Surfactants involvement in the toxicity of glyphosate-based herbicides on the cerebral of African catfish (Clarias gariepinus)

Authors

  • Titilope Ayoola Iyanda Department of Environmental Chemistry, Federal University of Technology, Akure 704, Ondo State, Nigeria Author
  • Ademola Festus Ayesanmi Department of Environmental Chemistry, Federal University of Technology, Akure 704, Ondo State, Nigeria Author
  • Ige Joseph Kade Department of Biochemistry, Federal University of Technology, Akure 704, Ondo State, Nigeria Author

DOI:

https://doi.org/10.65746/pec61

Keywords:

Clarias gariepinus; force up; glyphosate herbicides; mortality; round up; surfactant

Abstract

The proliferation of glyphosate-based herbicides is becoming a global menace due to their economic viability, thereby resulting in their indiscriminate usage among the consumers. Consequently, there is an increase in the occurrence of these herbicides in aquatic bodies, posing a threat to aquatic life. The present study sought to investigate the variations in toxicities of glyphosate-based herbicides in African catfish (Clarias gariepinus). Evaluation of the response of Clarias gariepinus juveniles when exposed to glyphosate-based herbicides, namely Round Up (RU) and Force Up (FU), during a range study, which was between 0.0 and 5000 mg/L in thousand doses, was carried out for 96 h. Thereafter, fish were exposed to lower concentrations of RU and higher concentrations of FU. Additionally, the effects of glyphosate-based herbicides were evaluated in surviving catfish for biochemical indices (enzymatic and redox status). At the expiration of the exposure period, there was total mortality of fish in the group treated with RU, while zero mortality was observed in the FU-treated group. As a result, RU concentration was downscaled to 0.0–200 mg/L in arithmetic progression, while FU was increased to 4800–5800 mg/L. Round Up was observed to have more toxicological effect on the biochemical indices investigated namely; lipid peroxidation, 1, 1-diphenyl-2 picrylhydrazyl (DPPH) radical scavenging property, ferric radical-reducing antioxidant property (FRAP), glutathione (γ-glutamylcysteinyl glycine (GSH)) levels, and the modulation of activities of redox-sensitive enzymes in the cerebral tissues of exposed catfish than observed with Force Up. Therefore, the variation in toxicological effects of these glyphosate herbicide products confers more or less toxicity on the environment, and this may be a function of the composition of surfactants included in their individual formulations.

References

1. Erhunmwunse NO, Ogbeide OS, Tongo II, et al. Acute toxicity of glyphosate-based isopropylamine formulation to juvenile African catfish (Clarias gariepinus). Nigerian Journal of Basic and Applied Science. 2018; 26(2): 97-101. doi: 10.5455/NJBAS.271521

2. Duke SO, Powles SB. Glyphosate-resistant crops and weeds: Now and in the future. AgBioForum. 2009; 12(3-4): 346-357.

3. Székács A, Darvas B. Forty years with glyphosate. In: Hasaneen MN (editor). Herbicides—Properties, Synthesis and Control of Weeds. InTech; 2012. pp. 247-284. doi: 10.5772/32491

4. Bureau of National Affairs. Monsanto reports higher Q2 income for ag chems, Green Markets Pesticide Report 2, 3 August 1998 (cited in Cox C, Glyphosate (Roundup), Journal of Pesticide Reform, 18(3) 3-16, 1998). Bureau of National Affairs; 1998.

5. Perry ED, Hennessy DA, Moschini G. Product concentration and usage: Behavioral effects in the glyphosate market. Journal of Economic Behavior & Organization. 2019; 158: 543-559. doi: 10.1016/j.jebo.2018.12.027

6. Franz JE, Mao MK, Sikorski JA. Glyphosate: A unique Global Herbicide. American Chemical Society; 1997.

7. Henderson AM, Gervais JA, Luukinen B, et al. Glyphosate General Fact Sheet. National Pesticide Information Center, Oregon State University Extension Services. Available online: http://npic.orst.edu/factsheets/archive/glyphotech.html (accessed on 15 February 2025).

8. Iyanda TA, Ayesanmi AF, Kade IJ, et al. Acute toxicological effect of glyphosate-based herbicide (round up) with cadmium as a co-contaminant on African catfish (Clarias gariepinus). Advanced Journal of Chemistry Research. 2023; 1(2): 20-28. doi: 10.31248/AJCR2023.004

9. Sikorski Ł, Baciak M, Bęś A, Adomas B. The effects of glyphosate-based herbicide formulations on Lemna minor, a non-target species. Aquatic Toxicology. 2019; 209: 70-80. doi: 10.1016/j.aquatox.2019.01.021

10. Da Fonseca MB, Glusczak L, Moraes BS, et al. The 2,4-D herbicide effects on acetylcholinesterase activity and metabolic parameters of piava freshwater fish (Leporinus obtusidens). Ecotoxicology and Environmental Safety. 2008; 69(3): 416-420. doi: 10.1016/j.ecoenv.2007.08.006

11. Salbego J, Pretto A, Gioda CR, et al. Herbicide formulation with glyphosate affects growth, acetylcholinesterase activity, and metabolic and hematological parameters in piava (Leporinus obtusidens). Archives of Environmental Contamination and Toxicology. 2010; 58(3): 740-745. doi: 10.1007/s00244-009-9464-y

12. Glusczak L, Loro VL, Pretto A, et al. Acute exposure to glyphosate herbicide affects oxidative parameters in piava (Leporinus obtusidens). Archives of Environmental Contamination and Toxicology. 2011; 61(4): 624-630. doi: 10.1007/s00244-011-9652-4

13. Annett R, Habibi HR, Hontela A. Impact of glyphosate and glyphosate‐based herbicides on the freshwater environment. Journal of Applied Toxicology. 2014; 34(5): 458-479. doi: 10.1002/jat.2997

14. Awoke JS, Nwele HO, Oti EE, Okoro CB. Acute toxicity effect of Mulsate (glyphosate) herbicide on behaviour and haematological indices of African catfish (Clarias gariepinus Burchell 1822) juvenile. International Journal of Oceanography & Aquaculture. 2023; 7(3): 000262. doi: 10.23880/ijoac-16000262

15. Alarape SA, Fagbohun AF, Ipadeola OA, et al. Assessment of glyphosate and its metabolites’ residue concentrations in cultured African catfish offered for sale in selected markets in Ibadan, Oyo State, Nigeria. Frontiers in Toxicology. 2023; 5: 1250137. doi: 10.3389/ftox.2023.1250137

16. Song HY, Kim YH, Seok SJ, et al. Cellular toxicity of surfactants used as herbicide additives. Journal of Korean Medical Science. 2012; 27(1): 3-9. doi: 10.3346/jkms.2012.27.1.3

17. Bradberry SM, Proudfoot AT, Vale JA. Glyphosate poisoning. Toxicological Reviews. 2004; 23(3): 159-167. doi: 10.2165/00139709-200423030-00003

18. Altenburger R, Nendza M, Schüürmann G. Mixture toxicity and its modeling by quantitative structure-activity relationships. Environmental Toxicology and Chemistry. 2003; 22(8): 1900-1915. doi: 10.1897/01-386

19. Lydy M, Belden J, Wheelock C, et al. Challenges in regulating pesticide mixtures. Ecology and Society. 2004; 9(6): 1. doi: 10.5751/es-00694-090601

20. Belden JB, Gilliom RJ, Lydy MJ. How well can we predict the toxicity of pesticide mixtures to aquatic life? Integrated Environmental Assessment and Management. 2007; 3(3): 364-372. doi: 10.1002/ieam.5630030307

21. Shiogiri N, Carraschi SP, Cubo P, et al. Ecotoxicity of glyphosate and aterbane® br surfactant on guaru (Phalloceros caudimaculatus). Acta Scientiarum Biological Sciences. 2010; 32(3): 285-289. doi: 10.4025/actascibiolsci.v32i3.6795

22. Nwani CD, Nagpure NS, Kumar R, et al. DNA damage and oxidative stress modulatory effects of glyphosate-based herbicide in freshwater fish, Channa punctatus. Environmental Toxicology and Pharmacology. 2013; 36(2): 539-547. doi: 10.1016/j.etap.2013.06.001

23. Mesnage R, Bernay B, Séralini GE. Ethoxylated adjuvants of glyphosate-based herbicides are active principles of human cell toxicity. Toxicology. 2013; 313(2-3): 122-128. doi: 10.1016/j.tox.2012.09.006

24. Mikó Z, Hettyey A.Toxicity of POEA-containing glyphosate-based herbicides to amphibians is mainly due to the surfactant, not to the active ingredient. Ecotoxicology. 2023; 32(2): 150–159. doi: 10.1007/s10646-023-02626-x

25. Amreen B, Lesseur C, Jagani R, et al. A pilot study to evaluate exposure to polyoxyethylene tallow amine (POEA), a glyphosate formulation adjuvant, in a US pregnant population. ISEE Conference Abstracts. 2024; 2024(1). doi: 10.1289/isee.2024.1936

26. Polli A, Alves GS, de Moraes JG, Kruger GR. Influence of surfactant-humectant adjuvants on physical properties, droplet size, and efficacy of glufosinate formulations. Agrosystems, Geosciences & Environment. 2022; 5(1): e20230. doi: 10.1002/agg2.20230

27. Burdiss C, Vosburgh MA, Stuart YE, Milanovich JR. The impacts of glyphosate and common co-formulations with surfactant and dye on American toad fitness. Ichthyology & Herpetology. 2024; 112(4): 652-658. doi: 10.1643/h2023007

28. Klátyik S, Simon G, Oláh M, et al. Aquatic ecotoxicity of glyphosate, its formulations, and co-formulants: Evidence from 2010 to 2023. Environmental Sciences Europe. 2024; 36(1): 22. doi: 10.1186/s12302-024-00849-1

29. Shalaby AM, Khattab YA, Abdel Rahman AM. Effects of Garlic (Allium sativum) and chloramphenicol on growth performance, physiological parameters and survival of Nile tilapia (Oreochromis niloticus). Journal of Venomous Animals and Toxins including Tropical Diseases. 2006; 12(2): 172-201. doi: 10.1590/s1678-91992006000200003

30. Chinedu E, Arome D, Ameh F. A new method for determining acute toxicity in animal models. Toxicology International. 2013; 20(3): 224-226. doi: 10.4103/0971-6580.121674

31. Kade IJ, Rocha JBT. Comparative study on the influence of subcutaneous administration of diphenyl and dicholesteroyl diselenides on sulphydryl proteins and antioxidant parameters in mice. Journal of Applied Toxicology. 2010; 30(7): 688-693. doi: 10.1002/jat.1542

32. Kade IJ, Nogueira CW, Rocha JBT. Diphenyl diselenide and streptozotocin did not alter cerebral glutamatergic and cholinergic systems but modulate antioxidant status and sodium pump in diabetic rats. Brain Research. 2009; 1284: 202-211. doi: 10.1016/j.brainres.2009.04.003

33. Kade IJ, Paixão MW, Rodrigues OED, et al. Comparative studies on dicholesteroyl diselenide and diphenyl diselenide as antioxidant agents and their effect on the activities of Na+/K+ ATPase and δ-aminolevulinic acid dehydratase in the rat brain. Neurochemical Research. 2008; 33(1): 167-178. doi: 10.1007/s11064-007-9432-8

34. Jones DP, Carlson JL, Mody VC, et al. Redox state of glutathione in human plasma. Free Radical Biology & Medicine. 2000; 28(4): 625-635. doi: 10.1016/s0891-5849(99)00275-0

35. Nogueira CW, Zeni G, Rocha JBT. Organoselenium and organotellurium compounds: Toxicology and pharmacology. Chemical Reviews. 2004; 104(12): 6255-6286. doi: 10.1021/cr0406559

36. Ukaegbu MC, Olatunde AO, Iheme PO, Uwa C. The sub-lethal effect of round-up (a glyphosate-based herbicide) on juveniles of African catfish (Clarias gariepinus). South Asian Journal of Experimental Biology. 2022; 12(2): 167-176. doi: 10.38150/sajeb.12(2).p167-176

37. Edeh IC, Nsofor CI, Iheanacho SC, et al. Behavioural and haematological alterations in the African catfish (Clarias gariepinus) exposed to varying concentrations of glyphosate. Asian Journal of Fisheries and Aquatic Research. 2023; 21(1): 32-42. doi: 10.9734/ajfar/2023/v21i1527

38. Mann RM, Bidwell JR. The toxicity of glyphosate and several glyphosate formulations to four species of southwestern Australian frogs. Archives of Environmental Contamination and Toxicology. 1999; 36(2): 193-199. doi: 10.1007/s002449900460

39. Pessagno RC, Grassi D, Pedraza C, et al. Eco-friendly surfactants in glyphosate formulation. Revista de Ciências Agroveterinárias. 2021; 20(3): 213-221. doi: 10.5965/223811712032021213

40. Giesy JP, Dobson S, Solomon KR. Ecotoxicological risk assessment for Roundup® herbicide. In: Ware GW (editor). Reviews of Environmental Contamination and Toxicology. Springer; 2000. Volume 167, pp. 35-120. doi: 10.1007/978-1-4612-1156-3_2

41. Tsui MT, Chu LM. Aquatic toxicity of glyphosate-based formulations: Comparison between different organisms and the effects of environmental factors. Chemosphere. 2003; 52(7): 1189-1197. doi: 10.1016/S0045-6535(03)00306-0

42. Howe CM, Berrill M, Pauli BD, et al. Toxicity of glyphosate-based pesticides to four North American frog species. Environmental Toxicology and Chemistry. 2004; 23(8): 1928-1938. doi: 10.1897/03-71

43. Fan J, Geng J, Ren H, et al. Herbicide Roundup® and its main constituents cause oxidative stress and inhibit acetylcholinesterase in liver of Carassius auratus. Journal of Environmental Science and Health, Part B. 2013; 48(10): 844-850. doi: 10.1080/03601234.2013.795841

44. Romero-Márquez JM, Navarro-Hortal MD, Jiménez-Trigo V, et al. An oleuropein rich-olive (Olea europaea L.) leaf extract reduces β-amyloid and tau proteotoxicity through regulation of oxidative- and heat shock-stress responses in Caenorhabditis elegans. Food and Chemical Toxicology. 2022; 162: 112914. doi: 10.1016/j.fct.2022.112914

45. Bednářová A, Kropf M, Krishnan N. The surfactant polyethoxylated tallowamine (POEA) reduces lifespan and inhibits fecundity in Drosophila melanogaster—In vivo and in vitro study. Ecotoxicology and Environmental Safety. 2020; 188: 109883. doi: 10.1016/j.ecoenv.2019.109883

46. Gandhi K, Khan S, Patrikar M, et al. Exposure risk and environmental impacts of glyphosate: Highlights on the toxicity of herbicide co-formulants. Environmental Challenges. 2021; 4: 100149. doi: 10.1016/j.envc.2021.100149

47. Relyea RA. The lethal impact of roundup on aquatic and terrestrial amphibians. Ecological Applications. 2005; 15(4): 1118-1124. doi: 10.1890/04-1291

48. Mesnage R, Benbrook C, Antoniou MN. Insight into the confusion over surfactant co-formulants in glyphosate-based herbicides. Food and Chemical Toxicology. 2019; 128: 137-145. doi: 10.1016/j.fct.2019.03.053

49. Kumar R, Nagpure NS, Kushwaha B, et al. Investigation of the genotoxicity of malathion to freshwater teleost fish Channa punctatus (Bloch) using the micronucleus test and comet assay. Archives of Environmental Contamination and Toxicology. 2009; 58(1): 123-130. doi: 10.1007/s00244-009-9354-3

50. Olorunfemi DI, Olomukoro JO, Anani OA. Acute toxicity of produced water on Clarias gariepinus juveniles. Studia Universitatis “Vasile Goldiş”, Seria Ştiinţele Vieţii. 2014; 24(3): 299-303.

51. Osioma EI, Ejoh AS. Activities of acetylcholinesterase, oxidative and nitrosative stress markers in Clarias gariepinus exposed to ‘Uproot’, a glyphosate–based herbicide. International Journal of Zoological Investigations. 2021; 7(1): 51-66. doi: 10.33745/ijzi.2021.v07i01.006

52. Zengin H. The effects of feeding and starvation on antioxidant defence, fatty acid composition and lipid peroxidation in reared Oncorhynchus mykiss fry. Scientific Reports. 2021; 11(1): 16716. doi: 10.1038/s41598-021-96204-y

53. Catalá A. An overview of lipid peroxidation with emphasis in outer segments of photoreceptors and the chemiluminescence assay. The International Journal of Biochemistry & Cell Biology. 2006; 38(9): 1482-1495. doi: 10.1016/j.biocel.2006.02.010

54. Mansour AT, Amen RM, Mahboub HH, et al. Exposure to oxyfluorfen-induced hematobiochemical alterations, oxidative stress, genotoxicity, and disruption of sex hormones in male African catfish and the potential to confront by Chlorella vulgaris. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 2023; 267: 109583. doi: 10.1016/j.cbpc.2023.109583

55. Chaijan M, Rodsamai T, Charoenlappanit S, et al. Antioxidant activity and stability of endogenous peptides from farmed hybrid catfish (Clarias macrocephalus × Clarias gariepinus) muscle. International Journal of Food Science and Technology. 2022; 57(2): 1083-1092. doi: 10.1111/ijfs.15474

56. Nasution AY, Sari NN, Fauzana A. Antioxidant activity of peel-off mask from pangasius catfish gelatin (Pangasius hypophthalmus) with astaxhantin. Pharmacon: Jurnal Farmasi Indonesia. 2024; 21(2): 104-109. doi: 10.23917/pharmacon.v21i2.6665

57. García-Moreno PJ, Batista I, Pires C, et al. Antioxidant activity of protein hydrolysates obtained from discarded Mediterranean fish species. Food Research International. 2014; 65: 469-476. doi: 10.1016/j.foodres.2014.03.061

58. Chen YT, Hsieh SL, Gao WS, et al. Evaluation of chemical compositions, antioxidant capacity and intracellular antioxidant action in fish bone fermented with Monascus purpureus. Molecules. 2021; 26(17): 5288. doi: 10.3390/molecules26175288

59. Baliyan S, Mukherjee R, Priyadarshini A, et al. Determination of antioxidants by DPPH radical scavenging activity and quantitative phytochemical analysis of Ficus religiosa. Molecules. 2022; 27(4): 1326. doi: 10.3390/molecules27041326

60. Guo Y, Michael N, Fonseca Madrigal J, et al. Protein hydrolysate from Pterygoplichthys disjunctivus, armoured catfish, with high antioxidant activity. Molecules. 2019; 24(8): 1628. doi: 10.3390/molecules24081628

61. Uzochukwu IE, Ossai NI, Aba PE, et al. Phytochemical profile and growth performance evaluation of African catfish (Clarias gariepinus) fed soursop (Annona muricata) leaf meal. Scientific African. 2025; 28: e02697. doi: 10.1016/j.sciaf.2025.e02697

62. Theodore AE, Raghavan S, Kristinsson HG. Antioxidative activity of protein hydrolysates prepared from alkaline-aided channel catfish protein isolates. Journal of Agricultural and Food Chemistry. 2008; 56(16): 7459-7466. doi: 10.1021/jf800185f

63. Yap JQ, Seflova J, Sweazey R, et al. FXYD proteins and sodium pump regulatory mechanisms. Journal of General Physiology. 2021; 153(4): e202012633. doi: 10.1085/jgp.202012633

64. Marx MTS, Souza CdF, Almeida APG, et al. Expression of ion transporters and Na+/K+-ATPase and H+-ATPase activities in the gills and kidney of silver catfish (Rhamdia quelen) exposed to different pHs. Fishes. 2022; 7(5): 261. doi: 10.3390/fishes7050261

65. Pirahanchi Y, Jessu R, Aeddula NR. Physiology, Sodium Potassium Pump. StatPearls; 2023.

66. Banerjee B, Chaudhury S. Thyroidal regulation of different isoforms of NaKATPase in the primary cultures of neurons derived from fetal rat brain. Life Sciences. 2002; 71(14): 1643-1654. doi: 10.1016/S0024-3205(02)01856-8

67. de Lima Santos H, Fortes Rigos C, Ciancaglini P. Kinetics behaviors of Na,K-ATPase: Comparison of solubilized and DPPC:DPPE-liposome reconstituted enzyme. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 2006; 142(3-4): 309-316. doi: 10.1016/j.cbpc.2005.11.003

68. Baldissera MD, Souza CF, Tavares GC, et al. Purinergic signaling and gene expression of purinoceptors in the head kidney of the silver catfish Rhamdia quelen experimentally infected by Flavobacterium columnare. Microbial Pathogenesis. 2020; 142: 104070. doi: 10.1016/j.micpath.2020.104070

69. Li S, Zhang T, Feng Y, et al. Extracellular ATP-mediated purinergic immune signaling in teleost fish: A review. Aquaculture. 2021; 537: 736511. doi: 10.1016/j.aquaculture.2021.736511

70. Baldissera MD, Souza CF, Viana AR, et al. Protective role of rutin dietary supplementation mediated by purinergic signaling in spleen of silver catfish Rhamdia quelen exposed to organophosphate pesticide trichlorfon. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 2021; 244: 109006. doi: 10.1016/j.cbpc.2021.109006

71. Rathbone MP, Middlemiss PJ, Gysbers JW, et al. Trophic effects of purines in neurons and glial cells. Progress in Neurobiology. 1999; 59(6): 663-690. doi: 10.1016/S0301-0082(99)00017-9

72. Ribeiro C, Petit V, Affolter M. Signaling systems, guided cell migration, and organogenesis: Insights from genetic studies in Drosophila. Developmental Biology. 2003; 260(1): 1-8. doi: 10.1016/S0012-1606(03)00211-2

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06/08/2025

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Surfactants involvement in the toxicity of glyphosate-based herbicides on the cerebral of African catfish (Clarias gariepinus). (2025). Progress in Environmental Chemistry, 1(1), 61. https://doi.org/10.65746/pec61