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Evaluation of toxicological responses and promising biomarkers of topmouth gudgeon (Pseudorasbora parva) exposed to fipronil at environmentally relevant levels

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Abstract

Fipronil is an insecticide commonly used in agriculture. We report here on the sublethal and sub-chronic effects of fipronil on non-target topmouth gudgeon (Pseudorasbora parva) at environmentally relevant levels. The results showed that fipronil did not cause significant changes in brain acetylcholinesterase activities, glutathione S-transferase (GST) activities in the intestine, and GST, glutamic pyruvic transaminase (GPT), and glutamic oxaloacetic transaminase (GOT) activities in the liver tissues at environmentally relevant levels for 96-h exposure. In the further test for a 12-day exposure, dose-dependent responses of the serum GPT and GOT activities were observed in all treated groups with sublethal concentrations of fipronil. Furthermore, fipronil could reduce the liver mitochondrial membrane fluidity of P. parva, especially with high concentration of fipronil at high temperature. The results suggest that serum GPT and GOT in P. parva might be useful biomarkers for effects of fipronil exposure at environmentally relevant level, and reducing fluidity of liver mitochondrial membrane may be one toxic mechanism of fipronil.

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References

  • Adham KG (2002) Sublethal effects of aquatic pollution in Lake Maryuˆt on the African sharptooth catfish, Clarias gariepinus (Burchell, 1822). J Appl Ichthyol 18:87–94

    Article  CAS  Google Scholar 

  • Antunes-Madeira MC, Madeira VMC (1989) Membrane fluidity as affected by the insecticide lindane. Biochim Biophys Acta 982:161–166

    Article  CAS  Google Scholar 

  • Ardeshir RA, Zolgharnein H, Movahedinia A, Salamat N, Zabihi E (2017) Comparison of waterborne and intraperitoneal exposure to fipronil in the Caspian white fish (Rutilus frisii) on acute toxicity and histopathology. Toxicol Rep 4:348–357

    Article  CAS  Google Scholar 

  • Bálint T, Ferenczy J, Kátai F, Kiss I, Kráczer L, Kufcsák O, Láng G, Polyhos C, Szabó I, Szegletes T, Nemcsók J (1997) Similarities and differences between the massive eel (Anguilla anguilla L.) devastations that occurred in Lake Balaton in 1991 and 1995. Ecotox Environ Safe 37:17–23

  • Bedient PB, Horsak RD, Schlenk D,Hovinga RM, Pierson JD (2005) Environmental impact of fipronil to the Louisiana crawfish industry. Environ Forensic 6:289–299

  • Beggel S, Werner I, Connon RE, Geist JP (2010) Sublethal toxicity of commercial insecticide formulations and their active ingredients to larval fathead minnow (Pimephales promelas). Sci Total Environ 408(16):3169–3175

  • Blasiak J (1995) Changes in membrane fluidity evoked by organophosphorus insecticide bromfenvinfos and its methylated analogue. Comp Biochem Physiol 110C:15–21

  • Cattaneo R, Clasen B, Loro VL, de Menezes CC, Pretto A, Baldisserotto B, Santi A, de Avila LA (2011) Toxicological responses of Cyprinus carpio exposed to a commercial formulation containing glyphosate. Bull Environ Contam Toxicol 87(6):597–602

  • Cheng S, Levy D (1979) The effects of cell proliferation on the lipid composition and fluidity of hepatocyte plasma membrane. Arch Biochem Biophys 196:424–429

  • Clasen B, Loro VL, Cattaneo R , Moraes B, Lópes T, de Avila LA, Zanella R, Reimche GB, Baldisserotto B (2012) Effects of the commercial formulation containing fipronil on the non-target organism Cyprinus carpio: implications for rice-fish cultivation. Ecotox Environ Safe 9(77):45–51

  • Dallarés S, Dourado P, Sanahuja I, Solovyev M, Gisbert E, Montemurro N, Torreblanca A, Blázquez M, Solé M (2020) Multibiomarker approach to fipronil exposure in the fish Dicentrarchus labrax under two temperature regimes. Aquatic Toxicol: 219. https://doi.org/10.1016/j.aquatox.2019.105378

  • Fredianelli AC, Pierin VH, Uhlig SC, Galeb LdAG, Rocha DCC, Ribeiro DR, Anater A, Pimpao CT (2019) Hematologic, biochemical, genetic, and histological biomarkers for the evaluation of the toxic effects of fipronil for Rhamdia quelen. Turk J Vet Anim Sci 43:54–59

  • Gabbianelli R, Falcioni G, Nasuti C, Cantalamessa F (2002) Cypermethrin-induced plasma membrane perturbation on erythrocytes from rats: reduction of fluidity in the hydrophobic core and in glutathione peroxidase activity. Toxicology 175:91–101

    Article  CAS  Google Scholar 

  • Galindo-Reyes JG, Dalla Venezia L, Lazcano-Alvarez G, Rivas-Mendoza H (2000) Enzymatic and osmoregulative alterations in white shrimp Litopenaeus vannamei exposed to pesticides. Chemosphere 40:233–237

    Article  CAS  Google Scholar 

  • Gan J, Bondarenko S, Oki L, Haver D, Li JX (2012) Occurrence of fipronil and its biologically active derivatives in urban residential runoff. Environ Sci Technol 46:1489–1495

  • Ghaffar A, Hussain R, Abbas G, Kalim M, Khan A, Ferrando S, Gallus L, Ahmed Z (2018) Fipronil (Phenylpyrazole) induces hemato-biochemical, histological and genetic damage at low doses in common carp, Cyprinus carpio (Linnaeus, 1758). Ecotoxicity 27:1261–1271

  • Gripp HS, Freitas JS, Almeida EA, Bisinoti MC, Moreira AB (2017) Biochemical effects of fipronil and its metabolites on lipid peroxidation and enzymatic antioxidant defense in tadpoles (Eupemphix nattereri: Leiuperidae). Ecotox Environ Safe 136:173–179

  • Gupta RC, Milatovic D (2014) Insecticides. In: Gupta RC (ed) Biomarkers in toxicology. Academic Press, Boston, pp 389–407

    Chapter  Google Scholar 

  • Gupta SK, Pal AK, Sahu NP, Jha AK, Akhtar MS, Mandal SC, Das P, Prusty AK (2013) Supplementation of microbial levan in the diet of Cyprinus carpio fry (Linnaeus, 1758) exposed to sublethal toxicity of fipronil: effect on growth and metabolic responses. Fish Physiol Biochem 39:1513–1524

    Article  CAS  Google Scholar 

  • Khan S, Jan MH, Kumar D, Telang AG (2015) Firpronil induced spermotoxicity is associated with oxidative stress, DNA damage and apoptosis in male rats. Pestic Biochem Physiol 124:8–14

  • Li SN, Fan DF (1996) Correlation between biochemical parameters and susceptibility of freshwater fish to malathion. J Toxicol Environ Health 48:413–418

    Article  Google Scholar 

  • Li HP, Chang J, Feng T, Gao XW (2015) Differential effects of insecticides on mitochondrial membrane fluidity and ATPase activity between the wolf spider and the rice stem borer. J Integr Agric 14:2574–2580

  • Lopez-Antia A, Ortiz-Santaliestra ME, Camarero PR, Mougeot F, Mateo R (2015) Assessing the risk of fipronil-treated seed ingestion and associated adverse effects in the red-legged partridg. Environl Sci Technol 49:13649–13657

  • Margarido TCS, Felício AA, Rossa-Feres DDC, Alves de Almeida E (2013) Biochemical biomarkers in Scinax fuscovarius tadpoles exposed to a commercial formulation of the pesticide fipronil. Mar Environ Res 91:61–67

  • Martins JD, Monteiro JP, Antunes-Madeira MC, Jurado AS, Madeira VM (2003) Use of the microorganism Bacillus stearothermophilus as a model to evaluate toxicity of the lipophilic environmental pollutant endosulfan. Toxicol in Vitro 17:595–601

    Article  CAS  Google Scholar 

  • Menezes C, Leitemperger J, Murussi C, de Souza Viera M, Adaime MB, Zanella R, Loro VL (2016) Effect of diphenyl diselenide diet supplementation on oxidative stress biomarkers in two species of freshwater fish exposed to the insecticide fipronil. Fish Physiol Biochem 42:1357–1368

  • Moya-Quiles MR, Munoz-Delgado E, Vidal CJ (1995) Effects of the pyrethroid insecticides allethrin on membrane fluidity. Biochem Mol Biol Int 36:1299–1308

    CAS  Google Scholar 

  • Moya-Quiles MR, Munoz-Delgado E, Vidal CJ (1996a) The pyrethroid insecticide deltamethrin modifies the thermotropic properties and lipid packing order of model membranes. Chem Phys Lipids 83:61–69

    Article  CAS  Google Scholar 

  • Moya-Quiles M, Munoz-Delgado E, Vidal CJ (1996b) Effects of the pyrethroid insecticides permethrin on membrane fluidity. Chem Phys Lipids 79:21–28

    Article  CAS  Google Scholar 

  • Murugesan R, Palaniswamy TN, Panneer S (1999) Glutamic oxaloacetic transaminase (GOT) and glutamic pyruvic transaminase (GPT) enzyme activities in different tissues of Sarotherodon mossambicus (Peters) exposed to a carbamate pesticides, carbaryl. Pestic Sci 55:1217–1221

  • OECD (Organization for Economic Cooperation and Development) (2004) Guideline for testing chemicals. Section 2: Effects on biotic systems. Earthworm, Acute Toxicity Tests, Paris

  • Oluah NS (1999) Plasma aspartate aminotransferase activity in the catfish Clarias albopunctatus exposed to sublethal zinc and mercury. Bull Environ Contam Toxicol 63:343–349

  • Qureshi IZ, Bibi A, Shahid S, Ghazanfar 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

    Article  CAS  Google Scholar 

  • Reynaud S, Worms IAM, Veyrenc S, Portier J, Maitre A, Miaud C, Raveton M (2012) Toxicokinetic of benzo[a]pyrene and fipronil in female green frogs (Pelophylax kl. esculentus). Environ Pollut 161:206–214

    Article  CAS  Google Scholar 

  • Shinitzky M, Barenholz Y (1978) Fluidity parameters of lipid regions determined by fluorescence polarization. Biochim Biophys Acta 515(4):367–394

    Article  CAS  Google Scholar 

  • Simondelso N, Amaralrogers V, Belzunces LP, Bonmatin JM, Chagnon M, Downs C, Furlan L, Gibbons DW, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke CH, Liess M, Long E, McField M, Mineau P, Mitchell EAD, Morrissey CA, Noome DA, Pisa L, Settele J, Stark JD, Tapparo A, Van Dyck H, Van Praagh J, Van der Sluijs JP, Whitehorn PR, Wiemers M (2015) Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environ Sci Pollut Res 22:5–34

  • Sprague LA, Nowell LH (2008) Comparison of pesticide concentrations in streams at low flow in six metropolitan areas of the United States. Environ Toxicol Chem 27:288–298

    Article  CAS  Google Scholar 

  • Stehr CM, Linbo TL, Incardona JP, Scholz NL (2006) The developmental neurotoxicity of fipronil: notochord degeneration and locomotor defects in zebrafish embryos and larvae. Toxicol Sci 92:270–278

    Article  CAS  Google Scholar 

  • Taillebois E, Alamiddine Z, Brazier C, Graton J, Laurent AD, Thany SH, le Questel JY (2015) Molecular features and toxicological properties of four common pesticides, acetamiprid, deltamethrin, chlorpyriphos and fipronil. Bioorg Med Chem 23:1540–1550

  • Tingle CC, Rother JA, Dewhurst CF, Lauer S, King WJ (2013) Fipronil: environmental fate, ecotoxicology, and human health concerns. Rev Environ Contam Toxicol 176:1–66

  • Venkateswara RJ (2006a) Biochemical alterations in euryhaline fish, Oreochromis mossambicus exposed to sub-lethal concentrations of an organophosphorus insecticide, monocrotophos. Chemosphere 65:1814–1820

    Article  Google Scholar 

  • Venkateswara RJ (2006b) Sublethal effects of an organophosphorus insecticide (RPR-II) on biochemical parameters of tilapia, Oreochromis mossambicus. Comp Biochem Physiol 143C:492–498

    Google Scholar 

  • Vidau C, Gonzalez-Polo RA, Niso-Santano M, Gómez-Sánchez R, Bravo-San Pedro JM, Pizarro-Estrella E, Blasco R, Brunet J-L, Belzunces LP, Fuentes JM (2011) Fipronil is a powerful uncoupler of oxidative phosphorylation that triggers apoptosis in human neuronal cell line SHSY5Y. Neurotoxicology 32:935–943

  • Voss DO, Campelo AP, Bacial M (1961) The respiratory chain and oxidative phosphorylation of rat brain mitochondria. Biochem Biophys Res Commun 4:48–51

    Article  CAS  Google Scholar 

  • Wang X, Zhou S, Ding X, Zhu G, Guo J (2010) Effect of triazophos, fipronil and their mixture on miRNA expression in adult zebrafish. J Environ Sci Heal 45B:648–657

  • Wang C, Qian Y, Zhang X, Chen F, Zhang Q, Li Z, Zhao M (2016) A metabolomic study of fipronil for the anxiety-like behavior in zebrafish larvae at environmentally relevant levels. Environ Pollut 11:252–258

  • Woo SJ, Kim NY, Kim SH, Ahn SJ, Seo JS, Jung SH, Cho MY, Chung JK (2018) Toxicological effects of trichlorfon on hematological and biochemical parameters in Cyprinus carpio L. following thermal stress. Comp Biochem Physiol 209C:18–27

  • Wu HH, Gao C, Guo YP, Zhang Y, Zhang J, Ma E (2014) Acute toxicity and sublethal effects of fipronil on detoxification enzymes in juvenile zebrafish (Danio rerio). Pestic Biochem Physiol 115:9–14

    Article  CAS  Google Scholar 

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Funding

This research was financially supported by the Major Science and Technology Program for Water Pollution Control and Treatment of China (2018ZX07208-001), the National Natural Science Foundation of the People’s Republic of China (41503106; 41807343; 41977270), and Inner Mongolia Natural Science Foundation (2018MS4011).

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Authors and Affiliations

  1. State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing, 100012, China

    Huixian Li, Fuhong Sun & Yahui Zhang

  2. School of Ecology and Environment, Inner Mongolia University, Hohhot, 010021, Inner Mongolia, China

    Ruiqing Zhang

  3. Environmental Analysis and Testing Laboratory of CRAES, Chinese Research Academy of Environmental Sciences, Beijing, 100012, China

    Yahui Zhang

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  1. Huixian Li
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All authors contributed to the study conception and design. The first draft of the manuscript was written by Huixian Li and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Huixian Li or Yahui Zhang.

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The procedures for the use and care of animals complied with Laboratory animal-Guideline for ethical review of animal welfare (GB/T 35892-2018). All experiments were performed according to the Experimental Animal Management Law of China and approved by the Animal Ethics Committee of Chinese Research Academy of Environmental Sciences.

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The authors declare that they have no conflict of interest.

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Li, H., Zhang, R., Sun, F. et al. Evaluation of toxicological responses and promising biomarkers of topmouth gudgeon (Pseudorasbora parva) exposed to fipronil at environmentally relevant levels. Environ Sci Pollut Res 27, 24081–24089 (2020). https://doi.org/10.1007/s11356-020-08555-0

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