Assessment of adverse impacts of glyphosate-based herbicide, Excel Mera 71 by integrating multi-level biomarker responses in fishes

  • P. Samanta
  • S. Pal
  • A. K. Mukherjee
  • T. Senapati
  • J. Jung
  • A. R. GhoshEmail author
Original Paper


This work was aimed to investigate the adverse impacts of Excel Mera 71 on Anabas testudineus, Heteropneustes fossilis and Oreochromis niloticus under laboratory (17.2 mg/L) and field (750 g/acre) conditions based on multiple-level integrated biomarker responses. Haematological parameters were influenced significantly and showed species specificity after Excel Mera 71 exposure under both the conditions. Physiological indices (hepato-somatic index and condition factor) showed higher values; however, hepato-somatic index induced significantly under both the conditions (p < 0.05). Total nuclear abnormalities at molecular level revealed enhanced level. Responses were more adverse in laboratory (O. niloticus > H. fossilis > A. testudineus), while total nuclear abnormalities under field showed the order as: H. fossilis (0.49 ± 0.08) > A. testudineus (0.46 ± 0.10) > O. niloticus (0.27 ± 0.05). Moreover, multi-level integrated biomarker responses displayed responses as: O. niloticus (6.97 fold) > H. fossilis (4.01 fold) > A. testudineus (2.33 fold) in laboratory; however, under field condition, responses were totally different [A. testudineusH. fossilis (3.98 fold) > O. niloticus (3.01 fold)]. Additionally, glyphosate concentration was significantly correlated with several multi-level biomarker responses (p < 0.05). Moreover, multi-level integrated biomarker responses clearly indicated the higher impacts under laboratory experiment. Present investigation documented that multi-level integrative biomarker responses should be considered as reliable tool for assessment of herbicidal intoxication.


Excel Mera 71 Haematology Genotoxicity Total nuclear abnormalities Hepato-somatic index 



Authors are thankful to Department of Science & Technology, India (DST/INSPIRE Fellowship/2011/164), for financial support. Presently, Dr Samanta joined Incheon National University as researcher. Authors are grateful to reviewers for improving the paper.


  1. Abedi Z, Khalesi MK, Eskandari SK (2013) Biochemical and hematological profiles of common carp (Cyprinus carpio) under sublethal effects of trivalent chromium. Iran J Toxicol 7(20):782–792Google Scholar
  2. Akinwande AA, Moody FO, Sogbesan OA, Ugwumba AAA, Ovie SO (2004) Haematological response of Heterobranchus longifilis fed varying dietary protein levels. In: Proceedings of the 19th annual conference of the fisheries society of Nigeria. Ilorin, NigeriaGoogle Scholar
  3. APHA-AWWA-WPCF (2005) Standard methods for the examination of water and wastewater. Washington, DCGoogle Scholar
  4. Ariweriokuma SV, Akinrotimi OA, Gabriel UU (2011) Effects of cypermethrin on condition factor and organosomatic indices of Clarias gariepinus. J Agric Soc Res 11(2):67–72Google Scholar
  5. Bacchetta C, Cazenave J, Parma MJ (2011) Responses of biochemical markers in the fish Prochilodus lineatus exposed to a commercial formulation of endosulfan. Water Air Soil Pollut 216:39–49CrossRefGoogle Scholar
  6. Barcellos LJG, Kreutz LC, Souza CD, Rodrigues LB, Fioreze I, Quevedo RM, Cericato J, Soso AB, Fagundes M, Conrad J, Lacerd LDA, Terr S (2004) Hematological changes in jundia´ (Rhamdia quelen Quoy and Gaimard Pimelodidae) after acute and chronic stress caused by usual aquacultural management, with emphasis on immunosuppressive effects. Aquaculture 237:229–236CrossRefGoogle Scholar
  7. Barreto-Medeiros JM, Feitoza EG, Magalhães K, Da Silva RR, Manhães-de-Castro FM, Manhães-de-Castro R, De-Castro CMMB (2005) The expression of an intraspecific aggressive reaction in the face of a stressor agent alters the immune response in rats. Braz J Biol 65:203–209CrossRefGoogle Scholar
  8. Battaglin WA, Rice CK, Foazio MJ, Salmons S, Barry RX (2009) The occurrence of glyphosate, atrazine and other pesticides in vernal pools and adjacent streams in Washington DC, Maryland, Iowa and Wyoming 2005–2006. Environ Monit Assess 155:281–307CrossRefGoogle Scholar
  9. Braz-Mota S, Sadauskas-Henrique H, Duarte RM, Val AL, Almeida-Val VMF (2015) Roundup® exposure promotes gills and liver impairments, DNA damage and inhibition of brain cholinergic activity in the Amazon teleost fish Colossoma macropomum. Chemosphere 135:53–60CrossRefGoogle Scholar
  10. Broeg K, Lehtonen KK (2006) Indices for the assessment of environmental pollution of the Baltic Sea coasts: integrated assessment of a multi-biomarker approach. Mar Pollut Bull 53:508–522CrossRefGoogle Scholar
  11. Dey S, Samanta P, Pal S, Mukherjee AK, Kole D, Ghosh AR (2016) Integrative assessment of biomarker responses in teleostean fishes exposed to glyphosate-based herbicide (Excel Mera 71). Emerg Contam 2:191–203CrossRefGoogle Scholar
  12. Dhembare AJ (2014) Haematological alteration in European rabbit, Oryctolagus cuniculus (Linn.) exposed to ethereal. Adv Appl Sci Res 5(3):59–63Google Scholar
  13. EPA, Environmental Protection Agency (2010) EPA review of existing water standard, vol 75, p 59Google Scholar
  14. Esteves FA (1988) Fundamentos de Limnologia. Interciencia/FINEP, Rio de JaneiroGoogle Scholar
  15. Froese R (2006) Cube law, condition factor and weight–length relationships: history, meta-analysis and recommendations. J Appl Ichthyol 22:241–253CrossRefGoogle Scholar
  16. Fukuto TR (1990) Mechanismof action of organophosphorus and carbamate insecticides. Environ Health Perspect 87:245–254CrossRefGoogle Scholar
  17. Ghisi N, Cestari MM (2013) Genotoxic effects of the herbicide Roundup® in the fish Corydoras paleatus (Jenyns 1842) after short-term, environmentally low concentration exposure. Environ Monit Assess 185(4):3201–3207CrossRefGoogle Scholar
  18. Giesy JP, Dobson S, Solomon KR (2000) Ecotoxicological risk assessment for Roundup herbicide. Rev Environ Contam Toxicol 167:35–120Google Scholar
  19. Glusczak L, Miron DS, Crestani M, Fonseca MB, Pedron FA, Duarte MF, Vieira VLP (2006) Effect of glyphosate herbicide on acetylcholinesterase activity, metabolic and haematological parameters in piava (Leporinus obtusidens). Ecotoxicol Environ Saf 65:237–241CrossRefGoogle Scholar
  20. Hardig J, Hoglund LB (1983) Seasonal and ontogenetic effects on methaemoglobin and reduced glutathione content in the blood of reared Baltic salmon. Comp Biochem Physiol 75:27–34CrossRefGoogle Scholar
  21. Jan MR, Shah J, Muhammad M, Ara B (2009) Glyphosate herbicide residue determination in samples of environmental importance using spectrophotometric method. J Hazard Mater 169:742–745CrossRefGoogle Scholar
  22. Kim WK, Lee SK, Jung J (2010) Integrated assessment of biomarker responses in common carp (Cyprinus carpio) exposed to perfluorinated organic compounds. J Hazard Mater 180:395–400CrossRefGoogle Scholar
  23. Kim WK, Lee SK, Park JW, Choi K, Cargo J, Schlenk D, Jung J (2014) Integration of multi-level biomarker responses to cadmium and benzo[k]fluoranthene in the pale chub (Zacco platypus). Ecotoxicol Environ Saf 110:121–128CrossRefGoogle Scholar
  24. Kligerman D (1982) Fishes as biological detectors of the effect of genotoxic agents. In: Heddle J (ed) Mutagenicity: new horizons in genetic toxicology. Academic Press, New York, pp 87–93Google Scholar
  25. Kreutz LC, Barcellos LJG, Valle SDF, Silva TDO, Anziliero D, Santos EDD, Pivato M, Zanatta R (2011) Altered hematological and immunological parameters in silver catfish (Rhamdia quelen) following short term exposure to sublethal concentration of glyphosate. Fish Shellfish Immunol 30:51–57CrossRefGoogle Scholar
  26. Mazon AF, Monteiro EA, Pinheiro GH, Fernandes MN (2002) Hematological and physiological changes induced by short-term exposure to copper in the freshwater fish, Prochilodus scrofa. Braz J Biol 62:621–631CrossRefGoogle Scholar
  27. Memaster ME, Van Der Kraak HI, Portt GJ, Monkittrick CB, Sibley KR, Smith PK, Dixon DG (1991) Changes in hepatic mixed function oxygenase (MFO) activity, plasma steroid levels and age and maturity of a white sucker (Castostomes commersoni) population exposed to bio acute Kraft mill effluent. Aquat Toxicol 21:191–218Google Scholar
  28. Modesto KA, Martinez CBR (2010) Effects of Roundup Transorb on fish: hematology, antioxidant defences and acetylcholinesterase activity. Chemosphere 81(6):781–787CrossRefGoogle Scholar
  29. Nikinmaa M, Jensen FB (1988) Blood oxygen transport and acid-base status of stressed trout (Salmo gairdnerz): pre-and postbranchial values in winter fish. Comp Biochem Physiol 84A:391–396Google Scholar
  30. Oliveira M, Pacheco M, Santos MA (2011) Fish thyroidal and stress responses in contamination monitoring—an integrated biomarker approach. Ecotoxicol Environ Saf 74:1265–1270CrossRefGoogle Scholar
  31. Olsen T, Ellerbeck L, Fisher T, Callaghan A, Crane M (2001) Variability in acetylcholinesterase and glutathione S-transferase activities in Chironomus riparus meigen deployed in situ at uncontaminated field sites. Environ Toxicol Chem 20:1725–1732CrossRefGoogle Scholar
  32. Pandey K, Shukla JP (2005) A textbook of fish and fisheries. Rastogi Publications, MeerutGoogle Scholar
  33. Peruzzo PJ, Porta AA, Ronco AE (2008) Levels of glyphosate in surface waters, sediments and soils associated with direct sowing soybean cultivation in north pampasic region of Argentina. Environ Pollut 156(1):61–66CrossRefGoogle Scholar
  34. Pimpao CT, Zampronio AR, de Assis HC (2007) Effects of deltamethrin on hematological parameters and enzymatic activity in Ancistrus multispinis (Pisces, Teleostei). Pestic Biochem Physiol 88:122–127CrossRefGoogle Scholar
  35. Rand GM (1995) Fundamentals of aquatic toxicology: effects, environmental fate and risk assessment. Taylor & Francis, WashingtonGoogle Scholar
  36. Rodrigues BN, Almeida FLS (2005) Guia de herbicidas. Grafmark, LondrinaGoogle Scholar
  37. Ruppel ML, Brightwell BB, Schaefer J, Marvel JT (1977) Metabolism and degradation of glyphosate in soil and water. J Agric Food Chem 25:517–528CrossRefGoogle Scholar
  38. Russo C, Rocco L, Morescalchi MA, Stingo V (2004) Assessment of environmental stress by the micronucleus test and the comet assay on the genome of teleost populations from two natural environments. Ecotoxicol Environ Saf 57(2):168–174CrossRefGoogle Scholar
  39. Samanta P, Pal S, Mukherjee AK, Ghosh AR (2014) Evaluation of metabolic enzymes in response to Excel Mera 71, a glyphosate-based herbicide, and recovery pattern in freshwater teleostean fishes. BioMed Res Int. Google Scholar
  40. Samanta P, Pal S, Mukherjee AK, Ghosh AR (2016a) Histopathological and ultrastructural study on the effects of glyphosate-based herbicide, Excel Mera 71 on teleostean fish, Heteropneustes fossilis (Bloch). J Gastrointest Dig Syst 6:479. Google Scholar
  41. Samanta P, Pal S, Mukherjee AK, Senapati T, Ghosh AR (2016b) Histopathological and ultrastructural alterations in stomach and intestine of Oreochromis niloticus induced by glyphosate-based herbicide, Excel Mera 71. Austin J Environ Toxicol 2(2):1016Google Scholar
  42. Samanta P, Pal S, Mukherjee AK, Senapati T, Jung J, Ghosh AR (2017) Multi-level integrative biomarker responses in freshwater teleostean fishes exposed to Almix herbicide. Int J Environ Res 11(4):475–487CrossRefGoogle Scholar
  43. Savithri Y, Ravi Sekhar P, Jacob Doss P (2010) Changes in hematological profiles of albino rats under chlorpyrifos toxicity. Int J Pharm Biol Sci 1:1–7Google Scholar
  44. Schmitt CJ, Dethloff GM (2000) Biomonitoring of environmental status and trends (BEST) program: selected methods for monitoring chemical contaminants and their effects in aquatic ecosystems (No. USGS/BRD/ITR-2000-0005). Geological Survey Columbia MO Biological Resource DIVGoogle Scholar
  45. Sinha AK, Sinha MK, Adhikari S (2000) Effect of the copper toxicity on haematological profile of Indian major corp, Lobeo rohita. Hand Book Ind Environ Pollut 166–172Google Scholar
  46. Suvetha L, Saravanan M, Hur JH, Ramesh M, Clara Bindu F (2015) Responses of the Indian major carp Labeo rohita to deltamethrin at acute and sublethal concentrations. Toxicol Environ Chem. Google Scholar
  47. Us EPA (1993) EPA reregistration eligibility decision (RED) facts glyphosate (EPA-738-F-93-011). United States Environmental Protection Agency, WashingtonGoogle Scholar
  48. van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149CrossRefGoogle Scholar

Copyright information

© Islamic Azad University (IAU) 2018

Authors and Affiliations

  • P. Samanta
    • 1
    • 2
    • 3
  • S. Pal
    • 4
  • A. K. Mukherjee
    • 5
  • T. Senapati
    • 1
  • J. Jung
    • 2
  • A. R. Ghosh
    • 1
    Email author
  1. 1.Department of Environmental ScienceThe University of BurdwanBardhamanIndia
  2. 2.Division of Environmental Science and Ecological EngineeringKorea UniversitySeoulRepublic of Korea
  3. 3.Department of Marine ScienceIncheon National UniversityIncheonRepublic of Korea
  4. 4.Department of Environmental ScienceAghorekamini Prakashchandra MahavidyalayaBengaiIndia
  5. 5.P.G. Department of Conservation BiologyDurgapur Govt. CollegeDurgapurIndia

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