 240-h periods. The 96-h median lethal concentration (LC50) was found to be 17.29 µg/L, and tau-fluvalinate was observed to cause a significant increase in DNA damage and a significant reduction in locomotor activity at the tested sublethal concentrations (2.15, 4.30 and 8.60 µg/L). The results of this study suggest that the long-term existence of tau-fluvalinate in aquatic environments at high concentrations is a noteworthy threat to non-target organisms and that its use in agricultural activities should be reconsidered.
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Bashir I, Lone FA, Bhat RA, Mir SA, Dar ZA, Dar SA. Concerns and threats of contamination on aquatic ecosystems. In: Hakeem KR, Bhat RA, Qadri H, editors. Bioremediation and Biotechnology: Sustain Approaches to Pollut Degrad. Cham: Springer; 2020. p;.1-26. https://doi.org/10.1007/978-3-030-35691-0_1
Hampel M, Blasco J, Segner H. Molecular and cellular effects of contamination in aquatic ecosystems. Environ Sci Pollut Res. 2015;22(22):17261-6. https://doi.org/10.1007/s11356-015-5565-5
Lebrun JD, De Jesus K, Rouillac L, Ravelli M, Guenne A, Tournebize J. Single and combined effects of insecticides on multi-level biomarkers in the non-target amphipod Gammarus fossarum exposed to environmentally realistic levels. Aquat Toxicol. 2020;218:105357. https://doi.org/10.1016/j.aquatox.2019.105357
Tudi M, Ruan HD, Wang L, Lyu J, Sadler R, Connell D, Chu C, Phung DT. Agriculture development, pesticide application and its impact on the environment. Int J Environ Res Public Health. 2021;18:1112. https://doi.org/10.3390/ijerph18031112
Pérez GL, Vera MS, Miranda LA. Effects of herbicide glyphosate and glyphosate-based formulations on aquatic ecosystems. In: Kortekamp A, editor. Herbicides and Environment. London: IntechOpen; 2011. p. 343-68. https://doi.org/10.5772/12877
Davies TGE, Field LM, Usherwood PNR, Williamson MS. DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB Life. 2007;59(3):151-62. https://doi.org/10.1080/15216540701352042
Field LM, Davies TGE, O'Reilly AO, Williamson MS, Wallace BA. Voltage-gated sodium channels as targets for pyrethroid insecticides. Eur Biophys J. 2017;46(7):675-9. https://doi.org/10.1007/s00249-016-1195-1
Cossi PF, Herbert LT, Yusseppone MS, Pérez AF, Kristoff G. Toxicity evaluation of the active ingredient acetamiprid and a commercial formulation (Assail® 70) on the non-target gastropod Biomphalaria straminea (Mollusca: Planorbidae). Ecotoxicol Environ Saf. 2020;192:110248. https://doi.org/10.1016/j.ecoenv.2020.110248
Sabová L, Cingeľová Maruščáková I, Koleničová S, Mudroňová D, Holečková B, Sabo R, Sobeková A, Majchrák T, Ratvaj M. The adverse effects of synthetic acaricide tau-fluvalinate (tech.) on winter adult honey bees. Environ Toxicol Pharmacol. 2022;92:103861. https://doi.org/10.1016/j.etap.2022.103861
MacNeil C, Dick JT, Elwood RW. The trophic ecology of freshwater Gammarus spp. (Crustacea: Amphipoda): problems and perspectives concerning the functional feeding group concept. Biol Rev. 1997;72(3):349-64. https://doi.org/10.1017/S0006323196005038
Gerhardt A, Bloor M, Mills CL. Gammarus: important taxon in freshwater and marine changing environments. Int J Zool. 2011;2011:2-4. https://doi.org/10.1155/2011/524276
MacNeil C, Dick JTA, Elwood RW. The dynamics of predation on Gammarus spp. (Crustacea: Amphipoda). Biol Rev. 1999;74(4):375-95. https://doi.org/10.1017/S0006323199005368
Kunz PY, Kienle C, Gerhardt A. Gammarus spp. in aquatic ecotoxicology and water quality assessment: toward integrated multilevel tests. Rev Environ Contam Toxicol. 2010;205:1-76. https://doi.org/10.1007/978-1-4419-5623-1_1
Demirçalı A, Karcı F, Sari F. Synthesis and absorption properties of five new heterocyclic disazo dyes containing pyrazole and pyrazolone and their acute toxicities on the freshwater amphipod Gammarus roeseli. Color Technol. 2021;137(3):280-91. https://doi.org/10.1111/cote.12530
Sari A, Sari F. A comparative examination of acute toxicities of three disazo dyes to freshwater macroinvertebrates Gammarus roeseli (Crustacea: Amphipoda) and Chironomus riparius (Insecta: Diptera). Chem Ecol. 2021;37(8):683-703. https://doi.org/10.1080/02757540.2021.1974008
Uğurlu P, Ünlü E, Satar EI. The toxicological effects of thiamethoxam on Gammarus kischineffensis (Schellenberg 1937) (Crustacea: Amphipoda). Environ Toxicol Pharmacol. 2015;39(2):720-6. https://doi.org/10.1016/j.etap.2015.01.013
Yildirim NC, Ak TP, Samasas O. Toxicological effects of di-(2-ethylhexyl) phthalate in Gammarus pulex: a biochemical and histopathological assessment. Environ Sci Pollut Res. 2021;28:44442-51. https://doi.org/10.1007/s11356-021-13925-3
Yildirim NC, Yaman M. The usability of oxidative stress and detoxification biomarkers in Gammarus pulex for ecological risk assessment of textile dye methyl orange. Chem Ecol. 2019;35(4):319-29. https://doi.org/10.1080/02757540.2019.1579199
Lacaze E, Geffard O, Bony S, Devaux A. Genotoxicity assessment in the amphipod Gammarus fossarum by use of the alkaline Comet assay. Mutat Res Toxicol Environ Mutagen. 2010;700(1-2):32-8. https://doi.org/10.1016/j.mrgentox.2010.04.025
Gollapudi BB, Krishna G. Practical aspects of mutagenicity testing strategy: an industrial perspective. Mutat Res Mol Mech Mutagen. 2000;455(1-2):21-8. https://doi.org/10.1016/S0027-5107(00)00114-7
Dusinska M, Rundén-Pran E, Carreira SC, Saunders M. Critical evaluation of toxicity tests. In: Fadeel B, Pietroiusti A, Shvedova AA, editors. Adverse Effects of Engineered Nanomaterials. Academic Press; 2012. p. 63-83. https://doi.org/10.1016/B978-0-12-386940-1.00004-0
Mersch J, Beauvais M-N, Nagel P. Induction of micronuclei in haemocytes and gill cells of zebra mussels, Dreissena polymorpha, exposed to clastogens. Mutat Res Toxicol. 1996;371(1-2):47-55. https://doi.org/10.1016/S0165-1218(96)90093-2
Cruzeiro C, Ramos A, Loganimoce EM, Arenas F, Rocha E, Cardoso PG. Genotoxic effects of combined multiple stressors on Gammarus locusta haemocytes: interactions between temperature, pCO2 and the synthetic progestin levonorgestrel. Environ Pollut. 2019;245:864-72. https://doi.org/10.1016/j.envpol.2018.11.070
Ronci L, Iannilli V, Matthaeis E De, Donato G Di, Setini A. Evaluation of genotoxic potential of waters from two Italian rivers in Gammarus elvirae (Amphipoda). Water Environ Res. 2015;87(11):2008-17. https://doi.org/10.2175/106143015X14212658614397
Ronci L, De Matthaeis E, Chimenti C, Davolos D. Arsenic-contaminated freshwater: assessing arsenate and arsenite toxicity and low-dose genotoxicity in Gammarus elvirae (Crustacea; Amphipoda). Ecotoxicology. 2017;26(5):581-8. https://doi.org/10.1007/s10646-017-1791-6
Lacaze E, Devaux A, Mons R, Bony S, Garric J, Geffard A, Geffard O. DNA damage in caged Gammarus fossarum amphipods: a tool for freshwater genotoxicity assessment. Environ Pollut. 2011;159(6):1682-91. https://doi.org/10.1016/j.envpol.2011.02.038
Di Donato G, De Matthaeis E, Ronci L, Setini A. Genotoxicity biomarkers in the amphipod Gammarus elvirae exposed in vivo to mercury and lead, and basal levels of DNA damage in two cell types. Chem Ecol. 2016;32(9):843-57. https://doi.org/10.1080/02757540.2016.1201078
Grabowski M, Bacela K, Konopacka A. How to be an invasive gammarid (Amphipoda: Gammaroidea) - Comparison of life history traits. Hydrobiologia. 2007;590(1):75-84. https://doi.org/10.1007/s10750-007-0759-6
Felten V, Charmantier G, Mons R, Geffard A, Rousselle P, Coquery M, Garric J, Geffard O. Physiological and behavioural responses of Gammarus pulex (Crustacea: Amphipoda) exposed to cadmium. Aquat Toxicol. 2008;86(3):413-25. https://doi.org/10.1016/j.aquatox.2007.12.002
Mehennaoui K, Georgantzopoulou A, Felten V, Andreï J, Garaud M, Cambier S, Serchi T, Pain-Devin S, Guérold F, Audinot JN, Giambérini L, Gutleb AC. Gammarus fossarum (Crustacea, Amphipoda) as a model organism to study the effects of silver nanoparticles. Sci Total Environ. 2016;566-567:1649-59. https://doi.org/10.1016/j.scitotenv.2016.06.068
Nørum U, Frederiksen MAT, Bjerregaard P. Locomotory behaviour in the freshwater amphipod Gammarus pulex exposed to the pyrethroid cypermethrin. Chem Ecol. 2011;27(6):569-77. https://doi.org/10.1080/02757540.2011.596831
Wallace WG, Estephan A. Differential susceptibility of horizontal and vertical swimming activity to cadmium exposure in a gammaridean amphipod (Gammarus lawrencianus). Aquat Toxicol. 2004;69(3):289-97. https://doi.org/10.1016/j.aquatox.2004.05.010
Singh NP, McCoy MT, Tice RR, Schneider EL. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res. 1988;175(1):184-91. https://doi.org/10.1016/0014-4827(88)90265-0
Nadin SB, Vargas-Roig LM, Ciocca DR. A silver staining method for single-cell gel assay. J Histochem Cytochem. 2001;49(9):1183-6. https://doi.org/10.1177/002215540104900912
Arslan I, Ili P. Genotoxicological assessment of nebuloside-A a triterpenoid saponin compound on whole blood DNA. Int J Food Prop. 2015;18(11):2374-9. https://doi.org/10.1080/10942912.2014.971185
Collins AR. The comet assay for DNA damage and repair: principles, applications, and limitations. Mol Biotechnol. 2004;26(3):249-61. https://doi.org/10.1385/MB:26:3:249
Oruc HH, Hranitz JM, Sorucu A, Duell M, Cakmak I, Aydin L, Orman A. Determination of acute oral toxicity of flumethrin in honey bees. J Econ Entomol. 2012;105(6):1890-4. https://doi.org/10.1603/EC12055
Rasmussen JJ, Wiberg-Larsen P, Kristensen EA, Cedergreen N, Friberg N. Pyrethroid effects on freshwater invertebrates: a meta-analysis of pulse exposures. Environ Pollut. 2013;182:479-85. https://doi.org/10.1016/j.envpol.2013.08.012
Strausfeld NJ. Crustacean - insect relationships: the use of brain characters to derive phylogeny amongst segmented invertebrates. Brain Behav Evol. 1998;52(4-5):186-206. https://doi.org/10.1159/000006563
Zucker E. Hazard Evaluation Division Standard Evaluation Procedure: Acute Toxicity Test for Freshwater Invertebrates. Washington, DC: US Environmental Protection Agency, Office of Pesticide Programs; 1985.
Ramakrishna M, Vijayakumar M, Srirangam GM. Toxicity and behavioural studies on the earthworm, Lampito mauritii (Kinberg) exposed to organophosphate insecticide monocrotophos. Int J Res Anal Rev. 2019;6(1):99-107.
Jia Q, Xu N, Mu P, Wang B, Yang S, Qiu J. Stereoselective separation and acute toxicity of tau-fluvalinate to zebrafish. J Chem. 2015;2015:9319081-5. https://doi.org/10.1155/2015/931908
Sogorb A, Andreu-Moliner ES, Almar MM, del Ramo J, Núñez A. Temperature-toxicity relationships of fluvalinate (synthetic pyrethroid) on Procambarus clarkii (Girard) under laboratory conditions. Bull Environ Contam Toxicol. 1988;40(1):13-7. https://doi.org/10.1007/BF01689379
Shen WF, Zhao XP, Wang Q, Niu BL, Liu Y, He LH, Weng HB, Meng ZQ, Chen YY. Genotoxicity evaluation of low doses of avermectin to hemocytes of silkworm (Bombyx mori) and response of gene expression to DNA damage. Pestic Biochem Physiol. 2011;101(3):159-64. https://doi.org/10.1016/j.pestbp.2011.08.011
Frenzilli G, Nigro M, Lyons BP. The Comet assay for the evaluation of genotoxic impact in aquatic environments. Mutat Res Mutat Res. 2009;681(1):80-92. https://doi.org/10.1016/j.mrrev.2008.03.001
Kalita MK, Haloi K, Devi D. Cypermethrin formulation (Ustad-10 EC) induces genotoxicity via apoptosis, affects nutritional physiology, and modulates immune response in silkworm Philosamia ricini (Lepidoptera: Saturniidae). J Econ Entomol. 2017;110(3):1010-24. https://doi.org/10.1093/jee/tox044
Sundaramoorthy R, Velusamy Y, Balaji APB, Mukherjee A, Chandrasekaran N. Comparative cytotoxic and genotoxic effects of permethrin and its nanometric form on human erythrocytes and lymphocytes in vitro. Chem Biol Interact. 2016;257:119-24. https://doi.org/10.1016/j.cbi.2016.08.001
Nagy K, Rácz G, Matsumoto T, Ádány R, Ádám B. Evaluation of the genotoxicity of the pyrethroid insecticide phenothrin. Mutat Res - Genet Toxicol Environ Mutagen. 2014;770:1-5. https://doi.org/10.1016/j.mrgentox.2014.05.001
Lebrun JD, Uher E, Fechner LC. Behavioural and biochemical responses to metals tested alone or in mixture (Cd-Cu-Ni-Pb-Zn) in Gammarus fossarum: from a multi-biomarker approach to modelling metal mixture toxicity. Aquat Toxicol. 2017;193:160-7. https://doi.org/10.1016/j.aquatox.2017.10.018
Watts MM, Pascoe D, Carroll K. Survival and precopulatory behaviour of Gammarus pulex (L.) exposed to two xenoestrogens. Water Res. 2001;35(10):2347-52. https://doi.org/10.1016/S0043-1354(00)00537-6
de Lange HJ, Noordoven W, Murk AJ, Lürling M, Peeters ETHM. Behavioural responses of Gammarus pulex (Crustacea, Amphipoda) to low concentrations of pharmaceuticals. Aquat Toxicol. 2006;78(3):209-16. https://doi.org/10.1016/j.aquatox.2006.03.002
Andreï J, Pain-Devin S, Felten V, Devin S, Giambérini L, Mehennaoui K, Cambier S, Gutleb AC, Guérold F. Silver nanoparticles impact the functional role of Gammarus roeseli (Crustacea Amphipoda). Environ Pollut. 2016;208(Part B):608-18. https://doi.org/10.1016/j.envpol.2015.10.036
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