Abstract
Insecticides that disrupt the healthy functioning of the ecosystem have toxic potential on non-target organisms. Fish, an important component of the aquatic ecosystem, are exposed to these pesticides in different ways. The stress response is regarded as an adaptive mechanism that allows the fish to cope with the perceived stressor to maintain its normal or homeostatic state. This mechanism is determined by antioxidant parameters and oxidative stress indicators measured in gill and liver tissue of rainbow trout. Accordingly, the effects of fipronil (FP) insecticide on the physiology of rainbow trout (Oncorhynchus mykiss) were determined with using the different biomarkers (superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPX), malondialdehyde (MDA), paraoxonase (PON), arylesterase (ARE), myeloperoxidase (MPO), 8-hydroxy-2-deoxyguanosine (8-OHdG)), and caspase 3 activity) in this study. Different doses of FP inhibited antioxidant enzyme activities in rainbow trout liver and gill tissues while inducing oxidative stress parameter (MDA, MPO, and 8-OHdG) levels. Also, caspase-3 activity was increased in liver and gill tissue, but this increase was statistically significant only in gill tissue (p < 0.05). When the results of the study were taken into consideration, it was concluded that different doses of FP insecticide caused physiological changes in rainbow trout and the studied parameters were usable biomarkers in explaining the adaptive response of stress factor.
Similar content being viewed by others
References
Aebi H (1974) In: Bergmeyer CHU (ed) Methods of enzymatic analysis. Academic Press, New York, pp 673–678
Alak G, Yeltekin AÇ, Tas IH, Ucar A, Parlak V, Topal A, Kocaman EM, Atamanalp M (2017a) Investigation of 8-OHdG, CYP1A, HSP70 and transcriptional analyses of antioxidant defence system in liver tissues of rainbow trout exposed to eprinomectin. Fish & Shellfish Immunology 65:136–144
Alak G, Ucar A, Parlak V, Yeltekin AÇ, Taş IH, Ölmez D, Yanık T (2017b) Assessment of 8-hydroxy-2-deoxyguanosine activity, gene expression and antioxidant enzyme activity on rainbow trout (Oncorhynchus mykiss) tissues exposed to biopesticide. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 203:51–58
Alak G, Uçar A, Yeltekin AÇ, Çomaklı S, Parlak V, Tas IH, Özkaraca M, Kirmanoğlu EM, Bolat İ, Atamanalp M, Türkez H (2018) Neuroprotective effects of dietary borax in the brain tissue of rainbow trout (Oncorhynchus mykiss) exposed to copper-induced toxicity. Fish Physiol Biochem 44(5):1409–1142
Alak G, Yeltekin AÇ, Uçar A, Parlak V, Türkez H. Atamanalp M (2019a) Borax alleviates copper-induced renal injury via inhibiting the DNA damage and apoptosis in rainbow trout. Biological trace element research, 191(2):495–501
Alak G, Ucar A, Yeltekin AÇ, Parlak V, Nardemir G, Kızılkaya M, Tas IH, Yılgın M, Atamanalp M, Topal A, Kocaman EM, Yanık T (2019b) Neurophysiological responses in the brain tissues of rainbow trout (Oncorhynchus mykiss) treated with bio-pesticide. Drug Chem Toxicol 42:203–209. https://doi.org/10.1080/01480545.2018.1526180
Alak G, Parlak V, Arslan ME, Uçar A, Atamanalp M, Türkez H (2019c) Borax supplementation alleviates hematotoxicity and DNA damage in rainbow trout (Oncorhynchus mykiss) exposed to copper. Biol Trace Elem Res 187:536–542. https://doi.org/10.1007/s12011-018-1399-6
Alak G, Uçar A, Parlak V, Yeltekin AÇ, Özgeriş FB, Atamanalp M, Türkez H (2020a) Antioxidant potential of Ulexite in Zebrafish brain: assessment of oxidative DNA damage, apoptosis, and response of antioxidant defense system. Biol Trace Elem Res. https://doi.org/10.1007/s12011-020-02231-7
Alak G, Parlak V, Ucar A, Yeltekin AC, Ozgeris FB, Cağlar O, Atamanalp M, Türkez H (2020b). Oxidative and DNA damage potential of colemanite on zebrafish: brain, liver and blood. Turk J Fish & Aquat Sci 20(8):593-602
Altınok İ, Capkın E, Boran H (2012) Mutagenic, genotoxic and enzyme inhibitory effects of carbosulfan in rainbow trout Oncorhynchus mykiss. Pestic Biochem Phys 102:61–67
Ambreen F, Javed M (2015) Assessment of acute toxicity of pesticides mixtures for Cyprinus carpio and Ctenopharyngodon idella. Pakistan J Zool 47(1):133–139
Banaee M (2013) Physiological dysfunction in fish after ınsecticides exposure, ınsecticides - development of safer and more effective technologies. Stanislav Trdan, IntechOpen. https://doi.org/10.5772/54742
Başkol G, Köse K (2004) Paraoxanase: biochemical features, functions and clinical importance. Erciyes Med J 26:75–80
Batista MTO, Junior ER, Oliveira MF, Ribeiro AC, Rodrigues E, Suda CK, Vani GS (2014) Tissue levels of the antioxidant enzymes superoxide dismutase and catalase in fish Astyanax bimaculatus from the Una River Basin. Rev Ambient Água 9(4):621–631
Beutler E (1984) Red cell metabolism: a manual of biochemical methods, 2nd edn. Grune and Starton, NewYork
Bhattacharjee R, Sil PC (2006) The protein fraction of Phyllanthus niruri plays a protective role against acetaminophen induced hepatic disorder via its antioxidant properties. Phytother Res 20(7):595–601
Çelik M, Gülcü F, Ozan G, Gürsu MF (2005) Paraoxonase and arylesterase activity levels in workers exposed to organic solvents. Turk J Biochem 30:194–199
Chagnon M, Kreutzweiser D, Mitchell EAD, Morrissey CA, Noome DA, Van der Sluijs JP (2015) Risks of large-scale use of systemic insecticides to ecosystem functioning and services Environ. Sci Pollut Res 22:119–134. https://doi.org/10.1007/s11356-014-3277-x
Chandler GT, Cary TL, Volz DC, Walse SS, Ferry JL, Klosterhaus SL (2004) Fipronil effects on estuarine copepod (Amphiascus tonuiremis) development, fertility, and reproduction: a rapid life-cycle assay in 96-well microplate format. Environ Toxicol Chem 23:117–124
Çınkıloğlu E (2007) Effects of Fenthion in the Brain of Cyprinus carpio on Antioxidant Defence System, Lipid Peroxidation and Acetylcholinesterase Enzyme Activities by the Modulation of n-acetylcysteine University of Çukurova Institute of Natural and Applied Sciences Department of Biology
Doyotte A, Cossu C, Jacquin MC, Babut M, Vaseural P (1997) Antioxidant enzymes, glutathione and lipid peroxidation as relevant biomarkers of experimental or field exposure in the gills and the digestive gland of the freshwater bivalve Unio tumidus. Aquat Toxicol 39:93–110
Eckerson HW, Wyte CM, La Du BN (1983) The human serum paraoxonase/arylesterase poly-morphism. Am J Hum Genet 35:1126–1138
Fernandes PN, Mannarino SC, Silva CG, Pereira MD, Panek AD, Eleutherio EC (2007) Oxidative stress response in eukaryotes: effect of glutathione, superoxide dismutase and catalase on adaptation to peroxide and menadione stresses in Saccharomyces cerevisiae. Redox Rep 12(5):236–244
Ferreira M, Antunes P, Gil O, Vale C, Reis-Henriques MA (2004) Organochlorine contaminants in flounder (Platichthys flesus) and mullet (Mugil cephalus), and their use as bio indicator species for environmental monitoring. Aquat Toxicol 69:347–357
Fırat Ö, Aytekin T (2018) Effect of neonicotinoid insectiside thiamethoxam on oxidative stress parameters in Oreochromis niloticus. BAUN Inst Sci Technol 20(2):224–234
Fischer U, Janicke RU, Schulze-Osthoff K (2003) Many cuts to ruin: a comprehen-sive update of caspase substrates. Cell Death Diff 10:76–100
Fulton MM, Key PB, Delorenzo ME (2014) Insecticide toxicity in fish. In: Tierney KB, Farrell AP, Brauner CJ (eds) Organic chemical toxicology of fishes. Academic Press, Amsterdam, pp 309–368
Gibbons D, Morrissey C, Mineau P (2015) A review of the direct and indirect effects of neonicotinoids and fipronil on vertebrate wildlife. Environ Sci Pollut Res 22:103–118
Gilbert N (2016) Global biodiversity report warns pollinators are under threat. Nat News May 2017. https://doi.org/10.1038/nature.2016.19456
Hussain R, Ghaffar A, Ali HM, Abbas RZ, Khan JA, Khan IA, Ahmad I, Iqbal Z (2018) Analysis of different toxic impacts of Fipronil on growth, hemato-biochemistry, protoplasm and reproduction in adult cockerels. Toxin Rev 37(4):294–303. https://doi.org/10.1080/15569543.2017.1366921
Kerr JFR (2002) History of the events leading to the formulation of the apoptosisconcept. Toxicology 181–182:471–474
Kılıç T, Yonar ME (2017) Investigation of effect of malathion on paraoxonase and arylesterase enzyme activities in scaly carp (Cyprinus carpio). Fırat Univ J Vet Sci 31(2):87–92
Konwick B, Fisk A, Garrison A, Avants J, Black M (2005) Acute enantioselective toxicity of fipronil and its desulfinyl photoproduct to Ceriodaphnia dubia. Environ Toxicol Chem 24(9):2350–2355
Lee JW, Choi YC, Kim R, Lee SK (2015) Multiwall carbon nanotube-induced apoptosis and antioxidant gene expression in the gills, liver, and intestine of Oryzias latipes. Biomed Res Int 1–10
Luo Y, Su Y, Lin RZ, Shi H, Wang XR (2006) 2-chlorophenol induced ROS generation in fish Carassius auratus based on the EPR method. Chemosphere 65(6):1064–1073
McCarthy JF, Shugart LR (1990) Biological markers of environmental contamination. In: McCarthy JF, Shugart LR (eds) Biomarkers of environmental contamination. Lewis, Boca Raton
Monteiro SM, Santos NMS, Calejo M, FontaínhasFernandes AA, Sousa M (2009) Copper toxicity in gills of the teleost fish, Oreochromis niloticus: effects in apoptosis induction and cell proliferation. Aquat Toxicol 94:219–228
Oliva M, González de Canales ML, Gravato C, Guilhermino L, Perales JA (2010) Biochemical effects and polycyclic aromatic hydrocarbons (PAHs) in Senegal sole (Solea senegalensis) from a Huelva estuary (SW Spain). Ecotoxicol Environ Saf 73:1842–1851. https://doi.org/10.1016/j.ecoenv.2010.08.035
Oruç EÖ, Sevgiler Y, Uner N (2004) Tissue specific oxidative stress responses in fish exposed to 2,4-D and azinphosmethyl. Comp Biochem Physiol C 137:43–51
Parlak V (2018) Evaluation of apoptosis, oxidative stress responses, AChE activity and body malformations in zebrafish (Danio rerio) embryos exposed to deltamethrin. Chemosphere 207:397–403
Qu C, Yang W, Xu Q, Sun J, Lu M, Wang Y, Song L (2018) A novel effector caspase (Caspase-3/7-1) involved in the regulation of immune homeostasis in Chinese mitten crab Eriocheir sinensis. Fish Shellf Immunol 83:76–83
Qureshi IZ, Bibi A, Shahid S, Ghazanfa M (2016) Exposure to sub-acute doses of fipronil and buprofezin in combination or alone induces biochemical, hematological, histopathological and genotoxic damage in common carp (Cyprinus carpio L.). Aquat Toxicol 179:103–114
Sole M, Baena M, Arnaua S, Carrasson M, Maynoua F, Cartes JE (2011) Muscular cholinesterase activities and lipid peroxidation levels as biomarkers in several Mediterranean marine fish species and their relationship with ecological variables. Enviro Int 36:202–211
Stara A, Machova J, Velisek J (2012) Effect of chronic exposure to simazine on oxidative stress and antioxidant response in common carp (Cyprinus carpio L.). Environ Toxicol Pharmacol 33(2):334–343
Sun Y, Oberley LW, Li Y (1988) A simple method for clinical assay of superoxide dismutase. Clin Chem 34(3):497–500
Tabassum H, Afjal MA, Khan J, Raisuddin S, Parve S (2015) Neurotoxicological assessment of pendimethalin in freshwater fish Channa punctata Bloch. Ecol Indic 58:411–417
Teng M, Zhou Y, Son M, Dong K, Chen X, Bi CWS, Zhu W (2019) Chronic toxic effects of Flutolanil on the liver of Zebrafish (Danio rerio). Chem Res Toxicol 32:995–1001
Topal A., Alak G, Altun S, Erol, HS, Atamanalp M (2017) Evaluation of 8-hydroxy-2-deoxyguanosine and NFkB activation, oxidative stress response, acetylcholinesterase activity, and histopathological changes in rainbow trout brain exposed to linuron. Environmental toxicology and pharmacology, 49:14–20
Toroser D, Orr WC, Sohal RS (2007) Carbonylation of mitochondrial proteins in Drosophila melanogaster during aging. Biochem Biophys Res Commun 363:418–424
Ucar A, Al-Hamdani HA, Alak G, Atamanalp M, Topal A, Arslan H, Parlak V, Fakioglu O, Sensurat T (2012) Effects of carboxin on superoxide dismutase enzyme activite in rainbow trout (Oncorhynus mykiss). Res J Biol Sci 5:2 83-85
Ullah S, Li Z, Hasan Z, Ullah S, Khan Fahad S (2018) Malathion induced oxidative stress leads to histopathological and biochemical toxicity in the liver of rohu (Labeo rohita, Hamilton) at acute concentration. Ecotoxicol Environ Saf 161:270–280
Vasylkiva OY, Kubraka OI, Storey KB, Lushchak VI (2011) Catalase activity as a potential vital biomarker of fish intoxication by the herbicide aminotriazole. Pestic Biochem Physiol 101(1):1–5
Wu H, Gao C, Guo Y, Zhang Y, Zhang J, Maa E (2014) Acute toxicity and sublethal effects of fipronil on detoxification enzymes in juvenile zebrafish (Danio rerio). Pestic Biochem Physiol 115:9–14
Yancheva V, Velcheva I, Stoyanova S, Georgieva E (2015) Fish in ecotoxicological studies. Ecol Balkan 7(1):149–169
Zwart LLD, Meerman JHN, Commandeur JNM, Vermeulen NPE (1999) Biomarkers of free radical damage applications in experimental animals and in humans. Free Radic Biol Med 27:202–226
Acknowledgments
We thank for all authors for assistance this research and Application Centre and the Laboratories of the Atatürk University Fisheries Faculty.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All conditions (stocking density, water parameters etc.) were designed according to the welfare-related assessments, suitable for O. mykiss.
Ethics committee
The trials with the rainbow trout were approved by Ataturk University Local Ethical Committee for Animal Studies (approved in 27/02/2020, Acceptance No:13).
Additional information
Editor: Tetsuji Okamoto
Rights and permissions
About this article
Cite this article
Uçar, A., Parlak, V., Özgeriş, F.B. et al. Determination of Fipronil toxicity by different biomarkers in gill and liver tissue of rainbow trout (Oncorhynchus mykiss). In Vitro Cell.Dev.Biol.-Animal 56, 543–549 (2020). https://doi.org/10.1007/s11626-020-00480-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11626-020-00480-3