Skip to main content
Log in

Effect of glyphosate-based herbicide on hematological and hemopoietic parameters in common carp (Cyprinus carpio L)

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

The effects of Roundup (glyphosate-based herbicide) on peripheral blood parameters and hematopoietic tissue cellular composition and activity in common carp juveniles were evaluated. The fish were exposed for 7 days at 0.0, 0.1, 0.5, or 5.0 mg/L of glyphosate. In fish exposed to Roundup, hematological alterations were observed; however, most of them were not directly related to the herbicide concentration. An increase in Ht and MCV, and decrease in Hb, MCH, and MCHC compared to the control were observed. Fish exposed to Roundup showed also a reduction in WBC and oxidative metabolic activity of phagocytes (NBT) compared to the control. The fish exposed to 0.1 and 5.0 mg/L showed increased glucose values, whereas in those subjected to 0.5 mg/L blood glucose concentration declined compared to the control. Cholesterol significantly increased at 0.1 mg/L and decreased at 5.0 mg/L. Analysis of head kidney hematopoietic tissue revealed that Roundup at concentrations 0.5 and 5.0 mg/L caused a significant increase in the rate of cell proliferation accompanied by an increase in frequency of early blast cells. No significant differences occurred in percentages of most cell lineages but the frequency of monocytoid, eosinophilic, and basophilic lineage cells significantly increased in the herbicide-exposed fish compared to the control. The obtained results revealed that sublethal concentrations of Roundup that may occur in polluted natural waters caused a slight anemic and significant immunosuppressive response in common carp juveniles. On the other hand, they indicate a considerable compensatory potential of carp hematopoietic system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anton FA, Labora E, De Ariz M (1994) Acute toxicity of the herbicide glyphosate to fish. Chemosphere 82:745–753

    Article  Google Scholar 

  • Ayoola SO (2008) Histopathological effects of glyphosate on juvenile African catfish (Clarias gariepinus). JAES 4:362–367

    Article  Google Scholar 

  • Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integ Comp Biol 42:517–525

    Article  CAS  Google Scholar 

  • Benachour N, Séralini GE (1997) Glyphosate formulations induce apoptosis and necrosis in human umbilical, embryonic, and placental cells. Chem Res Toxicol 22:97–105

    Article  CAS  Google Scholar 

  • Binukumari S, Vasanthi J (2013) The toxic effect of pesticide dimethoate 30% EC on the protein metabolism of the fresh water fish, Labeorohita. IJCMAS 2:79

    Google Scholar 

  • Brausch JM, Smith PN (2007) Toxicity of three polyethoxylated tallowamine surfactant formulations to laboratory and field collected fairy shrimp, Thamnocephalus platyurus. Arch Environ Contam Toxicol 52:217–221

    Article  PubMed  CAS  Google Scholar 

  • Cavas T, Konen 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

    Article  PubMed  CAS  Google Scholar 

  • Fijan N (2002a) Morphogenesis of blood cell lineages in channel catfish. J Fish Biol 60:999–1014

    Article  Google Scholar 

  • Fijan N (2002b) Composition of main haematopoietic compartments in normal and bled channel catfish. J Fish Biol 60:1142–1154

    Article  Google Scholar 

  • Folmar LC, Sander HO, Julin AM (1979) Toxicity of the herbicide glyphosate and several of its formulations to fish and aquatic invertebrate. Arch Environ Contam Toxicol 8:269–278

    Article  PubMed  CAS  Google Scholar 

  • Franz JE, Mao MK, Sikorski JA (1997) Glyphosate: a unique global herbicide. ACS 4:65–97

    Google Scholar 

  • Gholami-Seyedkolaei SJ, Mirvaghefi A, Farahmand H, Kosari AA (2013) Effect ofaglyphosate-based herbicidein Cyprinus carpio: assessment of acetylcholinesterase activity, hematological responses and serum biochemical parameters. Ecotox Environ Safe 98:135–141

    Article  CAS  Google Scholar 

  • Giesy JP, Dobson S, Solomon KR (2000) Ecotoxicological risk assessment for Roundup herbicide. Rev Environ Contam Toxicol 167:35–120

    CAS  Google Scholar 

  • Gimsing AL, Borggaard OK, Jacobsen OS, Aamand J, Sorensen J (2004) Chemical and microbiological soil characteristics controlling glyphosate mineralization in Danish surface soils. Appl Soil Ecol 27:233–242

    Article  Google Scholar 

  • Glusczak L, Miron DS, Crestani M, Fonseca MB, Pedron FA, Duarte MF, Vieira VLP (2006) Effect of glyphosate herbicide on acetylcholinesterase activity and metabolic and hematological parameters in piava (Leporinus obtusidens). Ecotox Environ Safe 65:237–241

    Article  CAS  Google Scholar 

  • Glusczak L, Loro VL, Pretto A, Moreas BS, Raabe A, Duarte MF, da Fonseca MB, de Menezes CC, Valladão DM (2011) Acute exposure to glyphosate herbicide affects oxidative parameters in piava (Leporinus obtusidens). Arch Environ Contam Toxicol 61:624–630

    Article  PubMed  CAS  Google Scholar 

  • Guilherme S, Santos MA, Barroso C, Gaivão I, Pacheco M (2010) Differential genotoxicity of Roundup® formulation and its constituents in blood cells of fish (Anguilla anguilla): considerations on chemical interactions and DNA damaging mechanisms. Ecotoxycology 21:1381–1390

    Article  CAS  Google Scholar 

  • Henderson M, Gervais JA, Luukinen B, Buhl K, Stone D (2010) Glyphosate technical fact sheet. National pesticide information center). Oregon State University Extension Services. Available: <http://npic.orst.edu/factsheets/glyphotech.html/> Updated on September 2010

  • Hildebrand LD, Sullivan DS, Sullivan TP (1982) Experimental studies of rainbow trout populations exposed to field applications of Roundup herbicide. Arch Environ Contam Toxicol 11:93–98

    Article  PubMed  CAS  Google Scholar 

  • Jiraungkoorskul W, Upatham ES, Kruatrachue M, Sahaphong S, Vichasri-Grams S, Pokethitiyook P (2002) Histopathological effects of Roundup, a glyphosate herbicide, on Nile tilapia (Oreochromis niloticus). Sci Asia 28:121–127

    Article  CAS  Google Scholar 

  • Kavitha C, Malarvizhi A, Kumaran SS, Ramesh M (2010) Toxicological effects of arsenate exposure on hematological, biochemical and liver transaminases activity in an Indian major carp, Catla catla. Food Chem Toxicol 48:2848–2854

    Article  PubMed  CAS  Google Scholar 

  • Khan A, Shah N, Gul A, Us-Sahar N, Ismail A, Aziz MF, Farooq M, Adnan M, Rizwan M (2016) Comparative study of toxicological impinge of glyphosate and atrazine (Herbicide) on stress biomarkers: blood biochemical and hematological parameters of the freshwater Common Carp (Cyprinus carpio). Pol J Environ Stud 25:1995–2001. https://doi.org/10.15244/pjoes/62698

    Article  CAS  Google Scholar 

  • Kondera E, Witeska M (2013) Cadmium and copper reduce hematopoietic potential in common carp (Cyprinus carpio L.) head kidney. Fish Physiol Biochem 39:755–764. https://doi.org/10.1007/s10695-012-9738-6

    Article  PubMed  CAS  Google Scholar 

  • Kondera E (2011) Haematopoiesis in the head kidney of common carp (Cyprinus carpio L): a morphological study. Fish Physiol Biochem 37:355–362

    Article  PubMed  CAS  Google Scholar 

  • Kotsanis N, Iliopoulou-Georgudaki J, Kapata-Zoumbos K (2000) Changesin selected hematological parameters at early stages of the rainbow trout, Oncorhynchus mykiss, subjected to metal toxicants: arsenic, cadmium and mercury. J Appl Ichthyol 16:276–278

    Article  CAS  Google Scholar 

  • Kreutz LC, Barcellos LJG, Marteninghe A, dos Santos ED, Zanatta R (2010) Exposure to sublethal concentration of glyphosate or atrazine-based herbicides alters the phagocytic function and increases the susceptibility of silver cat fish fingerlings (Rhamdia quelen) to Aeromonas hydrophila challenge. Fish Shellfish Immunol 29:694–697

    Article  PubMed  CAS  Google Scholar 

  • Kreutz LC, Barcellos LJG, de Faria Valle S, de Oliveira Silva T, Anziliero D, dos Santos ED, 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 30:51–57

    Article  PubMed  CAS  Google Scholar 

  • Langiano VC, Martinez CBR (2008) Toxicity and effects of a glyphosate-based herbicide on the Neotropical fish Prochilodus lineatus. CBP 147:222–231

    Google Scholar 

  • LeÁvesque A, Rahe JE (1992) Herbicide interactions with fungal root pathogens, with special reference to glyphosate. Annu Rev Phytopathol 30:579–602

    Article  Google Scholar 

  • Mallory-Smith CA, Ratzinger EJ Jr (2003) Revised classification of herbicides by sites of action for weed resistance management strategies. Weed Technol 17:605–619

    Article  CAS  Google Scholar 

  • Modesto KA, Martinez CBR (2010) Effects of Roundup Transorb on fish: hematology, antioxidant defenses and acetylcholinesterase activity. Chemosphere 81:781–787

    Article  PubMed  CAS  Google Scholar 

  • Neskovic NK, Poleksic V, Elezovic I, Karan V, Budimir M (1996) Biochemical and histopathological effects of glyphosate on carp, Cyprinus carpio L. Bull Environ Contam Toxicol 56:295–302

    Article  PubMed  CAS  Google Scholar 

  • Okomoda VT, Ataguba GA, Ayuba VO (2013) Hematological response of Clarias gariepinus fingerlings exposed to acute concentrations of Sunsate®. J Stress Physiol Biochem 9:271–278

    Google Scholar 

  • Olurin KB, Olojo EAA, Mbaka GO, Akindele AT (2006) Histopathological responses of the gill and liver tissues of Clarias gariepinus fingerlings to the herbicide, glyphosate. Afr J Biotechnol 5:2480–2487

    CAS  Google Scholar 

  • Orun I, Dogru MI, Erdogan K, Dogru A, Yuksel E, Talas ZS (2013) Effects of acute and chronic exposure to glyphosate on common carp (Cyprinus carpio L.) hematological parameters: the beneficial effect of propolis. Fresenius Environ Bull 22:2504–2509

    CAS  Google Scholar 

  • Relyea RA (2006) The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities: response. Ecol Appl 16:2027–2034

    Article  Google Scholar 

  • Salbego J, Pretto A, Gioda CR, Cavalheiro de Menezes C, Lazzari R, Neto JR, Baldisserotto B, Loro VL (2010) Herbicide formulation with glyphosate affects growth, acetylcholinesterase activity, and metabolic and hematological parameters in piava (Leporinus obtusidens). Arch Environ Contam Toxicol 58:740–745. https://doi.org/10.1007/s00244-009-9464-y

    Article  PubMed  CAS  Google Scholar 

  • Schuette AJ (1998) Environmental fate of glyphosate, in: Environmental Monitoring & Pest Management, Department of Pesticide Regulation, Sacramento, CA9 5824-5624, Available: http://www.cdpr.ca.gov/docs/emon/pubs/fatememo/glyphos.pdf/ Updated on November 1998

  • Sopińska A, Grochoła A, Niezgoda J (2000) Influence of water polluted with herbicide Roundap on the organism of fish. Med Wet 56:593–597 [In Polish]

    Google Scholar 

  • Stoyanova S, Yancheva V, Iliev I, Vasileva T, Bivolarski V, Velcheva I, Georgieva E (2015) Glyphosate induces morphological and enzymatic changes in common carp (CyprinuscarpioL.) liver. Bulg J Agric Sci 21:409

    Google Scholar 

  • Studnicka M, Siwicki AK, Ryka B (1985) Phagocytic ability of neutrophils in carp (Cyprinus carpio L.) Isr J Aquacult Bamidgeh 37:123–128

    Google Scholar 

  • Svobodova Z, Groch L, Flajshans M, Vykusova B, Machova J (1997) The effect of long-term therapeutic bath of malachite green on common carp Cyprinus carpio L. Acta Vet Brno 66:111–117

    Article  CAS  Google Scholar 

  • Svobodova Z, Pravda D, Palackova J (1991) Unified methods of haematological examination of fish VURH Vodnany, 31

  • Svobodova Z, Vykusova B, Machova J (1994) The effects of pollutants on selected haematological and biochemical parameters in fish. In: Müller,R, Lloyd,R (Eds.), Sublethal and chronic effects of pollutants on fresh water fish. FAO Fishing NewsBooks, Great Britain, pp. 39–52

  • Szarek J, Siwicki A, Andrzejewska A, Terech-Majewska E, Banaszkiewicz T (2000) Effects of the herbicide Roundups on the ultrastructural pattern of hepatocytes in carp (Cyprinus carpio). Mar Environ Res 50:263–266

    Article  PubMed  CAS  Google Scholar 

  • Tu MC, Hurd R, Robison J, Randall M (2001) Glyphosate weed control methods handbook, The Nature Conservancy, pp. 7e1–7e10, Available: http://www.invasive.org/gist/products/handbook/14Glyphosate.pdf/>. Updates on November 2001

  • U.S. EPA. Pesticides Industry Sales and usage: 2006 and 2007 market estimates; U.S. Environmental Protection Agency: Washington, DC, 2011

  • Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was financed from the science grant 387/14/S granted by the Ministry of Science and Higher Education.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. Kondera.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kondera, E., Teodorczuk, B., Ługowska, K. et al. Effect of glyphosate-based herbicide on hematological and hemopoietic parameters in common carp (Cyprinus carpio L). Fish Physiol Biochem 44, 1011–1018 (2018). https://doi.org/10.1007/s10695-018-0489-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-018-0489-x

Keywords

Navigation