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Hematological, hepatic enzymes’ activity and oxidative stress responses of gray mullet (Mugil cephalus) after sub-acute exposure to copper oxide

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Abstract

Given the importance of assessing potential toxicity of heavy metals in valuable species of aquatic animals, the goal of the present research was to assess the sub-acute effects of copper oxide on hematological, enzymological, and oxidative stress responses of gray mullet to measure toxicity of copper oxide pollution in this significant fish. The median lethal concentration (LC50) value of copper oxide to gray mullet was detected at 3.15 ± 0.039 mg/L for 96 h, and 25 and 50% of the 96-h LC50 values were selected as sub-acute concentrations. The fish were exposed to (0.79 and 1.57 mg/L) copper oxide for 21 days. At the end of 21 days, the results showed that hemoglobin (Hb), hematocrit (Hct), red blood cells (RBC) count, MCV, MCH, and MCHC levels were found to be decreased in copper oxide treated fish, whereas white blood cells (WBC) count increased in copper-treated fish. Plasma aspartate aminotransferase (AST), alanine aminotransferase (ALT), and lactate dehydrogenase (LDH) activity increased in treated groups; however, copper oxide in both groups of sub-acute exposure significantly decreased plasma alkaline phosphatase (ALP) activity compared to the control group. Superoxide dismutase (SOD), catalase (CAT), and glutathione (GSH) levels significantly declined in copper oxide-treated fish. These findings indicated the deleterious effects of copper oxide on gray mullet, even at low concentrations, and offered that hematological and hepatic enzyme activity and antioxidants are suitable tools for evaluating heavy metals toxicity.

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References

  • Abdel-Khalek AA, Mohamed A, Kadry M, Shereen R, Badran M-AS, Marie S (2015) Comparative toxicity of copper oxide bulk and Nano particles in Nile tilapia; Oreochromis niloticus: biochemical and oxidative stress. J Basic App Zoo 72:43–57

    Article  CAS  Google Scholar 

  • Adakole JA (2012) Changes in some haematological parameters of the African catfish (Clarias gariepinus) exposed to a metal finishing company effluent. Ind J Sci Technol 4:2510–2514

    Google Scholar 

  • Aebi H (1984) Catalase in vitro. Meth Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • Akbary P, Jahanbakhshi A (2016) Growth yield, survival, carcass quality, haematological, biochemical parameters and innate immune responses in the grey mullet (Mugil cephalus Linneaus, 1758) fingerling induced by Immunogen® prebiotic. J App Anim Res:1–7. https://doi.org/10.1080/09712119.2016.1251927.

  • Akbary P, Pirbeigi A, Jahanbakhshi A (2016) Analysis of primary and secondary stress responses in bighead carp (Hypophthalmichthys nobilis) by anesthetization with 2-phenoxyethanol. Int J Environ Sci Technol 13:1009–1016

    Article  Google Scholar 

  • Almeida JR, Oliveira C, Gravato C, Guilhermino L (2010) Linking behavioral alterations with biomarkers responses in the European sea bass Dicentrarchus labrax L. exposed to the organophosphate pesticide fenitrothion. Ecotoxicology 19(8):1369–1381

    Article  CAS  Google Scholar 

  • Amr A, Shereen RB, Mohamed-Assem SM (2016) Toxicity evaluation of copper oxide bulk and nanoparticles in Nile tilapia, Oreochromis niloticus, using hematological, bioaccumulation and histological biomarkers. Fish Physiol Biochem 42:1225–1236

    Article  Google Scholar 

  • Bahmani M, Kazemi R, Donskaya P (2012) A comparative study of some hematological features in young reared sturgeons (Acipenser persicus and Huso huso). Fish Physiol Biochem 4(2):135–140

    Google Scholar 

  • Banaee M, Mirvagefei A, Rafei G, Amiri BM (2008) Effect of sub-lethal diazinon concentrations on blood plasma biochemistry. Int J Environ Res 2(2):189–198

    CAS  Google Scholar 

  • Belfield A, Goldberg DM (1971) Revised assay for serum phenyl phosphatase activity using 4-amino-antipyrine. Enzymol 12:561–573

    Article  CAS  Google Scholar 

  • Das D, Moniruzzaman M, Sarbajna A, Chakraborty SB (2017) Effect of heavy metals on tissue-specific antioxidant response in Indian major carps. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-017-9415-5

  • Dorval J, Hontela A (2003) Role of glutathione redox cycle and catalase in defense against oxidative stress induced by endosulfan in adrenocortical cells of rainbow trout (Oncorhynchus mykiss). Toxicol Appl Pharmacol 192:191–200

    Article  CAS  Google Scholar 

  • Eroglu A, Dogan Z, Kanak EG, Atli G, Canli M (2014) Effects of heavy metals (Cd, Cu, Cr, Pb, Zn) on fish glutathione metabolism. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-014-2972-y

  • Eyckmans M, Celis N, Horemans N, Blust R, De Boeck G (2011) Exposure to waterborne copper reveals differences in oxidative stress response in three freshwater fish species. Aquat Toxicol 103:112–120

    Article  CAS  Google Scholar 

  • Fırat O, Hikmet Y, Cogun, Tu¨zin A, Yu¨zereroglu, Gu¨lbin Go¨k, Fırat O, Ferit Kargin, Yasemin Ko¨temen (2011) A comparative study on the effects of a pesticide (cypermethrin) and two metals (copper, lead) to serum biochemistry of Nile tilapia, Oreochromis niloticus Fish Physiol Biochem 37:657–666

  • Ghosh D, Bhattacharya S, Mazumder S (2006) Perturbations in the catfish immune responses by arsenic: organ and cell specific effects. Comp Biochem Physiol C Comp Pharmacol Toxicol 143:455–463

    Article  Google Scholar 

  • Gomes T, Pinheiro JP, Cancio I, Pereira CG, Cardoso C, Bebianno MJ (2011) Effects of copper nanoparticles exposure in the mussel Mytilus galloprovincialis. Environ Sci Technol 45(21):9356–9362

    Article  CAS  Google Scholar 

  • Guney T, Yıldız B, Altikat S, Kural N, Alatas O (2009) Decreased antioxidant capacity and increased oxidative stress in patients with juvenile idiopathic arthritis. J Pediatric Sci 1:1–6

    Google Scholar 

  • Hedayati A, Jahanbakhshi A (2012) The effect of water-soluble fraction of diesel oil on some hematological indices in the great sturgeon Huso huso. Fish Physiol Biochem 38:1753–1758

    Article  CAS  Google Scholar 

  • Hedayati A, Ghaffari Z (2013) Effect of mercuric chloride on some hematological, biochemical parameters in silver carp (Hypophthalmichthys molitrix). Int J Vet Med: Res and Rep 20:1–11

    Google Scholar 

  • Hedayati A, Kolangi H, Jahanbakhshi A, Shaluei F (2012) Evaluation of silver nanoparticles ecotoxicity in silver carp (Hypophthalmicthys molitrix) and goldfish (Carassius auratus). Bul J Vet Med 15(3):172–177

    Google Scholar 

  • Hoseini S, Hedayati A, Ghelichpour M (2014) Plasma metabolites, ions and thyroid hormones levels, and hepatic enzymes’ activity in Caspian roach (Rutilus rutilus caspicus) exposed to waterborne manganese. Ecotoxic Environ Safe 107:84–89

    Article  CAS  Google Scholar 

  • Iger Y, Lock RAC, Jenner HA, Bonga SEW (1994) Cellular responses in the skin of carp (Cyprinus carpio) exposed to copper. Aquat Toxicol 29:49–64

    Article  CAS  Google Scholar 

  • Islam MS, Tanaka M (2004) Impacts of pollution on coastal and marine ecosystems including coastal and marine fisheries and approach of management: a review and synthesis. Marine Poll Bull 48(7):624–649

    Article  CAS  Google Scholar 

  • Jahanbakhshi A, Hedayati A (2013) The effect of water-soluble fraction of crude oil on serum biochemical changes in the great sturgeon Huso huso. Comp Clin Pathol 22(6):1099–1102

    Article  CAS  Google Scholar 

  • Javed M, Usmani N (2014) Assessment of heavy metals (Cu, Ni, Fe, Co, Mn, Cr, Zn) in rivulet water, their accumulations and alterations in hematology of fish Channa punctatus. Afr J Biotechnol 13(3):492–501

    Article  Google Scholar 

  • Kanak EG, Dogan Z, Eroglu A, Atli G, Canli M (2014) Effects of fish size on the response of antioxidant systems of Oreochromis niloticus following metal exposures. Fish Physiol Biochem 40:1083–1091

    CAS  Google Scholar 

  • Kavitha C, Malarvizhi A, Senthil KS, 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  CAS  Google Scholar 

  • Kaya H, Aydınb F, Gürkanc M, Yılmaza S, Atesd M, Demire V, Arslan Z (2015) Effects of zinc oxide nanoparticles on bioaccumulation and oxidativestress in different organs of tilapia (Oreochromis niloticus). Environ Toxicol and Pharmacol 40:936–947

  • Kono Y, Fridovich I (1982) Superoxide radical inhibits catalase. J Biol Chem 257:5751–5754

    CAS  Google Scholar 

  • Lavanya S, Ramesh M, Kavitha C, Malarvizhi A (2011) Hematological, biochemical and ionoregulatory responses of Indian major carp Catla catla during chronic sub-lethal exposure to inorganic arsenic. Chemosphere 82:977–985

    Article  CAS  Google Scholar 

  • Lee GR, Foerster J, Lukens J, Paraskevas F, Greer JP, Rodgers GM (1999) Wintrobe’s clinical hematology 10th. Lippincott Williams and Wilkins, Bethseda, Maryland

    Google Scholar 

  • Lee RG, Foerster J, Jukens J, Paraskevas F, Greer JP, Rodgers GM (1998) Wintrobe’s clinical hematology, 10th edn. Lippincott Williams & Wilkins, New York, USA

    Google Scholar 

  • Livingstone DR (2001) Contaminant-stimulated reactive oxygen production and oxidative damage in aquatic organisms. Marine Poll Bull 42(8):656–666

    Article  CAS  Google Scholar 

  • Gagnon MM (2002) Metabolic enzymes as biochemical markers of effect following exposure of fish to sodium pentachlorophenate (Na-PCP). Bull Environ Contam Toxicol 69:570–575

    Article  Google Scholar 

  • Malarvizhi A, Kavitha C, Saravanan M, Ramesh M (2012) Carbamazepine (CBZ) induced enzymatic stress in gill, liver and muscle of a common carp, Cyprinus carpio. J King Saud Univ Sci 24:179–186

    Article  Google Scholar 

  • Manduzio MT, Rocher B, Leboulenger F, Galap C (2003) Characterization of inducible isoform of the Cu/Zn superoxide dismutase in the blue mussel Mytilus edulis. Aquat Toxicol 64:73–83

    Article  CAS  Google Scholar 

  • Ates M, Demir V, Arslan Z, Kaya H, Yılmaz S, Camas M (2016) Chronic exposure of tilapia (Oreochromis niloticus) to iron oxide nanoparticles: effects of particle morphology on accumulation, elimination, hematology and immune responses. Aquat Toxicol 177:22–32

    Article  CAS  Google Scholar 

  • Monteiro DA, Rantin FT, Kalinin AL (2010) Inorganic mercury exposure: toxicological effects, oxidative stress biomarkers and bioaccumulation in the tropical freshwater fish matrinxa, Brycon amazonicus (Spix and Agassiz, 1829). Ecotoxicology 19:105–123

    Article  CAS  Google Scholar 

  • Monteiro DA, Almeida JA, Rantin FT, Kalinin AL (2006) Oxidative stress biomarkers in the freshwater characid fish, Brycon cephalus, exposed to organophosphorus insecticide Folisuper 600 (methyl parathion). Comp Biochem Physiol C143:141–149

    Google Scholar 

  • Nelson DA, Morris MW (1989) Basic methodology. Hematology and coagulation, part IV. In: Nelson DA, Henry JB (eds) Clinical diagnosis and management by laboratory methods, 17th edn. Saunder Company, Philadelphia, pp 578–625 (Chapter 27)

    Google Scholar 

  • Oner M, Atli G, Canli M (2008) Changes in serum parameters of freshwater fish Oreochromis niloticus following prolonged metal (Ag, Cd, Cr, Cu, Zn) exposures. Environ Toxicol Chem 2:360–366

    Article  Google Scholar 

  • Owens CWI, Belcher RV (1965) A colorimetric micro-method for the determination of glutathione. Biochem J 94:705–711

    Article  CAS  Google Scholar 

  • Palaniappan PLRM, Vijayasundaram V (2009) The effect of arsenic exposure and the efficacy of DMSA on the proteins and lipids of the gill tissues of Labeo rohita. Food Chem Toxicol 47(8):1752–1759

    Article  CAS  Google Scholar 

  • Palanivelu V, Vijayavel K, Ezhilarasibalasubramanian S, Balasubramanian MP (2005) Influence of insecticidal derivative (Cartap Hydrochloride) from the marine polychaete on certain enzyme systems of the freshwater fish Oreochromis mossambicus. J Environ Biol 26:191–196

    CAS  Google Scholar 

  • Parvez S, Raisuddin S (2006) Effects of paraquat on the freshwater fish Channa punctata (Bloch): nonenzymatic antioxidants as biomarkers of exposure. Arch Environ Contam Toxicol 50(3):392-397.

  • Prousek J (2007) Fenton chemistry in biology and medicine. Pure Appl Chem 79:2325–2338

    Article  CAS  Google Scholar 

  • Ramesh M, Sankaran M, Veera-Gowtham V, Krishnan PR (2014) Hematological, biochemical and enzymological responses in an Indian major carp Labeo rohita induced by sublethal concentration of waterborne selenite exposure. Chem Biol Interact 207:67–73

    Article  CAS  Google Scholar 

  • Reddy SLN, Venugopal NBRK (1991) In vivo effects of cadmium chloride on certain aspects of protein metabolism in tissues of a freshwater field crab, Barytelphusa guerini. Bull Environ Contam Toxicology 46:583–590

    Article  CAS  Google Scholar 

  • Reitman S, Frankel S (1957) A colorimetric method for the determination of oxaloacetic acid glutamic pyruvic transaminase. Am J Clin Pathol 28:53–56

    Article  Google Scholar 

  • Remyla SR, Ramesh M, Sajwan KS, Kumar KS (2008) Influence of zinc on cadmium induced haematological and biochemical responses in a freshwater teleost fish Catla catla. Fish Physiol Biochem 34:169–174

    Article  CAS  Google Scholar 

  • Sathya V, Ramesh M, Poopal RK, Dinesh B (2012) Acute and sub lethal effects in an Indian major carp Cirrhinus mrigala exposed to silver nitrate: gill Na+/K+− ATPase, plasma electrolytes and biochemical alterations. Fish Shellfish Immunol 32(5):862–868

    Article  CAS  Google Scholar 

  • Sevcikova M, Modra H, Blahova J, Dobsikova R, Plhalova L, Zitka O, Hynek D, Kizek R, Skoric M, Svobodova Z (2016) Biochemical, haematological and oxidative stress responses of common carp (Cyprinus carpio L.) after sub-chronic exposure to copper. Vet Med 61(1):35–50

    Article  Google Scholar 

  • Shaheen T, Akhtar T (2012) Assessment of chromium toxicity in Cyprinus carpio through hematological and biochemical blood markers. Turk J Zool 36:682–690

    CAS  Google Scholar 

  • Speisky H, Gómez M, Burgos-Bravo F, López-Alarcón C, Jullian C, Olea-Azar C (2009) Generation of superoxide radicals by copper-glutathione complexes: redoxconsequences associated with their interaction with reduced glutathione. Bioorg Med Chem 17(5):1803–1810

    Article  CAS  Google Scholar 

  • Stevens ML (1997) Fundamentals of clinical hematology, Saunders Philadelphia, PA

  • Subha Rao P, Rajender K, (1990) Kinetics of aspartate amino transferase inhibition by certain insecticides in haemolymph of Periplaneta americana, J Environ Biol 11 (4) 383–387.

  • Tietz NW (1976) Fundamentals of clinical chemistry, Saunders, W.B., Co., Philadelphia, PA (p. 652).

  • Tort L, Puigcerver M, Crespo S, Padros F (2002) Cortisol and haematological response in sea bream and trout subjected to the anesthetics clove oil and 2-phenoxyethanol. Aquac Res 33:907–910

    Article  CAS  Google Scholar 

  • Tripathi S, Sahu DB, Kumar R, Kumar A (2003) Effect of acute exposure of sodium arsenite (Na3 Aso3) on some haematological parameters of Clarias batrachus (common Indian cat fish) in vivo. Indian J Environ Health 45:183–188

    CAS  Google Scholar 

  • Vutukuru SS, Suma Chintada K, Radha MJ, Venkateswara R, Anjaneyulu Y (2006) Acute effects of copper on superoxide dismutase, catalase and lipid peroxidation in the freshwater teleost fish, Esomus danricus. Fish Physiol Biochem 32:221–229

    Article  CAS  Google Scholar 

  • Wang J, Zhang W, Sun D, Song L, Li Y, Xu C (2012) Analysis of neuroglobin mRNA expression in rat brain due to arsenite-induced oxidative stress. Environ Toxicol 27(9):503–509

    Article  CAS  Google Scholar 

  • Wang T, Long X, Chen X, Liu Y, Liu Z, Han S, Yan S (2016) Integrated transcriptome, proteome and physiology analysis of Epinephelus coioides after exposure to copper nanoparticles or copper sulfate. Nanotoxicol 11(2):236–246

    Article  Google Scholar 

  • Witeska M, Kosciuk B (2003) Changes in common carp blood after short-term zinc exposure. Environ Sci Pollut Res 3:15–24

    Google Scholar 

  • Xiong D, Fang T, Yu L, Sima X, Zhu W (2011) Effects of nano-scale TiO2, ZnO and their bulk counterparts on zebra fish: acute toxicity, oxidative stress and oxidative damage. Sci Total Environ 409:1444–1452

    Article  CAS  Google Scholar 

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Acknowledgements

We are grateful to the Chabahar Maritime University of Iran for providing technical and financial facilities.

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Authors and Affiliations

  1. Department of Marine Sciences, Fisheries Group, Chabahar Maritime University, Chabahar, Iran

    Paria Akbary

  2. MSc of Environmental Department, Tonekabon Branch, Islamic Azad University (IAU), Tonekabon, Iran

    Sahar Sartipi Yarahmadi

  3. Department of Fishery, Faculty of Fisheries and Environment, Gorgan University of Agricultural Science and Natural Resources, Gorgan, Iran

    Abdolreza Jahanbakhshi

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  1. Paria Akbary
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Akbary, P., Sartipi Yarahmadi, S. & Jahanbakhshi, A. Hematological, hepatic enzymes’ activity and oxidative stress responses of gray mullet (Mugil cephalus) after sub-acute exposure to copper oxide. Environ Sci Pollut Res 25, 1800–1808 (2018). https://doi.org/10.1007/s11356-017-0582-1

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