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Effect of glyphosate-based herbicide roundup on hemato-biochemistry of Labeo rohita (Hamilton, 1822) and susceptibility to Aeromonas hydrophila infection

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Abstract

In the present study, comprehensive research was executed to investigate the salient toxic effects of glyphosate herbicide in static water system by evaluating the haemato-biochemical profiles of Labio rohita. A challenge study against Aeromonas hydrophila was conducted to determine disease susceptibility of the fish, treated to varying concentrations of commercial-grade glyphosate herbicide. A static range finding bioassay and definitive test revealed that the 96-h LC50 value of glyphosate was 10.16 mg L−1. The experimental fish were subjected to three sub-lethal concentrations of 2.06, 1.03, and 0.63 mg l−1 for 28 days and changes were documented bi-fortnightly to study haemato-biochemical alterationsin the fish. Significantly (p < 0.05) low values in red blood corpuscles (RBC), hemoglobin (Hb), and hematocrit value (Hct) were documented. In contrast, a significant (p < 0.05) escalation in white blood corpuscles (WBC) was documented in comparison to the control. Biochemical and stress markers such as blood glucose, total protein, and alkaline phosphatase (ALP) were significantly (p < 0.05) low, whereas serum glutamate pyruvate transaminase (SGPT) and serum glutamate oxaloacetate transaminase (SGOT) escalated significantly (p < 0.05). Chronic exposure to glyphosate, on the other hand, had the least effect on the Na+ and K+ ions. Further, a challenge assay against A. hydrophila at three sub-lethal glyphosate concentrations demonstrated a synergistic impact that reduced the fish survivability. The findings conclude that persistent low glyphosate concentrations in aquatic ecosystems show significant pathophysiological changes in L. rohita, with increased vulnerability to infections. Altogether, our findings indicate the need to further study the possible assessment for a sustainable bio-remediation technique, mitigation of the detrimental effects of glyphosate exposure in fish, and recommendation of an acceptable residue concentration of the glyphosate in aquatic ecosystem.

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References

  • Adhikari S, Sarkar B, Chatterjee A, Mahapatra CT, Ayyappan S (2004) Effects of cypermethrin and carbofuran on certain haematological parameters and prediction of their recovery in a freshwater teleost, Labeorohita (Hamilton). Ecotoxicol Environ Saf 58:220–226. https://doi.org/10.1016/j.ecoenv.2003.12.003

    Article  CAS  Google Scholar 

  • Agrahari S, Pandey KC, Gopal K (2007) Biochemical alteration induced by monocrotophos in the blood plasma of fish, Channa punctatus (Bloch). Pesticbiochemphys 88(3):268–272. https://doi.org/10.1016/j.pestbp.2007.01.001

    Article  CAS  Google Scholar 

  • Ajani EK, Akpoilih BU (2010) Effect of chronic dietary copper exposure on haematology and histology of common carp (Cyprinus carpioL.). J Appl Sci Environ Manage 14(4):39–45

    Google Scholar 

  • Ajima MNO, Pandey PK, Kumar K, Poojary N (2018) Alteration in DNA structure, molecular responses and Na+ -K+ -ATPase activities in the gill of Nile tilapia, Oreochromis niloticus (Linnaeus, 1758) in response to sub-lethal verapamil. Ecotoxicol Environ Saf 147:809–816. https://doi.org/10.1016/j.ecoenv.2017.09.050

    Article  CAS  Google Scholar 

  • Albinati ACL, Moreira ELT, Albinati RCB, de Carvalho JV, Santos GB, de Lira AD (2007) Toxic idadeaguda do herbicida roundup® parapiauçu (“Leporinus macrocephalus”). Rev Bras Saúde Prod Anim 8(3)

  • Al-Harbi MS, El-Rahman FA, El-Shenawy NS, Al-Mutrafi WM (2014) The beneficial effects of ascorbic acid during chlorpyrifos-induced oxidative stress and histo pathological changes in Oreochromis spilurus. Toxicol Environ Health Sci 6:203–216

    Article  Google Scholar 

  • Aljerf L (2018) High-efficiency extraction of bromocresol purple dye and heavy metals as chromium from industrial effluent by adsorption onto a modified surface of zeolite: kinetics and equilibrium study. J Environ Manage 225:120–132. https://doi.org/10.1016/j.jenvman.2018.07.048

    Article  CAS  Google Scholar 

  • Amarante Junior OPD, Santos TCRD, Brito NM, Ribeiro ML (2002) Glifosato: propriedades, toxicidade, usos e legislação. Quimica Nova 25:589–593. https://doi.org/10.1590/S0100-40422002000400014

    Article  Google Scholar 

  • Annett R, Habibi HR, Hontela A (2014) Impact of glyphosate and glyphosate-based herbicides on the freshwater environment. J Appl Toxicol 34(5):458–479. https://doi.org/10.1002/jat.2997

    Article  CAS  Google Scholar 

  • Aranha ML, Garcia MS, de Carvalho Cavalcante DN, Silva AP, Fontes MK, Gusso-Choueri PK, Choueri RB, Perobelli JE (2021) Biochemical and histopathological responses in peripubertal male rats exposed to agrochemicals isolated or in combination: a multivariate data analysis study. Toxicol 447:152636

    Article  CAS  Google Scholar 

  • Authority EFS (2015) Conclusion on the peer review of the pesticide risk assessment of the active substance glyphosate. EFSA J 13:4302

    Google Scholar 

  • Ayoola SO (2008) Toxicity of herbicide, glyphosate on Nile tilapia (Oreochromis niloticus) juvenile. Afr J Agric Res 3(12):825–834

    Google Scholar 

  • Bacchetta C, Rossi A, Ale A, Campana M, Parma MJ, Cazenave J (2014) Combined toxicological effects of pesticides: a fish multi-biomarker approach. EcolIndicat 36:532–538. https://doi.org/10.1016/j.ecolind.2013.09.016

    Article  CAS  Google Scholar 

  • Banaee M, Mirvaghefi AR, Sureda A, Rafei GR, Ahmadi K (2012) Effect of sub-Lethal concentrations of diazinon on blood parameters and liver histopathology of rainbow trout (Oncorhynchus mykiss). Ir J Nat Res (J Nat Environ) 65(3):297–313. https://doi.org/10.1016/j.pestbp.2010.09.001

    Article  CAS  Google Scholar 

  • Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroid. Integr Comp Biol 42(3):517–525. https://doi.org/10.1093/icb/42.3.517

    Article  CAS  Google Scholar 

  • Bhagwant S, Bhikajee M (2000) Induction of hypochromic macrocytic anaemia in Oreochromis hybrid (Cichlidae) exposed to 100mg/L sub-lethal dose of aluminium. J Sci Technol 5–2000

  • Buikema AL Jr, Niederlehner BR, Cairns J Jr (1982) Biological monitoring part IV—toxicity testing. Water Resour 16(3):239–262. https://doi.org/10.1016/0043-1354(82)90188-9

    Article  CAS  Google Scholar 

  • Carvalho CS, Fernandes MN (2006) Effect of temperature on copper toxicity and hematological responses in the neotropical fish Prochilodus scrofa at low and high pH. Aquaculture 251(1):109–117. https://doi.org/10.1016/j.aquaculture.2005.05.018

    Article  CAS  Google Scholar 

  • Cattaneo R, Clasen B, Loro VL, de Menezes CC, Pretto A, Baldisserotto B, Santi A, de Avila LA (2011) Toxicological responses of Cyprinus carpio exposed to a commercial formulation containing glyphosate. Bull Environ Contam Toxicol 87(6):597–602. https://doi.org/10.1007/s00128-011-0396-7

    Article  CAS  Google Scholar 

  • Cattani D, de LO Cavalli VL, Rieg CEH, Domingues JT, Dal-Cim T, Tasca CI, Silva FRMB, Zamoner A (2014) Mechanisms underlying the neurotoxicity induced by glyphosate-based herbicide in immature rat hippocampus: involvement of glutamate excitotoxicity. Toxicology 320:34–45. https://doi.org/10.1016/j.tox.2014.03.001

    Article  CAS  Google Scholar 

  • Costa RN, Nomura F (2016) Measuring the impacts of Roundup Original® on fluctuating asymmetry and mortality in a Neotropical tadpole. Hydrobiologia 765(1):85–96. https://doi.org/10.1007/s10750-015-2404-0

    Article  Google Scholar 

  • Dacie JV, Lewis SM (2001) Practical haematology, 9th edn. Churchill Livingstone, London, pp 633

  • Das BK, Mukherjee SC (2003) Toxicity of cypermethrin in Labeorohita fingerlings: biochemical, enzymatic and haematoogical consequences. Comp Biochem Physiol Part C: Regul Toxicol Pharmacol 134:109–121. https://doi.org/10.1016/S1532-0456(02)00219-3

    Article  Google Scholar 

  • de Moura FR, Brentegani KR, Gemelli A, Sinhorin AP, Sinhorin VDG (2017) Oxidative stress in the hybrid fish jundiara (Leiarius marmoratus × Pseudoplatysto mareticulatum) exposed to Roundup Original®. Chemosphere 185:445–451. https://doi.org/10.1016/j.chemosphere.2017.07.030

    Article  CAS  Google Scholar 

  • de Oliveira JL, Campos EVR, Bakshi M, Abhilash PC, Fraceto LF (2014) Application of nanotechnology for the encapsulation of botanical insecticides for sustainable agriculture: prospects and promises. Biotechnol Adv 32(8):1550–1561. https://doi.org/10.1016/j.biotechadv.2014.10.010

    Article  CAS  Google Scholar 

  • Do CarmoLangiano V, Martinez CB (2008) Toxicity and effects of a glyphosate-based herbicide on the neotropical fish Prochilodus lineatus. Comp Biochem Physiol Part C: Toxicol Appl Pharmacol 147(2):222–231. https://doi.org/10.1016/j.cbpc.2007.09.009

    Article  CAS  Google Scholar 

  • Doumas BT, Watson WA, Biggs HG (1971) Albumin standards and the measurement of serum albumin with bromcresol green. ClinicaChimicaacta 31(1):87–96

    CAS  Google Scholar 

  • El-Murr AE, Imam TS, Hakim Y, Ghonimi WA (2015) Histopathological, immunological, hematological and biochemical effects of fipronil on Niletilapia (Oreochromis niloticus). J Vet Sci Technol 6(5):2–9. https://doi.org/10.4172/2157-7579.1000252

    Article  CAS  Google Scholar 

  • EPA US (1993) Registration eligibility decision (RED) glyphosate. EPA-738-R-93–014.Washington, DC: US Environmental protection agency, office of prevention, pesticides and toxic substances (7s0ew)

  • Faheem M, Zainab Z, Ferreira NGC (2021) Toxicity assessment of dibutyl phthalate in grass Carp: an integrated biomarker approach. Pak Vet J 41:365–371. https://doi.org/10.29261/pakvetj/2021.031

    Article  CAS  Google Scholar 

  • Fazio F (2019) Fish hematology analysis as an important tool of aquaculture: a review. Aquaculture 500:237–242. https://doi.org/10.1016/j.aquaculture.2018.10.030

    Article  Google Scholar 

  • Fennell CW, Lindsey KL, McGaw LJ, Sparg SG, Stafford GI, Elgorashi EE, Grace OM, Van Staden J (2004) Assessing African medicinal plants for efficacy and safety: pharmacological screening and toxicology. J Ethnopharmacol 94(2–3):205–217

    Article  CAS  Google Scholar 

  • Gallegos CE, Baier CJ, Bartos M, Bras C, Domínguez S, Mónaco N, Gumilar F, Giménez MS, Minetti A (2018) Perinatal glyphosate-based herbicide exposure in rats alters brain antioxidant status, glutamate and acetylcholine metabolism and affects recognition memory. Neurotox Res 34:363–374. https://doi.org/10.1007/s12640-018-9894-2

    Article  CAS  Google Scholar 

  • Ghaffar A, Hussain R, Khan A, Abbas RZ, Asad M (2015a) Butachlor induced clinic-hematological and cellular changes in fresh water fish Labeo rohita (Rohu). Pak Vet J 35(2):201–6

    Google Scholar 

  • Ghaffar A, Rani K, Hussain R, Mehreen M, Rubi T, Yasin S (2015b) Histopathological and serum biochemical changes induced by sub-chronic doses of Triazophos in Quail. Pak Vet J 35(1):13–17

    CAS  Google Scholar 

  • Ghaffar A, Hussain R, Ahmad N, Ghafoor R, Akram MW, Khan I, Khan A (2021) Evaluation of hemato-biochemical, antioxidant enzymes as biochemical biomarkers and genotoxic potential of glyphosate in freshwater fish (Labeo rohita). Chem Ecol 37(7):646–67. https://doi.org/10.1080/02757540.2021.1937141

    Article  CAS  Google Scholar 

  • Gholami-Seyedkolaei SJ, Mirvaghefi A, Farahmand H, Kosari AA (2013) Effect of aglyphosate-based herbicidein Cyprinus carpio: assessment of acetylcholinesterase activity, hematological responses and serum biochemical parameters. Ecotox Environ Safe 98:135–141. https://doi.org/10.1016/j.ecoenv.2013.09.011

    Article  CAS  Google Scholar 

  • Gibem TT, Balogun JK, Lawal FA, Anunne PA (2003) Trace metal accumulation in Clariasgariepinu (Teugels) exposed to sub-lethal levels of tannery effluent. Sci Total Environ 2:71–79. https://doi.org/10.1016/s0048-9697(00)00773-7

    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 (Leporinusobtusidens). Ecotoxicol Environ Saf 65:237–241. https://doi.org/10.1016/j.ecoenv.2005.07.017

    Article  CAS  Google Scholar 

  • Gul ST, Khan A, Farooq M, Niaz S, Ahmad M, Khatoon A, Hussain R, Saleemi MK, Hassan MF (2017) Effect of sub lethal doses of thiamethoxam (a pesticide) on hemato-biochemical values in cockerels. Pak Vet J 37(2):135–8

    CAS  Google Scholar 

  • Hong Y, Yang X, Yan G, Huang Y, Zuo F, Shen Y, Ding Y, Cheng Y (2017a) Effects of glyphosate on immune responses and haemocyte DNA damage of Chinese mitten crab Eriocheir sinensis. Fish Shellfish Immunol 7:119–127. https://doi.org/10.1016/j.fsi.2017.09.062

    Article  CAS  Google Scholar 

  • Hong Y, Yang X, Yan G, Huang Y, Zuo F, Shen Y, Ding Y, Cheng Y (2017b) Effects of glyphosate on immune responses and haemocyte DNA damage of Chinese mitten crab, Eriocheir sinensis. Fish Shellfish Immunol 71:19–27. https://doi.org/10.1016/j.fsi.2017.09.062

    Article  CAS  Google Scholar 

  • Hossain S, Khatun MH, Rahman MK, Shahjahan M (2015) Impacts of Sumithion on blood glucose and some hematological parameters in common carp. Int J Environ 5:8–13

    Google Scholar 

  • Hussain R, Mahmood F, Khan A (2015) Genotoxic and pathological effects of malathion in male Japanese quail (Coturnix japonica). Pak J Agri Sci 52:1143–1149

    Google Scholar 

  • Hussain R, Ali F, Rafique A, Ghaffar A, Jabeen G, Rafay M, Liaqat S, Khan I, Malik R, Khan MK, Niaz M (2019) Exposure to sub-acute concentrations of glyphosate induces clinico-hematological, serum biochemical and genotoxic damage in adult cockerels. Pak Vet J 39:181–6. https://doi.org/10.29261/pakvetj/2019.064

    Article  CAS  Google Scholar 

  • Hussein SY, El-Nasser MA, Ahmed SM (1996) Comparative studies on the effects of herbicide atrazine on freshwater fish Oreochromis niloticus and Chrysichthyes auratus at Assiut, Egypt. Bull Environ ContamToxicol 57(3):503–510. https://doi.org/10.1007/s001289900218

    Article  CAS  Google Scholar 

  • Inyang IR, Izah SC (2016) Effect of glyphosate on some enzymes and electrolytes in Heterobranchusbidosalis (a common African catfish). Biotechnol Res Int 2(4):161–165

    Google Scholar 

  • Inyang IR, Ekweozor IKE, Ollor A (2014) Physiological effects of diazinon on Clariasgariepinus. Best J 11:171–176

    Google Scholar 

  • Jabeen G, Manzoor F, Arshad M, Barbol B (2021) Effect of cadmium exposure on hematological, nuclear and morphological alterations in erythrocyte of fresh water fish (Labeo rohita). Cont Vet J 1(1):20–4

    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). SciAsia 28(3):121–7. https://doi.org/10.2306/scienceasia1513-1874.2002.28.121

    Article  CAS  Google Scholar 

  • Joshi PK, Bose M, Harish D (2002) Changes in certain haematological parameters in a siluroid catfish, Clariasbatrachus exposed to cadmium chloride. J Pollut Res 21(2):129–131

    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, Catlacatla. Food Chem Toxicol 48:2848–2854. https://doi.org/10.1016/j.fct.2010.07.017

    Article  CAS  Google Scholar 

  • Kelly DW, Poulin R, Tompkins DM, Townsend CR (2010a) Synergistic effects of glyphosate formulation and parasite infection on fish malformations and survival. J Appl Ecol 47(2):498–504. https://doi.org/10.1111/j.1365-2664.2010.01791.x

    Article  CAS  Google Scholar 

  • Kelly DW, Poulin R, Tompkins DM, Townsend CR (2010b) Synergistic effects of glyphosate formulation and parasite infection on fish malformations and survival. J Appl Ecol 47:498–504. https://doi.org/10.1111/j.1365-2664.2010.01791.x

    Article  CAS  Google Scholar 

  • Khalil F, Emeash H (2018) Behavior and stereotypies of Nile tilapia (Oreochromis niloticus) in response to experimental infection with Aeromonas hydrophila. Aquat Sci Eng 33(4):124–130. https://doi.org/10.26650/ASE2018407191

    Article  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, Teodorczuk B, Ługowska K, Witeska M (2018) Effect of glyphosate-based herbicide on hematological and hemopoietic parameters in common carp (Cyprinus carpio L). Fish PhysiolBiochem 44(3):1011–1018. https://doi.org/10.1007/s10695-018-0489-x

    Article  CAS  Google Scholar 

  • Kothari SC, Shivarudraiah P, Venkataramaiah SB, Gavara S, Soni MG (2012) Subchronic toxicity and mutagenicity/genotoxicity studies of Irvingia gabonensis extract (IGOB131). Food Chem Toxicol 50(5):1468–1479

    Article  CAS  Google Scholar 

  • Kotsanis N, Iliopoulou-Georgudaki J, Kapata-Zoumbos K (2000) Changes in 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. https://doi.org/10.1046/j.1439-0426.2000.00163.x

    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 catfish fingerlings (Rhamdiaquelen) to Aeromonas hydrophila challenge. Fish Shellfish Immunol 29(4):694–697. https://doi.org/10.1016/j.fsi.2010.06.003

    Article  CAS  Google Scholar 

  • Lajmanovich RC, Sandoval MT, Peltzer PM (2003) Induction of mortality and malformation in Scinaxnasicus tadpoles exposed to glyphosate formulations. Bull Environ Contam Toxicol 70(3):612–618. https://doi.org/10.1007/s00128-003-0029-x

    Article  CAS  Google Scholar 

  • Mahmood Y, Ghaffar A, Hussain R (2021) New insights into hemato-biochemical and histopathological effects of Acetochlor in bighead carp (Aristichthys nobilis). Pak Vet J 41(4):538–544. https://doi.org/10.29261/pakvetj/2021.072

    Article  CAS  Google Scholar 

  • Mahmood Y, Hussain R, Ghaffar A, Ali F, Nawaz S, Mehmood K, Khan A (2022) Acetochlor affects bighead carp (Aristichthys nobilis) by producing oxidative stress, lowering tissue proteins, and inducing genotoxicity. Biomed Res Int. https://doi.org/10.1155/2022/9140060

  • Mahmoud AH, Noura M, Darwish NM, Kim YO, Viayaraghavan P, Kwon JT, Na SW, Lee JC, Kim HJ (2020) Fenvalerate induced toxicity in Zebra fish, Danio rerio and analysis of biochemical changes and insights of digestive enzymes as important markers in risk assessment. J King Saud Uni-Sci 32:1569–80 https://scholarworks.bwise.kr/sch/handle/2021.sw.sch/3050

  • Martínez MA, Ares I, Rodríguez JL, Martínez M, Martínez-Larrañaga MR, Anadón A (2018) Neurotransmitter changes in rat brain regions following glyphosate exposure. Environ Res 161:212–219. https://doi.org/10.1016/j.envres.2017.10.051

    Article  CAS  Google Scholar 

  • Maruthanayagam C, Sharmila G (2004) Haemato-biochemical variations induced by the pesticide, monocrotophos in Cyprinus carpio during the exposure and recovery periods. Nat Environ Pollut Technol 3(4):491–494

    CAS  Google Scholar 

  • Menéndez-Helman RJ, Ferreyroa GV, Dos Santos AM, Salibián A (2012) Glyphosate as an acetylcholinesterase inhibitor in Cnesterodondecem maculatus. Bull Environ Contam Toxicol 88(1):6–9. https://doi.org/10.1007/s00128-011-0423-8

    Article  CAS  Google Scholar 

  • Misra CK, Das BK, Mukherjee SC, Pattnaik P (2006) Effect of multiple injections of β-glucan on non-specific immune response and disease resistance in Labeo rohita fingerlings. Fish Shellfish Immunol 20(3):305–319. https://doi.org/10.1016/j.fsi.2005.05.007

    Article  CAS  Google Scholar 

  • Modesto KA, Martinez CB (2010) Effects of Roundup Transorb on fish: hematology, antioxidant defenses and acetylcholinesterase activity. Chemosphere 81(6):781–7. https://doi.org/10.1016/j.chemosphere.2010.07.005

    Article  CAS  Google Scholar 

  • Moreno NC, Sofia SH, Martinez CB (2014) Genotoxic effects of the herbicide Roundup Transorb® and its active ingredient glyphosate on the fish Prochilodus lineatus. Environ Toxicol Pharmacol 37(1):448–454. https://doi.org/10.1016/j.etap.2013.12.012

    Article  CAS  Google Scholar 

  • Namratha ML, Lakshman M, Jeevanalatha M, Kumar BA (2020) Assessment of vitamin c protective activity in glyphosate- induced hepatotoxicity in rats. Pak Vet J. https://doi.org/10.29261/pakvetj/2020

    Article  Google Scholar 

  • Nardi J, Moras PB, Koeppe C, Dallegrave E, Leal MB, Rossato-Grando LG (2017) Prepubertal subchronic exposure to soy milk and glyphosate leads to endocrine disruption. Food Chem Toxicol 100:247–252

    Article  CAS  Google Scholar 

  • Naveed A, Venkateshwarlu P, Janaiah C (2004) The action of sublethal concentration of endosulfan and kelthane on regulation of protein metabolism in the fish, Claria sbatrachus(L). Nat Environ Poll Technol 3(4):539–544

    CAS  Google Scholar 

  • Naveed A, Janaiah C, Venkateshwarlu P (2011) The effects of lihocin toxicity on protein metabolism of the fresh water edible fish, Channa punctatus (Bloch) J Toxicol. Environ Health Part A3(1):018–023. https://doi.org/10.5897/JTEHS.9000070

    Article  Google Scholar 

  • Nešković NK, Poleksić V, Elezović I, Karan V, Budimir M (1996) Biochemical and histopathological effects of glyphosate on carp, Cyprinus carpio L. Bull Environ Contam Toxicol 56(2):295–302. https://doi.org/10.1007/s001289900044

    Article  Google Scholar 

  • Nussey G, Van Vuren JH, Du Preez HH (1995) Effect of copper on blood coagulation of Oreochromis mossambicus (Cichlidae). Comp Biochem Physiol C Pharmacol Toxicol 111(3):359–367. https://doi.org/10.1016/0742-8413(95)00062-3

    Article  CAS  Google Scholar 

  • Nwani CD, Nagpure NS, Kumar R, Kushwaha B, Kumar P, Lakra WS (2011) Muta-genic and genotoxic assessment of atrazine-based herbicide to freshwater fish Channa puntatus (Bloch) using micronucleus test and single cell gel electrophoresis. Environ Toxicol Pharmacol 31:314–322

    Article  CAS  Google Scholar 

  • OECD (2012) New and emerging water pollutants arising from agriculture, prepared by Alistair B.A. Boxall. Paris, Organisation for Economic Co-operation and Development (OECD) Publishing

  • Ogamba EN, Inyang IR, Azuma IK (2011) Effect of paraquat dichloride on some metabolic and enzyme parameters of Clariasgariepinus. Curr Res J Biol Sci 3(3):186–190

    CAS  Google Scholar 

  • Omoniyi MP (2018) Toxicity effect of atrazine on histology, haematology and biochemicalindices of Clariasgariepinus. Int J Fish Aquat Stud 6(3):87–92

    Google Scholar 

  • Pandey PK, Ajima MNO, Kumar K, Poojary N, Kumar S (2017) Evaluation of DNA damage and physiological responses in Nile tilapia, Oreochromis niloticus (Linnaeus, 1758) exposed to sub-lethal diclofenac (DCF). Aqua Toxicol 186:205–214. https://doi.org/10.1016/j.aquatox.2017.03.007

    Article  CAS  Google Scholar 

  • Peixoto F (2005) Comparative effects of the Roundup and glyphosate on mitochondrial oxidative phosphorylation. Chemosphere 61(8):1115–1122. https://doi.org/10.1016/j.chemosphere.2005.03.044

    Article  CAS  Google Scholar 

  • Pereira AG, Jaramillo ML, Remor AP, Latini A, Davico CE, da Silva ML, Müller YMR, Ammar D, Nazari EM (2018) Low-concentration exposure to glyphosate-based herbicide modulates the complexes of the mitochondrial respiratory chain and induces mitochondrial hyperpolarization in the Danio rerio brain. Chemosphere 209:353–362. https://doi.org/10.1016/j.chemosphere.2018.06.075

    Article  CAS  Google Scholar 

  • Poiger T, Buerge IJ, Bächli A, Müller MD, Balmer ME (2017) Occurrence of the herbicide glyphosate and its metabolite AMPA in surface waters in Switzerland determined with on-line solid phase extraction LC-MS/MS. Environ Sci Poll Res 24(2):1588–1596. https://doi.org/10.1007/s11356-016-7835-2

    Article  CAS  Google Scholar 

  • Pu Y, Yang J, Chang L, Qu Y, Wang S, Zhang K, Xiong Z, Zhang J, Tan Y, Wang X, Fujita Y, Ishima T, Wang D, Hwang SH, Hammock BD, Hashimoto K (2020) Maternal glyphosate exposure causes autism-like behaviors in offspring through increased expression of soluble epoxide hydrolase. Proc Natl Acad Sci U S A 117:11753–11759. https://doi.org/10.1073/pnas.1922287117

    Article  CAS  Google Scholar 

  • Ramesh M, Saravanan M (2008) Haematological and biochemical responses in a freshwater fish Cyprinus carpio exposed to chlorpyrifos. Int J Integr Biol 3:80–83

    CAS  Google Scholar 

  • Reish DL, Oshida PS (1987) Manual of methods in aquatic environment research Part 10 Short-term static bio-assay. FAO Fish Tech Pap 247:162

    Google Scholar 

  • Reitman S, Frankel S (1957) A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am J Clin Pathol 28:56–63. https://doi.org/10.1093/ajcp/28.1.56

    Article  CAS  Google Scholar 

  • Relyea RA (2005) The lethal impacts of Roundup and predatory stress on six species of North American tadpoles. Arch Environ Contam Toxicol 48(3):351–357. https://doi.org/10.1007/s00244-004-0086-0

    Article  CAS  Google Scholar 

  • Rogers JA, Mirza RS (2013) The effects of bisphenol-A on the immune system of wild yellow perch, Perca flavescens. Water Air Soil Poll 224:1–6

    Article  Google Scholar 

  • Roy NM, Carneiro B, Ochs J (2016) Glyphosate induces neurotoxicity in zebra fish. Environ Toxicol Pharmacol 42:45–54

    Article  CAS  Google Scholar 

  • Salam MA, Shahjahan M, Sharmin S, Haque F, Rahman MK (2015) Effects of sub-lethal doses of an organo-phosphorous insecticide sumithion on some hematological parameters in common carp, Cyprinus carpio. Pak J Zool 47:1487–1491

    CAS  Google Scholar 

  • Salbego J, Pretto A, Gioda CR, de Menezes CC, Lazzari R, Radünz Neto J, 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(3):740–745. https://doi.org/10.1007/s00244-009-9464-y

    Article  CAS  Google Scholar 

  • Saravanan M, Karthika S, Malarvizhi A, Ramesh M (2011) Ecotoxicological impacts of clofibric acid and diclofenac in common carp (Cyprinus carpio) fingerlings: hematological, biochemical, ionoregulatory and enzymological responses. J Hazard Mater 195:188–194. https://doi.org/10.1093/ajcp/28.1.56

    Article  CAS  Google Scholar 

  • Schaperclaus W (1991) Fish diseases, vol 1. Oxonian Press Private Limited, New Delhi, pp 594

  • Shiogiri NS, Carraschi SP, Cubo P, Schiavetti BL, da Cruz C, Pitelli RA (2010) Ecotoxicity of glyphosate and Aterbane® br surfactant on guaru (Phalloceroscaudi maculatus). Acta Sci Biol Sci 32(3):285–289. https://doi.org/10.4025/actascibiolsci.v32i3.6795

    Article  CAS  Google Scholar 

  • Singh RN, Yadava CL, Singh AK (2015) Dimethoate induced alterations in tissue protein levels of common carp. Cyprinus carpio (Linn.). Int J Adv Res Bio Sci 2(3):176–182

    CAS  Google Scholar 

  • Singh S, Kumar V, Gill JP, Datta S, Singh S, Dhaka V, Kapoor D, Wani AB, Dhanjal DS, Kumar M, Harikumar SL (2020) Herbicide glyphosate: toxicity and microbial degradation. Int J Environ Res Public Health 17(20):7519. https://doi.org/10.3390/ijerph17207519

    Article  CAS  Google Scholar 

  • Strickland RD, Freeman ML, Gurule FT (1961) Copper binding by proteins in alkaline solution. Anal Chem 33(4):545–552. https://doi.org/10.1021/ac60172a019

    Article  CAS  Google Scholar 

  • Svoboda M (2001) Stress in fishes. Bulletin VURH Vodnany (Czech Republic), A review

    Google Scholar 

  • Svoboda M, Luskova V, Drastichova J, Žlabek V (2001) The effect of diazinon on haematological indices of common carp (Cyprinus carpio L.). Acta Vet Brno 70(4):457–465. https://doi.org/10.2754/avb200170040457

    Article  CAS  Google Scholar 

  • Svobodova Z, Groch L, Flajšhans M, Vykusova B, Machova J (1997) Effect of long-term therapeutic bath in malachite green on common carp (Cyprinus carpio L.). Acta Vet Brno 66(2):111–116

    Article  CAS  Google Scholar 

  • 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. https://doi.org/10.1016/j.ecoenv.2014.09.027

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Tsui MT, Chu LM (2004) Comparative toxicity of glyphosate-based herbicides: aqueous and sediment pore water exposures. Arch Environ ContamToxicol 46(3):316–323. https://doi.org/10.1007/s00244-003-2307-3

    Article  CAS  Google Scholar 

  • Ullah S, Zorriehzahra MJ (2015) Ecotoxicology: a review of pesticides induced toxicity in fish. Adv Anim Vet Sci 3(1):40–57

    Article  Google Scholar 

  • Veedu SK, Ayyasamy G, Tamilselvan H, Ramesh M (2022) Single and joint toxicity assessment of acetamiprid and thiamethoxam neonicotinoids pesticides on biochemical indices and antioxidant enzyme activities of a freshwater fish Catla catla. Comp Biochem Physiol Part C: Toxicol Pharmacol. https://doi.org/10.1016/j.cbpc.2022.109336

  • Velmurugan B, Selvanayagam M, Cengiz EI, Unlu E (2009) Histopathological changes in the gill and liver tissues of freshwater fish, Cirrhinus mrigala exposed to dichlorvos. Brazil Arch Biol Technol 52:1291–1296

    Article  Google Scholar 

  • Vencill WK (2002) Herbicide Handbook. Weed Science Society of America, Champaign, pp 299–300

  • Vosilinko V, Grebenev A (1990) Internal diseases Jordan. J Bio Sci 36:76–79

  • Wang JQ, Hussain R, Ghaffar A, Afzal G, Saad AQ, Ahmad N, Nazir U, Ahmad HI, Hussain T, Khan A (2022) Clinico-hematological, mutagenic, and oxidative stress induced by pendimethalin in freshwater fish bighead carp (Hypophthalmichthys nobilis). Oxid Med Cell Longev. https://doi.org/10.1155/2022/2093822

  • Wepener V, Van Vuren JH, Du Preez HH (1992) The effect of hexavalent chromium at different pH values on the haematology of Tilapia sparrmanii (Cichlidae). Comp Biochem Physiol C Toxicol Pharmacol 101(2):375–81. https://doi.org/10.1016/0742-8413(92)90290-n

    Article  CAS  Google Scholar 

  • Williams GM, Kroes R, Munro IC (2000) Safety evaluation and risk assessment of the herbicide Roundup and its active ingredient, glyphosate, for humans. RegulToxicolPharmacol 31(2):117–165. https://doi.org/10.1006/rtph.1999.1371

    Article  CAS  Google Scholar 

  • World Health Organization (WHO) (1994) Glyphosate. Environmental health criteria 159. Geneva, Switzerland. https://wedocs.unep.org/20.500.11822/29463

  • Yang X, Song Y, Zhang C, Pang Y, Song X, Wu M, Cheng Y (2019) Effects of the glyphosate-based herbicide roundup on the survival, immune response, digestive activities and gut microbiota of the Chinese mitten crab, Eriocheir sinensis. Aquat Toxicol 214:105243. https://doi.org/10.1016/j.aquatox.2019.105243

    Article  CAS  Google Scholar 

  • Yousafzai AM, Shakoori AR (2011) Hepatic responses of a freshwater fish against aquatic pollution. Pak J Zool 43(2):209–221

    CAS  Google Scholar 

  • Zare MR, Dehghani M, Fard AF (2020) Investigating the relationship between synergistic effects and diversity of four widely used agricultural pesticides by using bacterial species in liquid culture medium. Environ Mon Assess 192(3):1–9. https://doi.org/10.1007/s10661-020-8125-5

    Article  CAS  Google Scholar 

  • Zhang C, Hu X, Luo J, Wu Z, Wang L, Li B, Wang Y, Sun G (2015) Degradation dynamics of glyphosate in different types of citrus orchard soils in China. Molecules 20(1):1161–1175. https://doi.org/10.3390/molecules20011161

    Article  CAS  Google Scholar 

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Acknowledgements

The authors are thankful to Vice-Chancellor, Central Agricultural University, Imphal, Manipur.

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Khaidem Rabina Chanu: investigation, methodology, software, and writing—original draft. Yumnam Abungcha Mangang: formal analysis and writing—review and editing. Sourabh Debbarma: formal analysis and resources. Pramod Kumar Pandey: conceptualization, writing—review and editing, validation, and supervision.

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Correspondence to Pramod Kumar Pandey.

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The fish species studied in the present study is not protected under The Wildlife Protection Act, 1972 (last amended in 2013), Government of India, and the experiment was approved by the Institutional Animal Ethics Committee (IAEC) of College of Fisheries (Central Agricultural University, Imphal), India. All the guidelines on animal use and care were followed accordingly.

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Chanu, K.R., Mangang, Y.A., Debbarma, S. et al. Effect of glyphosate-based herbicide roundup on hemato-biochemistry of Labeo rohita (Hamilton, 1822) and susceptibility to Aeromonas hydrophila infection. Environ Sci Pollut Res 30, 110298–110311 (2023). https://doi.org/10.1007/s11356-023-29967-8

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