Histopathological and biochemical responses to the oxidative stress induced by glyphosate-based herbicides in the rainbow trout (Oncorhynchus mykiss)

Year 2018, Volume: 10 Issue: 1, 656 - 665, 26.04.2018

Gökhan Nur , Haci Ahmet Deveci

https://doi.org/10.37212/jcnos.418666

Cited By: 7

Abstract

This study aimed to determine the effects of glyphosate, a herbicide commonly used in weed control, on aquatic life. For this purpose, 30 one-year-old rainbow trout with an average weight of 150-165 g were obtained from a local trout production station in Mazmanlı (Hatay, Turkey) and transferred to our laboratory, where they were allowed to adapt to the new environment in polyethylene tanks approximately for 7 days. Three groups each containing 10 fish were formed: a control group with no treatment, the group treated with 1.25 mg/l glyphosate-based herbicide (GBH), and the group treated with 2.5 mg/l glyphosate-based herbicide. At the end of 14 days of treatment, blood samples were taken from the caudal vein of the fish under anaesthesia, and their sera were separated. Total oxidant/antioxidant levels and paraoxonase activity were analysed in the obtained serum samples. Also, for histopathological examination, gill tissues were removed and fixed in 10% buffered formalin. After the fixation and routine tissue processing (graded alcohols, methyl benzoate and benzol processing), the tissues taken were embedded in paraffin and 5 μm serial sections were taken by microtome from the blocks to slides pre-coated with chrome alum gelatine. Histopathological changes were examined at the light microscopic level by staining the sections with haematoxylin-eosin. According to the evaluation of the biochemical parameters obtained from the groups, antioxidant capacity and paraoxonase activity decreased and oxidant level increased in the group treated with 1.25 and 2.5 mg/l glyphosate-based herbicide as compared with the control group. In the

histopathological examination of the sections, it was observed that the primary and secondary lamellae had a normal structure in the gill sections obtained from the control group. Irregular secondary lamellae and epithelial hyperplasia were observed in the gill sections obtained from the group receiving 1.25 mg/l GBH. And in the gill sections obtained from the group receiving 2.5 mg/ l GBH, swelling in chloride cells, degeneration in secondary lamellae, and areas of necrosis were detected. In conclusion, results of the study suggests that glyphosate, which is widely used in agricultural activities and has a potential to leak into aquatic ecosystems, may cause oxidative stress due to reactive oxygen species formed in the rainbow trout, and may therefore has a toxic effect.

Keywords

Oncorhynchus mykiss; Glyphosate-based herbicide; Oxidative stress; Histopathology; Gill.

References

• Aksu P, Gül S, Ozkan O, Nur G, Kaya ÖT. 2008. Evaluation of the acute toxicity and genotoxicity of NaOCI on blackbrow bleak (Acanthalburnus microlepis, De Filippi 1863). Fresen Environ Bull. 17:298-302.
• Atamanalp M, Aksakal E, Kocaman EM, Uçar A, Şişman T, Türkez H. 2011. Kobalt klorite maruz kalan gökkuşağı (O. mykiss)’nın kan parametrelerindeki değişimler. Kafkas Univ Vet Fak Derg. 17:573-576.
• Atamanalp M, Keleş MS, Haliloğlu Hİ, Aras MS. 2002a. The effects of cypermethrin (a synthetic pyrethroid) on some biochemical parameters (Ca, P, Na and TP) of rainbow trout (O. mykiss). Turk J Vet Anim Sci. 26:1157-1160. Atamanalp M, Yanık T, Haliloğlu Hİ, Aras MS. 2002b. Alterations in the hematological parameters of rainbow trout, Oncorhynchus mykiss, exposed to cypermethrin. Isr J Aquac. 54(2):99-103.
• Altınok İ, Çapkın E. 2007. Histopathology of rainbow trout exposed to subletal concentrations of methiocarb or endosulfan. Toxicol Pathol. 35:405-410.
• Baylis AD. 2000. Why glyphosate is a global herbicide: strenghts, weakness and prospects. Pest Manag Sci. 56:299-308.
• Boran H, Altınok İ, Çapkın E. 2010. Histopathological changes induced by maneb and carbaryl on some tissues of rainbow trout (O. mykiss). Tissue Cell. 42:158-164.
• Cengiz Eİ. 2006. Gill and kidney histopathology in the freshwater fish Cyprinus carpio after acute exposure to deltamethrin. Environ Toxicol Pharmacol. 22:200-204.
• Cox C. 2004. Herbicide factsheet: Glyphosate. J Pest Ref. 24:10-15.
• Cox C. 1998. Glyphosate (Roundup). J Pest Ref. 18:3-17.
• Cox C. 1995. Glyphosate, Part 2: Human exposure and ecological effects. J Pest Ref. 15:14-20.
• Çavas T, Könen S. 2007. Detection of cytogenetic and DNA damage in peripheral erythrocytes of goldfish (Carassius auratus) exposed to a glyphosate formulation using the micronucleus test and the comet assay. Mutagenesis 22:263-268.
• Dallegrave E, Mantase FD, Coelho RS, Pereira JD, Dalsanter PR, Langeloh A. 2003. The Teratogenic potential of the herbicide glifosat-roundup in wistar rats. Toxicol Lett. 142:45-52.
• Deveci HA, Unal S, Karapehlivan M, Ayata MK, Gaffaroglu M, Kaya I, Yilmaz M. 2017. Effects of glyphosate (herbicide) on serum paraoxonase activity, high density lipoprotein, total antioxidant and oxidant levels in kars creek transcaucasian barbs (Capoeta capoeta [Guldenstaedt, 1773]). Fresen Environ Bull. 26(5):3514-3518.
• Duran S, Erdem C. 2013. Effects of sublethal concentratıons of copper, zinc and cadmium, applied singly and in mixture, on some hematological parameters of Oreochromis niloticus (L., 1758). Fresen Environ Bull. 22(10a):2977-2980.
• Eckerson HW, Romson J, Wyte CM, La Du BN. 1983. The human serum paraoxonase polymorphism: Identification of phenotypes by their response to salts. Am J Hum Genet. 35:214-227.
• Erel Ö. 2004. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable abts radical cation. Clin Biochem. 37:277-285.
• Erel Ö. 2005. A new automated colorimetric method for measuring total oxidant status. Clin Biochem. 38:1103-1111.
• Glusczak L, dos Santos Miron D, Crestani M, Braga da Fonseca M, Araujo Pedron F, Duarte MF, Vieira VL. 2006. Effect of glyphosate herbicide on acetylcholinesterase activity and matabolic and hematological parameters in piava (Leporinus obtusidens). Ecotoxicol Environ Saf. 65:237-241.
• Glusczak L, dos Santos Miron D, Moraes BS, Simxes RR, Schetinger MR, Morsch VM, Loro VL. 2007. Acute effects of glyphosate herbicide on metabolic and enzymatic parameters of silver catfish (Rhamdia quelen). Comp Biochem Physiol C. 146:519-524.
• Giesy JP, Dobson S, Solomon KR. 2000. Ecotoxicological risk assessment for roundup herbicide. Rev Environ Contam Toxicol. 167:35-120.
• Güven A, Gül S, Kaya İ, Nur G, Deveci HA, Kaya OT. 2008. Antioxidant enzymes and lipit peroxidation in Alburnus filippii (Kessler, 1877) and Acanthalburnus microlepis (Filippi, 1863): A comparative study. Kafkas Univ Vet Fak Derg. 14:13-18.
• Guilherme S, Santos MA, Barroso C, Gaivao I, Pacheco M. 2012. Differential genotoxicity of roundup formulation and its constituents in blood cells of fish (Anguilla anguilla): considerations on chemical interactions and DNA damaging mechanisms. Ecotoxicology. 21:1381-1390.
• Gül S, Ozkan O, Nur G, Aksu P. 2008. Genotoxic effects and LC50 value of NaOCI on Orthrias angorae (Steindachner, 1897). Bull Environ Contam Toxicol. 80(6):544-548.
• Gülcü F, Gürsu MF. 2003. Paraoksonaz ve aril esteraz aktivite ölçümlerinin standardizasyonu. Turk J Biochem. 28:45-49.
• He H, Yu J, Chen G, Li W, He J, Li H. 2012. Acute toxicity of butachlor and atrazine to freshwater green alga Scenedesmus obliquus and cladoceran Daphnia carinata. Ecotoxicol Environ Saf. 80:91-96.
• Kayhan FE, Muşlu MN, Koç ND. 2009. Bazı ağır metallerin sucul organizmalar üzerinde yarattığı stres ve biyolojik yanıtlar. J Fisher Sci. 3:153-162.
• Kolpin DW, Thurman EM, Lee EA, Meyer MT, Furlong ET, Glassmeyer ST. 2006. Urban contributions of glyphosate and its degragrade AMPA to streams in the United States. Sci Total Environ. 354:191-197.
• Langiano VDC, Martinez CBR. 2008. Toxicity and effects of a glyphosate-based herbicide on the Neotropical fish Prochilodus lineatus. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol. 147:222-231.
• Lendhardt M. 1992. Seasonal changes in some blood chemistry parameters and in relative liver and gonad weights of pike (Essox lucius) from River Danube. J Fish Biol. 40:709-718.
• Lushchak OV, Kubrak OI, Torous IM, Nazarchuk TY, Storey KB, Lushchak VI. 2009. Trivalent chromium induces oxidative stress in goldfish brain. Chemosphere 75:56-62.
• Lusková V. 1997. Annual cycles and normal values of hematological parameters in fishes. Acta Sci Nat Brno. 31(5), 70 p.
• Medina HSG, Lopata ME, Bacila M. 1994. The response of sea-urchin egg embryogenesis towards the effect of some pesticides. Arq Biol Tecnol. 37:895-906.
• Modesto KA, Martinez CBR. 2010. Effect of roundup transorb on fish: Hematology, antioksidant defenses and acetylcholinesterase activity. Chemosphere 81:781-787.
• Mitchell DG, Chapman PM, Long TJ. 1987. Acute toxicity of Roundup© and Rodeo© herbicides to rainbow trout, chinook, and coho salmon. Arch Environ Contamin Toxicol. 39:1028-1035.
• Nwani CD, Nagpure NS, Kumar R, Kushwaha B, Lakra WS. 2013. DNA damage and oxidative stress modulatory effects of glyphosate-based herbicide in freshwater fish, Channa punctatus. Environ Toxicol Pharm. 36:539-547.
• Ozkan O, Gül S, Keles O, Aksu P, Kaya OT, Nur G. 2009. The Investigation of the mutagenic activity of Kars river sediments on Orthrias angorae (Steindachner, 1897). Kafkas Univ Vet Fak Derg. 15:35-40.
• Piska MB, Waghray S. 1997. Toxic effects of dimethoate on primary production of lake ecosystem. Indian J Environ Health. 33:126-127.
• Pline WA, Price AJ, Wilcut JW, Edmisten KL, Wells R. 2001. Adsorption and translocation of glyphosate in glyphosate-resistant cotton as influenced by application method and growth stage. Weed Sci. 49:460-7.
• Presnell J, Schreibman MP. 1997. Animal tissue techniques. 5 th ed. The Johns Hopkins University Pres Ltd. London, pp.269-271.
• Rezende dos Santos AP, Rocha TL, Borges CL, Bailao AM, De Almeida Soares CM, De Saboia-Morais SMT. 2017. A glyphosate-based herbicide induces histomorphological and protein expression changes in the liver of the female guppy Poecilia reticulata. Chemosphere 168:933-943.
• Ross LG, Ross B. 2008. Anaesthetic and sedative techniques for aquatic animals. 3rd Edition, John Wiley&Sons, Oxford, 240 pages.
• Santos BM, Gilreath JP, Camile EE, Siham MN. 2007. Effects of sublethal glyphosate rates on fresh market tomato. Crop Prot. 26:89-91.
• Soso AB, Barcellos LJG, Ranzai-Paiva MJ, Kreutz LC, Quevedo RM, Anziliero D, Lima M, Silva LB, Ritter F, Bedin AC, Finco JA. 2007. Chronic exposure to sub-lethal concentration of a glyphosate-based herbicide alters hormone profiles and affects reproduction of female Jundiá (Rhamdia quelen). Environ Toxicol Pharmacol. 23:308-313.
• Tate TM, Spurlock JO, Christian FA. 1997. Effect of glyphosate on the development of Pseudosuccinea columella snails. Arch Environ Contam Toxicol. 33:286-9.
• Topal A, Atamanalp M, Uçar A, Oruç E, Kocaman EM, Sulukan E, Akdemir F, Beydemir Ş, Kılınç N, Erdoğan O, Ceyhun SB. 2015. Effects of glyphosate on juvenile rainbow trout (Oncorhynchus mykiss): Transcriptional and enzymatic analyses of antioxidant defence system, histopathological liver damage and swimming performance. Ecotoxicol Environ Saf. 111:206-214.
• US Environmental Protection Agency. 2011. Pesticides industry sales and usage, 2006 and 2007 Market Estimates. Washington, DC: US Environmental Protection Agency. Available at:(http://www.epa.gov/opp00001/pestsales/07pestsales/market_estimates2007.pdf).
• Vollenhofer S, Burg K, Schmidt J, Kroath H. 1999. Genetically modified organisms in foodscreeening and specific detection by polymerase chain reaction. J Agric Food Chem. 7:5038-5043.
• Williams GM, Kroes R, Munro IC. 2000. Safety evaluation and risk assessment of the herbicide roundup and its active ingredient, glyphosate, for humans. Regul Toxicol Pharmacol. 31:117-165.