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Histological and hematological changes to Clarias gariepinus juveniles exposed to acute doses of Emamectin benzoate in a static bioassay

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Abstract

Emamectin benzoate (EMB) is a potent neurotoxic pesticide, extensively used in agriculture and aquaculture in Nigeria. The knowledge of its toxicological impact to C. gariepinus in Nigeria is scarce. Thus, the investigation was designed to uncover its 96 h LC50, safe level to aquatic media, histological impact on fish liver, gill and hematological changes in the blood parameters. 96 h LC50 was 0.34 mg L−1. Safe level of EMB was 0.034 mg L−1. Dose dependent liver degenerations were characterized by; Congestion of the central vein by inflammatory cells, pyknotic nuclei of hepatocytes, coagulation necrosis, focal necrosis, dilations of sinusoidal spaces and infiltration of periportal regions by inflammatory cells. Dose dependent changes in gill were characterized by; mucus secretion, shrinkage of secondary lamellae, hyperplasia, occlusion of secondary lamellae, degeneration of gill cartilage, necrosis of respiratory epithelia and erosion of secondary lamellae. Red blood cell indices decreased minimally at the end of the 96 h exposure. White blood cell count (WBCC), mean corpuscular volume (MCV) and mean corpuscular hemoglobin (MCH) were significantly (p ≤ 0.05) elevated in three treatments. Neutrophils decreased significantly (p ≤ 0.05), basophils, eosinophils and monocytes showed mixed tendencies. The findings of this investigation imply that C. garipinus exposed to EMB may cause dose and time-dependent changes in the liver and gill histology as well as alterations in the fish’s hematological profile, all of which were harmful to the fish’s health. To avoid negative effects on fish in nearby aquatic settings, it is advised that the use of EMB be monitored and limited.

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References

  • Aghamirkarimi SH, Mashinchian MA, Sharifpour I, Jamili SH, Ghavam MP (2017) Sublethal effects of copper nanoparticles on the histology of gill, liver and kidney of the Caspain roach, Rutilus rutilus caspicus. Global J Environ Sci Manag 3(3):323–332

    CAS  Google Scholar 

  • Ajima MNO, Pandey PK, Kumar K, Poojary N (2017) Neurotoxic effects, molecular responses and oxidative stress biomarkers in nile tilapia, Oreochromis niloticus (Linnaeus, 1758) exposed to verapamil. Comp Biochem Physiol Part C: Toxicol Pharmacol 196:44–52. https://doi.org/10.1016/j.cbpc.2017.03.009

    Article  CAS  Google Scholar 

  • Alan JAS, Genaci JR, Holdson PV (1983) Histopathological and physiological response of rainbow trout, Salmo gairdneri (R) to sub-lethal levels of lead. Water Res. 17:1115–1118

    Article  Google Scholar 

  • Amaeze NH, Komolafe BO, Salako AF, Akagha KK, Briggs TD, Olatinwo OO, Femi MA (2020) Comparative assessment of the acute toxicity, haematological and genotoxic effects of ten commonly used pesticides on the African Catfish, Clarias gariepinus Burchell 1822. Heliyon 6(2020):e04768

    Article  Google Scholar 

  • APHA [American Public Health Association] American Water Works Association and Water Pollution Control Federation (APHA/AWWA/WEF) (2005) Stand Meth Exam Water Wastewater 21st edn. APHA, Washington.

  • Blaxhall PC, Daisley KW (1973) Routine hematological methods for use with fish blood. J Fish Biol 5(6):771–781. https://doi.org/10.1111/j.1095-8649.1973.tb04510.x

    Article  Google Scholar 

  • Bowker JD, Carty DG, Wandelear N, Schaffer J, Swee W, LaPatra SE (2012) Efficacy of SLICE premix (0.2% emamectin benzoate) for reducing infestations of Salmincola spp. on freshwater-reared rainbow trout. N Am J Aquac 74:428–437

    Article  Google Scholar 

  • BPDB Bio-Pesticides DataBase, Univ. Hertfordsh. (n.d.). http://sitem.herts.ac.uk/aeru/bpdb/Reports/1326.htm.

  • CAHS (Centre for Aquatic Health Sciences) (2007) SLICE R _: action/use/effects. CAHS, Campbell River, British Columbia

  • CCREM (1991) Canadian water quality guidelines. Canadian council of resources and environmental ministry, inland waters directorate, environment Canada, Ottawa

    Google Scholar 

  • Cengiz EI, Uniu E, Balci K (2001) The histopathological effects of Thiodan on the liver and gut of Mosquitofish, Gambusia affinis. J Environ Sci Health, Part B; Pestic, Food Contam, Agric, Wastes.Taylor and Francis 36(1):75–85

    Article  CAS  Google Scholar 

  • Chinabut S, Limsuwan C, Kitswat P (1991) Histology of walking catfish, Clarias batrachus. Aquatic Animal Health Research Institute, Thailand, 96

    Google Scholar 

  • CWQC [Committee on Water Quality Criteria] (1972) A report of the committee on water quality research series. EPA-R3–73–003, US environmental protection agency report, CWQC, Cincinnati

  • Dacie JV, Lewis SM (2011) Practical haematology, 11th Edn. Churchill Livingstone, New York

    Google Scholar 

  • Daoust PY, Ferguson HW (1983) Gill diseases of cultured Salmonids in Ontario. Can J Comp Med 47:358–362

    CAS  Google Scholar 

  • Edson LR, Maria Jose TRP, Fabio JP, Marcelo LV (2001) Histopathologic lesions in the liver of Prochilodus lineatus exposed to a sublethal concentration of the organophosphate insecticide Dipterex 500(R)(Trichlorfon). Acta Sci Maringa 23(2):503–505

    Google Scholar 

  • Emmanuel O, Christopher N, Christian M, Stanley I, Friday N (2020) Oxidative stress, biochemical, lipid peroxidation and antioxidant responses in Clarias gariepinus exposed to acute concentrations of ivermectin. Environ Sci Pollut Res 27(14):16806–16815

    Article  Google Scholar 

  • FAO (1987) Manual of methods in aquatic environmental research. Part to Short – term static bioassays Fish Tech. paper, No. 247. FAO, Rome

    Google Scholar 

  • Finney YT (1971) Probit Analysis. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Hakalahti T, Lankinen Y, Valtonen ET (2004) Efficacy of emamectin benzoate in the control of Argulus coregoni (Crustacea: branchiura) on rainbow trout Oncorhynchus mykiss. Dis Aquat Organ 60:197–204

    Article  CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (1995) In free radicals in biology and medicine. Oxford University Press New York p543

    Google Scholar 

  • Hanson SK, Hill JE, Watson CA, Yanong RPE, Endris R (2011) Evaluation of emamectin benzoate for the control of experimentally induced infestations of Argulus sp. in goldfish and koi carp. J Aquat Anim Health 23:30–34

    Article  CAS  Google Scholar 

  • Hibiya T (1982) An atlas of fish histology: normal and pathological features. Kodansha Tokyo

    Google Scholar 

  • Hinton DE, Laurén DJ (1990) Integrative histopathological effects of environmental stressors on fishes. Symp Am Fish Soc 8:51–66

    Google Scholar 

  • Hong X, Zhao X, Tian X, Li J, Zha J (2018) Changes of hematological and biochemical parameters revealed genotoxicity and immunotoxicity of neonicotinoids on Chinese rare minnows (Gobiocypris rarus). Environ Pollut 233:862–871

    Article  CAS  Google Scholar 

  • Iheanacho SC, Adeolu AI, Nwose R, Ekpenyong J, Offu P, Amadi-Eke A, Iheanacho AC, Ogunji J (2021) Genotoxicity, oxidative stress and lysozyme induction in Clarias gariepinus chronically exposed to water-soluble fraction of burnt tire ash. Ecotoxicology 30:1983–1996. https://doi.org/10.1007/s10646-021-02474-7

    Article  CAS  Google Scholar 

  • Iheanacho SC, Ekpenyong J, Nwose R, Adeolu AI, Offu P, Amadi-Eke A, Iheanacho AC, Ogunji J (2022). Effects of burnt tire-ash on Na+/K+, Ca2+ - ATPase, serum immunoglobulin and brain acetylcholinesterase activities in Clarias gariepinus (Burchell, 1822). Drug Chem Toxicol. 1–7. https://doi.org/10.1080/01480545.2022.2061987

  • IJC (1977) New and Revised Great Lakes Water Quality Objectives. Great Lake Basin, Windsor. IJC, Ottawa

  • Jansson RK, Peterson RF, Mookerjee PK, Halliday WR, Argentine JA, Dybas RA (1997) Development of a novel soluble granule formulation of emamectin benzoate for control of lepidopterous pests. Fla Entomol 80:425–443

    Article  CAS  Google Scholar 

  • Jee JH, Kang JC (2004) Effect of phenanthrene on haematological parameters in olive flounder, Paralichthys olivaceus (Temminch et Schlegel). Aquac Res 35:1310–1317

    Article  CAS  Google Scholar 

  • Jenkins FJ, Smith B, Rajanna U, Shameem K, Umadevi VS, Madhavi R (2003) Effect of sub-lethal concentrations of endosulfan on hematological and serum biochemical parameters in the carp (Cyprinus carpio). B Environ Contam Toxicol 70:0993–0997. https://doi.org/10.1007/s00128-003-0080-7

    Article  CAS  Google Scholar 

  • Kumar V, Swain HS, Das BK, Roy S, Upadhyay A, Ramteke MH, Kole RK, Banerjee H (2022) Assessment of the effect of sub-lethal acute toxicity of Emamectin benzoate in Labeo rohita using multiple biomarker approach. Toxicol Rep 9:102–110

    Article  CAS  Google Scholar 

  • Kumari K (2020) Pesticides toxicity in fishes: a review. J Entomol Zool Studies 8(5):1640–1642

    Google Scholar 

  • Lasota JA, Dybas RA (1991) Avermectins, a novel class of compounds: implications for use in arthropod pest control. Annu Rev Entomol 36:91–117

    Article  CAS  Google Scholar 

  • Laurent P, Perry SF (1995) Morphological basis of acid-base and ionic regulation in fish. In: Heisler N (ed) Advances in Comparative and Environmental Physiology. Mechanisms of Systemic Regulation: Acid-Base Regulation Ion Transfer and Metabolism, Springer, Heidelberg, pp 91–118

  • Matey VE (1999). The functional morphology of gill epithelia in freshwater teleosts fish. In: Physiology, Biochemistry and Toxicology of Freshwater Animals. Nauka. Leningrad (in Russian). pp: 104–114

  • Modra H, Svobodova Z, Kolarova J (1998) Comparism of Differential Leukocyte Counts in Fish of Economic and Indicator Importance. Acta Veterinaria Brno 67(4):215–226

    Article  Google Scholar 

  • NAS/NAE (1973) Water quality criteria, EPA-R3–033. US Government Printing Office, Washington

  • Nwani CD, Somdare PO, Ogueji EO, Nwani JC, Ukonze JA, Nwadinigwe AO (2017) Genotoxicity assessment and oxidative stress responses in freshwater African catfish Clarias gariepinus exposed to fenthion formulations. Drug Chem Toxicol 40(3):273–280. https://doi.org/10.1080/01480545.2016.1209772

    Article  CAS  Google Scholar 

  • Nelson DA, Morris MW (1989) Basic Methodology, Haematology and Coagulation, Part IV eds.Nelson DA, Henry JBIn: Clinical Diagnosis and Management by Laboratory Methods17th ed. WB Saunders Philadelphia 578–625

    Google Scholar 

  • Ogueji EO, Nwani CD, Mbah C, Iheanacho S, Nweke F (2020) Oxidative stress, biochemical, lipid peroxidation, and antioxidant responses in Clarias gariepinus exposed to acute concentrations of ivermectin. Environ Sci Pollut Res 27:16806–16815

    Article  CAS  Google Scholar 

  • Ogueji EO (2008) Toxicity of chlorpyrifos-ethyl and lambda-cyhalothrin (pesticides) to juveniles of African catfish Clarias gariepinus (Burchell, 1822) Department of Biological Sciences, Ahmadu Bello University, Zaria, Nigeria, PhD dissertation

    Google Scholar 

  • Ogueji EO, Usman BI, Auta J (2013) Histopathology of liver and gill of C.gariepinus (Burchell 1822) with swollen abdomen following exposure to acute and sublethal concentrations of chlorpyrifos-ethyl. Int J Basic Appl Sci 2(3):223–229

    Google Scholar 

  • Ogueji EO, Nwani CD, Iheanacho SC, Mbah CE, Okeke CO, Yaji A (2018) Acute toxicity effects of ibuprofen on behaviour and haematological parameters of african catfish clarias Gariepinus (Burchell, 1822). African. J Aquat Sci 43(3):293–303. https://doi.org/10.2989/16085914.2018.1465393

    Article  CAS  Google Scholar 

  • Ogueji EO, Nwani CD, Mbah CE, Nweke FN (2019) Acute hematological toxicity of ivermectin to juvenile Clarias gariepinus. Toxicolog Environ Chem 101(3-6):300–314

    Article  CAS  Google Scholar 

  • Ogueji EO, Iheanacho SC, Nwani CD, Mbah CE, Okeke OC, Ibrahim BU (2017) Toxicity of diazepam on lipid peroxidation, biochemical and oxidative stress indicators on liver and gill tissues of African catfish Clarias gariepinus (Burchell, 1822). Int J Fish Aquat Stud 5(3):114–123

    Google Scholar 

  • Okey IB, Ekpenyong JJ, Inya FU (2021) Haematological and histopathological examinations of African Catfish (Clarias gariepinus) exposed to sub-lethal concentrations of Paraquat. Asian J Fish Aquat Res 15(6):29–45. https://doi.org/10.9734/AJFAR/2021/v15i630348

    Article  Google Scholar 

  • Okey IB, Igiri MR, Ekpenyong JJ, Inya FU (2022) Haematological and biochemical responses in African catfish, (Clarias gariepinus) juveniles immobilized with clove basil, (Ocimum gratissimum) powder. Anaesthetic. J Aquat Sci Oceanogr 3(1):102

    Google Scholar 

  • Oliveira R, Grisolia CK, Monteiro MS, Soares AMVM, Domingues I (2016) Multilevel assessment of ivermectin effects using different zebrafish life stages. Comp Biochem Physiol, Part C 187:50–61. https://doi.org/10.1016/j.cbpc.2016.04.004

    Article  CAS  Google Scholar 

  • Ostaszewska T, Dabrowski K, Palacios ME, Olejniczak M, Wieczorek M (2005) Growth and morphological changes in digestive tract of rainbow trout (Oncorhynchus mykiss) and pacu (Piaractus mesopotamicus) due to casein replacement with soybean proteins. Aquaculture 245:273–286

    Article  CAS  Google Scholar 

  • Parrish PR (1988). Acute toxicity tests: In: Fundamentals of AquaticToxicology, Methods and Applications, Hemisphere, Washington DC pp. 34–42

  • Perry SF (1997) The chloride cell: structure and function in the gills of freshwater fishes. Annu Rev Physiol 59:325–347

    Article  CAS  Google Scholar 

  • Perry SF, Laurent P (1993) Environmental Effects on Fish Gill Structure and Function eds.Rankin JCliff, Jensen FrankBIn: Fish Ecophysiology Chapman and Hall, London, 231–264

    Chapter  Google Scholar 

  • Randall DJ (1990) Control and co-ordination of gas exchange in water breathers. Adv Comp Environ Physiol 6:253–278

    Article  Google Scholar 

  • Reish DL, Oshida PS (1987) Manual of methods in aquatic environment research Part 10 Short term static bioassay FAO. fisheries. Technical paper 247. FAO, Rome,1–62

    Google Scholar 

  • Rusia V, Sood SK (1992) Routine Hematological Tests eds.Mukerjee KLIn: Medical Laboratory Technology Tata McGraw Hill, New Delhi, 252–258

    Google Scholar 

  • Saravanan M, Devi KU, Malarvizhi A, Ramesh M (2012) Effects of ibuprofen on hematological, biochemical and enzymological parameters of blood in an indian major carp, Cirrhinus mrigala. Environ Toxicol Pharmacol 34(1):14–22. https://doi.org/10.1016/j.etap.2012.02.005

    Article  CAS  Google Scholar 

  • Seith N, Saxena KK (2003) Hematological responses in a freshwater fish Channa punctatus due to fenvalerate. Bulletin Environ Contam Toxicol 71:1192–1199. https://doi.org/10.1007/s00128-003-8732-1

    Article  CAS  Google Scholar 

  • Sprague JB (1977) Measurement of pollutant toxicity to fish: in: bioassay methods for acute toxicity. Water Res 3:793–821

    Article  Google Scholar 

  • Svobodova Z, Vykusova B, Machova J (1994) The effects of pollutants on selected haematological and biochemical parameters in fish, chapter 4 eds.Muller R, Lloyd RIn: Sublethal and Chronic Effects of Pollutants on Freshwater Fishes. FAO Oxford 39–52

    Google Scholar 

  • Thompson SW, Hunt RD (1966) Selected histo-chemical and histopathological methods. Spring field, Illinois USA, 98–103

    Google Scholar 

  • US EPA (2008). Environmental fate and ecological risk assessment for the registration of emamectin benzoate use on tree nuts and pistachios (New Use). D345948

  • Whyte SK, Poley JD, Mueller A, Van Iderstine C, Fitzpatrick KE, Purcell SL, Koop BF, Johnson SC, Wadsworth S, Fast MD (2019) Avermectin treatment for Lepeophtheirus salmonis: impacts on host (Salmo salar) and parasite immunophysiology. Aquaculture 501:488–501

    Article  CAS  Google Scholar 

  • WRc (2017) Review of environmental quality standard for Emamectin Benzoate, Scottish environment protection agency, UC12191.03. Wiltshire

  • Yaji A, Iheanacho S, Ogueji E (2018) Sublethal exposure and toxicity effect of propanil on hematology and serum biochemistry in Oreochromis niloticus in a static bioassay. Gazi Univ J Sci 31(4):1048–1062. https://www.researchgate.net/publication/329338115

    Google Scholar 

  • Yaji A, Ogueji EO, Ekpenyong JJ (2021) Sub-lethal behavioral and biochemical toxicity of cypermetrin to juvenile Oreochromis niloticus in static bioassay. Fish Aquat Life 29:148–157. https://doi.org/10.2478/aopf-2021-0016

    Article  CAS  Google Scholar 

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“Emmanuel Ogueji and Joseph Nwakpa contributed to the study conception and design. Material preparation, data collection was done by Chukwunonso Elo and Ugochinyere Agbo. Analysis were performed by, Joshua Ekpenyong, and Michael Olaolu. The first draft of the manuscript was written by Emmanuel Ogueji and all authors commented on previous versions of the manuscript”. E.O and A.Y. did the semi quantitative analysis of histopathological changes in the tissues. They also wrote the main manuscript text. J.N. contributed in the design of the work and the analysis of water chemistry. C.E. was responsible for the collection of fish blood, and gathering of data for hematological parameters. U.A. collected gill samples and did the histological analysis. I.O. and G.A. collected the liver samples and did the histological analysis. M.O. did the analysis of blood parameters. J.E. did the bar chart for blood parameters and probit analysis for 96 h LC30-90. All authors read and approved the final manuscript.

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Correspondence to Emmanuel Ogueji.

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All experimental trials were approved by the Alex Ekwueme Federal University Ndufu Alike (AEFUNAI) ethics clearance committee in accordance with the university’s animal welfare act and the National Environmental Standard Regulations Enforcement Agency (NESREA) Act of Nigeria on the protection of animals against cruelty (Ref: FUNAI/SEN/ EBC/18/VOL.1/10).

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Ogueji, E., Nwakpa, J., Ekpenyong, J. et al. Histological and hematological changes to Clarias gariepinus juveniles exposed to acute doses of Emamectin benzoate in a static bioassay. Ecotoxicology 32, 569–582 (2023). https://doi.org/10.1007/s10646-023-02662-7

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