Advertisement

Toxicological impact of oxyfluorfen 24% herbicide on the reproductive system, antioxidant enzymes, and endocrine disruption of Biomphalaria alexandrina (Ehrenberg, 1831) snails

  • Amina Mohamed IbrahimEmail author
  • Dawlat A. Sayed
Research Article
  • 52 Downloads

Abstract

Oxyfluorfen (Goal 24%EC) herbicide is widely used in agriculture for weed control. Biomphalaria alexandrina snails can be used as bioindicator of the chemical pollution in the aquatic environment. The objective of this study was to evaluate the molluscicidal activity of this herbicide on Biomphalaria alexandrina snails and how it affected its biological system. The present study revealed a molluscicidal effect of oxyfluorfen 24%EC on these snails at LC50 5.9 mg/l. After exposure of snails to the sub-lethal concentrations (LC0, LC10, or LC25) of this herbicide, the survival rates, reproductive rate (R0), and fecundity (Mx) of adult B. alexandrina snails were significantly decreased in comparison with the control group. Also, levels of testosterone and estradiol were decreased significantly. It caused alterations in the antioxidant system, where exposure to sub-lethal concentration of this herbicide caused significant increases in levels of lipid peroxide malondialdehyde (MDA), catalase (CAT), and superoxide dismutase (SOD), while it significantly decreased glutathione transferase (GST). Histopathological changes in the digestive gland included severe damage in the digestive cells, where, they lost their tips and some were degenerated, while the secretory cells increased in number. Regarding the hermaphrodite gland, there were losses of the connective tissues, irregular sperms, and the eggs degenerated. These findings concluded that B. alexandrina snails can be used as a bioindicator for pollution with pesticide in the aquatic environment.

Keywords

Oxyfluorfen 24%EC Biomphalaria alexandrina Reproductive rate Oxidative stress Endocrine disruptor Histology 

Notes

Compliance with ethical standards

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abdel-Ghaffar F, Ahmed AK , Bakry F, Rabei I, Ibrahim A (2016) The impact of three herbicides on biological and histological aspects of biomphalaria alexandrina, intermediate host of Schistosoma mansoni. Malacologia 59(2):197–210Google Scholar
  2. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126CrossRefGoogle Scholar
  3. Atli G, Grosell M (2016) Characterization and response of antioxidant systems in the tissues of the freshwater pond snail (Lymnaea stagnalis) during acute copper exposure. Aquat Toxicol 176:38–44.  https://doi.org/10.1016/j.aquatox.2016.04.007 CrossRefGoogle Scholar
  4. Bagul PK, More BC, Patole SS (2016) Sub lethal effects of cypermethrin and oxyfluorfen on stress enzyme activities of earthworm species, Eisenia foetida Savigny, 1826. Int J Innov Res Sci Eng Technol.  https://doi.org/10.15680/IJIRSET.2016.0512047
  5. Banhawy MA, Soliman FM, Abdel-Rehim SA, Hamada HMA (1996) Metabolic changes in the Nile bolti Oreochromis niloticus exposed to different concentrations of the herbicide (Goal). Proc Egypt Acad Sci 46:99–117Google Scholar
  6. Barky FA, Abdelsalam HA, Mahmoud MB, Hamdi SAH (2012) Influence of Atrazine and Roundup pesticides on biochemical and molecular aspects of Biomphalaria alexandrina snails. Pestic Biochem Physiol 104:9–18.  https://doi.org/10.1016/j.pestbp.2012.05.012 CrossRefGoogle Scholar
  7. Beutler E (1963) Improved method for determination of blood glutathione. J Lab Clin Med 61:882–888Google Scholar
  8. Clair É, Mesnage R, Travert C, Séralini G-É (2012) A glyphosate-based herbicide induces necrosis and apoptosis in mature rat testicular cells in vitro, and testosterone decrease at lower levels. Toxicol in Vitro 26:269–279CrossRefGoogle Scholar
  9. El-Gindy MS, Radhawy IA et al (1965) Effect of low concentrations of sodium pentachlorophenate on the fecundity and egg viability of Bulinus truncatus from Central Iraq. Bull Endem Dis (Baghdad) 7:44–54Google Scholar
  10. EPA/OPP US (U. SEPA of PP) (2001) Revised Environmental Fate and Effects Division preliminary risk assessment for oxyfluorfen reregistration eligibility decision document. http://fluoridealert.org/wpcontent/pesticides/oxyfluorfen.enveffects.2001.pdf
  11. Eveland LK, Haseeb MA (2011) Laboratory rearing of Biomphalaria glabrata snails and maintenance of larval Schistosomes in vivo and in vitro. In: Biomphalaria snails and larval trematodes. Springer New York, New York, pp 33–55CrossRefGoogle Scholar
  12. Fahmy SR, Sayed DA (2017) Toxicological perturbations of zinc oxide nanoparticles in the Coelatura aegyptiaca mussel. Toxicol Ind Health 33(7):564–575CrossRefGoogle Scholar
  13. Fahmy SR, Abdel-Ghaffar F, Bakry FA, Sayed DA (2014) Ecotoxicological effect of sublethal exposure to zinc oxide nanoparticles on freshwater snail Biomphalaria alexandrina. Arch Environ Contam Toxicol 67:192–202CrossRefGoogle Scholar
  14. Finney DJ (1971) Probit analysis, 3rd edn. Cambrige University Press, CambrigeGoogle Scholar
  15. Godfrey W, Longacre S (1990) Rohm and Haas Company Phase 3 Summary of MRID 00134452. Goal Technical Herbicide Oxyfluorfen Acute Toxicity to the Freshwater Clam: Rohm and Haas Report 77RC-1103; UCES Project No. 11506–33-02. Prepared by Union Carbide Corp. 14 pGoogle Scholar
  16. Hasheesh WS, Mohamed RT (2011) Bioassay of two pesticides on Bulinus truncatus snails with emphasis on some biological and histological parameters. Pestic Biochem Physiol 100:1–6CrossRefGoogle Scholar
  17. Hassanein HMA (2002) Toxicological effects of the herbicide oxyfluorfen on acetylcholinesterase in two fish species: Oreochromis niloticus and Gambusia affinis. J Environ Sci Health A 37:521–527CrossRefGoogle Scholar
  18. Ibrahim MA, Ahmed AK et al (2018) Hematological, physiological and genotoxicological effects of Match 5% EC insecticide on Biomphalaria alexandrina snails. Ecotoxicol Environ Saf:147.  https://doi.org/10.1016/j.ecoenv.2017.09.059
  19. Keum YS, Lee YJ, Han KJ (2008) Metabolism of nitrodiphenyl ether herbicides by dioxin-degrading bacterium Sphingomonas wittichii RW1. J Agric Food Chem 56:9146–9151.  https://doi.org/10.1021/jf801362k CrossRefGoogle Scholar
  20. Langiano do CV, Martinez RC (2008) Toxicity and effects of a glyphosate-based herbicide on the Neotropical fish Prochilodus lineatus. Comp Biochem Physiol C Toxicol Pharmacol 147:222–231CrossRefGoogle Scholar
  21. Litchfield JT Jr, Wilcoxon F (1949) A simplified method of evaluating dose-effect experiments. J Pharmacol Exp Ther 96:99–113Google Scholar
  22. Mohamed SH, Saad AA (1990) Histological studies on the hermaphrodite gland of Lymnaea caillaudi and Biomphalaria alexandrina upon infection with certain larval trematodes. Egypt J Histol 13:47–53Google Scholar
  23. Moustafa GG, Shaaban FE, Hadeed AH, AboElhady WM (2016) Immunotoxicological, biochemical, and histopathological studies on roundup and stomp herbicides in Nile catfish (Clarias gariepinus). Vet World 9:638–647.  https://doi.org/10.14202/vetworld.2016.638-647 CrossRefGoogle Scholar
  24. Nduku WK, Harrison AD (1980) Cationic responses of organs and haemolymph of Biomphalaria pfeifferi (Krauss), Biomphalaria glabrata (Say) and Helisoma trivolvis (Say)(Gastropoda: Planorbirdae) to cationic alterations of the medium. Hydrobiologia 68:119–138CrossRefGoogle Scholar
  25. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358CrossRefGoogle Scholar
  26. Omran NE, Salama WM (2016) The endocrine disruptor effect of the herbicides atrazine and glyphosate on Biomphalaria alexandrina snails. Toxicol Ind Health 32:656–665CrossRefGoogle Scholar
  27. Osman GY, Mohamed AH, Mohamed AM, Al-Qormuti SA (2008) Effect of Roundup herbicide on biological activity of Biomphalaria alexandrina snails infected with Schistosoma mansoni. Mansoura J Biol 35:147–167Google Scholar
  28. Pašková V, Hilscherová K, Bláha L (2011) Teratogenicity and embryotoxicity in aquatic organisms after pesticide exposure and the role of oxidative stress. In: Reviews of environmental contamination and toxicology, vol 211. Springer, Berlin, pp 25–61Google Scholar
  29. Peixoto F, Alves-Fernandes D, Santos D, Fontainhas-Fernandes A (2006) Toxicological effects of oxyfluorfen on oxidative stress enzymes in tilapia Oreochromis niloticus. Pestic Biochem Physiol 85:91–96CrossRefGoogle Scholar
  30. Sharaf HM, Salama MA, Abd El-Atti MS (2015) Biochemical and histological alterations in the digestive gland of the land snail Helicella vestalis (Locard, 1882) exposed to methiocarb and chlorpyrifos in the laboratory. Int J Sci Res 4:334–343Google Scholar
  31. Sharaf-El-Din AT, Mohamed AM, Mohamed AH et al (2010) Relationship between some heavy metals and Schistosoma mansoni infection rates in Biomphalaria alexandrina snails collected from different Egypt localities. World Appl Sci J 11:38–43Google Scholar
  32. Talib AH, AL-Rudainy JA et al (2018) The acute toxicity of herbicide roundup ultra in mosquito fish Gambusia affinis. J Biodivers Environ Sci 13:9–15Google Scholar
  33. Tellez-Bañuelos MC, Santerre A, Casas-Solis J, Bravo-Cuellar A, Zaitseva G (2009) Oxidative stress in macrophages from spleen of Nile tilapia (Oreochromis niloticus) exposed to sublethal concentration of endosulfan. Fish Shellfish Immunol 27:105–111CrossRefGoogle Scholar
  34. Tilton F, La Du JK, Tanguay RL (2008) Sulfhydryl systems are a critical factor in the zebrafish developmental toxicity of the dithiocarbamate sodium metam (NaM). Aquat Toxicol 90:121–127CrossRefGoogle Scholar
  35. Tsui M, Chu LM (2008) Environmental fate and non-target impact of glyphosate-based herbicide (Roundup®) in a subtropical wetland. Chemosphere 71:439–446CrossRefGoogle Scholar
  36. Vera-Candioti J, Safety SS-… and environmental, 2013 U (2012) Evaluation of the genotoxic and cytotoxic effects of glyphosate-based herbicides in the ten spotted live-bearer fish Cnesterodon decemmaculatus (Jenyns, 1842). Ecotoxicol Environ Saf 89:166–173CrossRefGoogle Scholar
  37. Warren E (1900) Memoirs: on the reaction of Daphnia magna (Straus) to certain changes in its environment. J Cell Sci 2:199–224Google Scholar
  38. WHO (1965) Molluscicide screening and evaluation. Bull WHO 33:567–581Google Scholar
  39. WHO (1983) Report of the scientific working group on Plant Molluscicide & Guidelines for evaluation of plant molluscicides. WHO, Geneva (TDR/SCHSWE (4)/833Google Scholar
  40. WHO (1993) The control of schistosomiasis, Technical Report Series Geneva Switz, pp 1–86Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Environmental Research and Medical Malacology DepartmentTheodor Bilharz Research InstituteGizaEgypt
  2. 2.Zoology department, Faculty of ScienceCairo UniversityGizaEgypt

Personalised recommendations