Role of effective microorganisms on hematological and biochemical indices of cultured Oreochromis niloticus exposed to lead, copper, and cadmium under temperature variations

Ragab G. Abdel Salam; Samah M. Bassem; Eman Salah Abdel-Reheim; Mahmoud Abdel-Latif; Giulia Guerriero; Fagr Kh Abdel-Gawad

doi:10.7324/JABB.2023.110222

Abstract References Article Metrics Similar Articles Request Permission Related Search Citation Alert By Google Scholar Comment On This Article

Abstract

The freshwater environment suffers from a combination of stressors; pollution and global warming. Multiple effects of copper sulfate [CuSO4], cadmium chloride [CdCl2], and lead nitrate Pb [NO3]2 were studied on Nile tilapia under three temperatures ranges, compared to bioremediation using effective microorganisms (EMs). The fish were divided into eight groups, with each group exposed to three temperatures (24, 28, and 32°C). Water physicochemical parameters were measured, and fish hematological, physiological, and biochemical changes were considered. Water quality parameters revealed a significant increase in both electrical conductivity and total dissolved solids in the EM/Cu fish group in the Cu fish group at 32°C. The chemical oxygen demand levels indicated a remarkable fluctuation with a slight decrease in the control group (at 28°C) while reduced in the control and EM. The results were highly significant incomplete blood cells, total red blood cell count, hemoglobin concentration (Hb), hematocrit, mean corpuscular Hb, mean corpuscular Hb concentration, and total protein (g/dl) in the EM group and control group. It can be concluded that using EM in fish farms (1:1000) could help fish adapt to different temperatures and reduce the effects of toxic pollutants.

Keyword: Effective microorganisms Hematological – biochemical indices Oreochromis niloticus Climate change

Citation:

Salam RGA, Bassem SM, Abdel-Reheim ES, Abdel-Latif M, Guerriero G, Abdel-Gawad FK. Role of effective microorganisms on hematological and biochemical indices of cultured Oreochromis niloticus exposed to lead, copper, and cadmium under temperature variations. J App Biol Biotech. 2023;11(1):153-160. https://doi.org/10.7324/JABB.2023.110222

Copyright: Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike license.

HTML Full Text

Reference

1. Food and Agriculture Organization. The State of World Fisheries and Aquaculture. Food and Agriculture Organization of the United Nations, Rome, Italy: Food and Agriculture Organization; 2018. p. 227.
2. Snapin S, Shyam KU, Meemetta W, Rattanarojpong T, Dong HT. Inapparent infection cases of tilapia lake virus (TiLV) in farmed tilapia. Aquaculture 2018;487:51-5.https://doi.org/10.1016/j.aquaculture.2018.01.007
3. Aaen SM, Helgesen KO, Bakke MJ, Kaur K, Horsberg TE. Drug resistance in sea lice: A threat to salmonid aquaculture. Trends Parasitol 2015;31:72-81.https://doi.org/10.1016/j.pt.2014.12.006
4. Jobling M. Fish nutrition research: Past, present and future. Aquac Int 2016;24:767-86.https://doi.org/10.1007/s10499-014-9875-2
5. Dawood MA, Koshio S. Recent advances in the role of probiotics and prebiotics in carp aquaculture. Rev Aquac 2016;454:243-51.https://doi.org/10.1016/j.aquaculture.2015.12.033
6. Zhou Q, Li K, Jun X, Bo L. Role and functions of beneficial microorganisms in sustainable aquaculture. Bioresour Technol 2009;100:3780-6.https://doi.org/10.1016/j.biortech.2008.12.037
7. Langston WJ. Toxic effects of metals and the incidence of the marine ecosystem. In: Plmess RW, Rainbow PS, editors. Heavy Metals in the Marine Environment. New York: CAC Press; 1990. p. 256.
8. KraaK MH, Wink YA, Stuijzand SC, Buckert-De Jong MC, De Groot CJ, Admiraal W. Chronic ecotoxicity of Zn and Pb to the zebra mussel Dreissena polymorpha. Aquatic Toxicol 1994;30:77-89.https://doi.org/10.1016/0166-445X(94)90007-8
9. Soliman MF, El-Shenawy NS, Ghobashy MA. Parasitology aspects and biochemical changes of infected cultured Tilapia (Oreochromis hybrid). Acta Ichthyol Piscatorial 2004;34:21-32.https://doi.org/10.3750/AIP2004.34.1.03
10. Canli M, Erdem C. Mercury toxicity and effects of exposure concentration and period on mercury accumulation in tissues of a tropical fish Tilapia nilotica (L). Tr J Zool 1994;I:233-9.
11. American Public Health Association. Standard Methods for the Examination of Water and Wastewater. 22nd ed. Washington, DC: APHA, AWWA and WEF; 2012.
12. Litchfield JR, Wilcoxon F. A simplified method of evaluating dose-effect experiments. J Pharmacol Exp Ther 1949;96:99-113.
13. Alkobaby AI, Abd El-Wahed RK. The acute toxicity of copper to Nile tilapia (Oreochromis niloticus) fingerlings and its effects on gill and liver histology. J Aquac Res Dev 2017;8:465.https://doi.org/10.4172/2155-9546.1000465
14. Garcia-Santos S, Fontaínhas-Fernandes A, Wilson JM. Cadmium tolerance in the Nile tilapia (Oreochromis niloticus) following acute exposure: Assessment of some ionoregulatory parameters. Environ Toxicol 2006;21:33-46.https://doi.org/10.1002/tox.20152
15. Ullah A, Hameed U, Alam Z, Ziafat R, Saeed A, Mujaddad U, et al. Determination of 96-Hr LC50 of lead nitrate for a fish, Oreochromis niloticus. J Entomol Zool Stud 2016;4:1216-8.
16. Bradford MM. Rapid and sensitive method for quantitating microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-54.https://doi.org/10.1016/0003-2697(76)90527-3
17. Reitman S, Frankel SA. A colourimetric method for determining serum glutamic oxaloacetic and glutamic pyruvic transaminases. Am J Clin Pathol 1957;28:56-63.https://doi.org/10.1093/ajcp/28.1.56
18. Henry RJ, Cannon DC, Winkelman JW. Clinical Chemistry, Principles and Techniques. 2nd ed. New York, USA: Harper and Row; 1974. p. 541-53.
19. Barham D, Trinder P. Enzymatic determination of uric acid. Analyst 1972;97:142-5.https://doi.org/10.1039/an9729700142
20. Selma K, Hatice P. The effects of pollution on haematological parameters of black goby (Gobius niger L., 1758) in Foca and Aliaga Bays, Turkey. EU J Fish Aquat Sci 2004;21:113-7.
21. Dacie SJ, Lewis SM. Practical Haematology. 11th ed. United Kingdom: Churchill Livingstone; 2002.
22. Statistical Analysis System. SAS/STAT User's Guide, Version 9.1. Cary, NC, USA: SAS Institute Inc.; 2006.
23. Steel RG, Torrie JH. Principles and Procedures of Statistics: A Biometrical Approach. 2nd ed. New York, USA: McGraw-Hill Inc.; 1980. p. 633.
24. Gupta P, Saxena KK. Biochemical and haematological studies in freshwater fish Channa punctatus exposed to synthetic pyrethroids. Pollut Res 2006;25:499-502.
25. Hued AC, Bistoni MA. Development and validation of a biotic index for evaluation of environmental quality in the central region of Argentina. Hydrobiologia 2005;543:279-98.https://doi.org/10.1007/s10750-004-7893-1
26. Guezgouz N, Costantino P, Boubsil S, Gaetano G, Hana SA, Guerriero G. Heavy metals assessment in the Medjerda river basin (Northeastern Algeria): A preliminary water analysis and toad skin biopsy. Proc Zool Soc 2020;74:104-13.https://doi.org/10.1007/s12595-020-00342-6
27. American Public Health Association. Standard Methods for the Examination of Water and Wastewater. 20th ed. Washington, DC: APHA; 2005. p. 1193-2950.
28. Gupta A, Rai DK, Pandey RS, Sharma B. Analysis of some heavy metals in the riverine water, sediments and fish from river Ganges at Allahabad. Environ Monit Assess 2009;157:449-58.https://doi.org/10.1007/s10661-008-0547-4
29. El-Sayed AF. Tilapia Culture in Salt Water: Environmental Requirements, Nutritional Implications and Economic Potentials. 8th Simposium Internacional de Nutricion Acuicola. Monterrey: Universidad Autonoma de Nuevo Leon Anais Monterrey; 2006.
30. Osman AG, Kloas W. Water quality and heavy metal monitoring in water, sediments, and tissues of the African catfish Clarias gariepinus (Burchell, 1822) from the River Nile, Egypt. J Environ Protec 2010;1:389-400.https://doi.org/10.4236/jep.2010.14045
31. F?rat Ö, Karg?n F. Response of Cyprinus carpio to copper exposure: Alterations in reduced glutathione, catalase and proteins electrophoretic patterns. Fish Physiol Biochem 2010;36:1021-8.https://doi.org/10.1007/s10695-010-9380-0
32. Mercaldo-Allen R, Dawson MA, Kuropat CA, Kapareiko D. Variability in the Blood Chemistry of Yellowtail Flounder, Limanda ferruginea, with Regard to Sex, Season, and Geographic Location. NOAA Technical Memorandum NMFS-NE-180; 2003.
33. Mallesh B, Pandey PK, Kumar K, Vennila A, Kumar S. Bioconcentration
of hexavalent chromium in Cirrhinus mrigala (Ham 1822): Effect on haematological parameters. J Bio Earth Sci 2015;5:59-67.
34. Shahjahan M, Uddin MH, Bain V, Haque MM. Increased water temperature altered hemato-biochemical parameters and structure of peripheral erythrocytes in striped catfish Pangasianodon hypophthalmus. Fish Physiol Biochem 2018;44:1309-18.https://doi.org/10.1007/s10695-018-0522-0
35. Hrubec TC, Cardinale JL, Smith SA. Hematology and plasma chemistry reference intervals for cultured Tilapia (Oreochromis hybrid). Vet Clin Pathol 2000;29:7-12.https://doi.org/10.1111/j.1939-165X.2000.tb00389.x
36. Coles EH. Veterinary Clinical Pathology. Philadelphia, PA: WB Saunders; 1986. p. 10-42.
37. O'Connor DV, Fromm PO. The effect of methyl mercury on gill metabolism and blood parameters of rainbow trout. Bull Environ Contam Toxicol 1975;13:406-11.https://doi.org/10.1007/BF01721843
38. Çiftçi1 N, Karayakar F, Ay Ö, Click B, Erdem C. Effects of copper and lead on some haematological parameters of Oreochromis niloticus. Fresenius Environ Bull 2015;24:2771-5.
39. Al-Asgah NA, Abdel-Warith AA, Younis EM, Allam HY. Haematological and biochemical parameters and tissue accumulations of cadmium in Oreochromis niloticus exposed to various concentrations of cadmium chloride. Saudi J Biol Sci 2015;22:543-50.https://doi.org/10.1016/j.sjbs.2015.01.002
40. Shahi J, Singh A. Genotoxic and haematological effect of commonly used fungicide on fish Clarias batracus. J Biol Earth Sci 2014;4:B137-43.
41. Kotsanis N, Iliopoulou-Georgudaki J, Kapata-Zoumbos K. Changes in selected haematological parameters at early stages of the rainbow trout, Oncorhynchus mykiss, subjected to metal toxicants: Arsenic, cadmium and mercury. J Appl Ichthyol 2000;16:276-8.https://doi.org/10.1046/j.1439-0426.2000.00163.x
42. Datta S, Ghosh D, Saha DR, Bhattacharaya S, Mazumder S. Chronic exposure to low concentration of arsenic is immunotoxic to fish: Role of head kidney macrophages as biomarkers of arsenic toxicity to Clarias batrachus. Aquat Toxicol 2009;92: 86-94.https://doi.org/10.1016/j.aquatox.2009.01.002
43. Shalaby AM. Biochemical and Physiological Studies on Metal Contamination in the Common Carp (Cyprinus carpio L). Ph. D.Thesis, Zagazig University: Faculty of Science, Benha Branch; 1997. p. 268.
44. Yamawaki K, Hashimoto W, Fujii K, Koyama J, Ikeda Y, Ozaki H. Hemochemical changes in carp (Cyprinus carpio) exposed to low cadmium concentrations. Nippon Suisan Gakkaishi Bull 1986;52:459-66.https://doi.org/10.2331/suisan.52.459
45. Chen CY, Wooster GA, Getchell RG, Bowser PA, Timmons MB. Blood chemistry of healthy, nephrocalcinosis-affected and ozone-treated tilapia in a recirculating system, with application of discriminant analysis. Aquaculture 2003;218:89-102.https://doi.org/10.1016/S0044-8486(02)00499-4
46. Öner M, Atli G, Canli M. Effects of metal (Ag, Cd, Cr, Cu, Zn) exposures on some enzymatic and non-enzymatic indicators in the liver of Oreochromis niloticus. Bull Environ Contam Toxicol 2009;82:317-21.https://doi.org/10.1007/s00128-008-9577-4
47. Mensinger AF, Walsh PJ, Hanlon RT. Blood biochemistry of the oyster toadfish. J Aquat Anim Health 2005;17:170-6.https://doi.org/10.1577/H04-021.1
48. Abdel-Tawwab M, Wafeek M. Evaluation of the response of Nile tilapia, Oreochromis niloticus (L.) to environmental cadmium toxicity during organic selenium supplementation. World Aquacult Soci 2010;41:106-14.https://doi.org/10.1111/j.1749-7345.2009.00317.x
49. Yousuf R, Mir SH, Tanveer S, Chishti MZ, Darzi MM, Mir MS. Comparative biochemical evaluation of Schizothorax niger and Cyprinus carpio from River Jhelum of Kashmir Valley. Res J Pharm Biol Chem Sci 2012;3:116-31.

Article Metrics

59 Views 65 Downloads 124 Total

Year

Month

Related Search

By author names

Salam R G A [PubMed] [Google Scholar ]

Bassem S M [PubMed] [Google Scholar ]

Abdel-Reheim E S [PubMed] [Google Scholar ]

Abdel-Latif M [PubMed] [Google Scholar ]

Guerriero G [PubMed] [Google Scholar ]

Abdel-Gawad F K [PubMed] [Google Scholar ]

By article title

1. Food and Agriculture Organization. The State of World Fisheries and Aquaculture. Food and Agriculture Organization of the United Nations, Rome, Italy: Food and Agriculture Organization; 2018. p. 227.

2. Snapin S, Shyam KU, Meemetta W, Rattanarojpong T, Dong HT. Inapparent infection cases of tilapia lake virus (TiLV) in farmed tilapia. Aquaculture 2018;487:51-5.https://doi.org/10.1016/j.aquaculture.2018.01.007

3. Aaen SM, Helgesen KO, Bakke MJ, Kaur K, Horsberg TE. Drug resistance in sea lice: A threat to salmonid aquaculture. Trends Parasitol 2015;31:72-81.https://doi.org/10.1016/j.pt.2014.12.006

4. Jobling M. Fish nutrition research: Past, present and future. Aquac Int 2016;24:767-86.https://doi.org/10.1007/s10499-014-9875-2

5. Dawood MA, Koshio S. Recent advances in the role of probiotics and prebiotics in carp aquaculture. Rev Aquac 2016;454:243-51.https://doi.org/10.1016/j.aquaculture.2015.12.033

6. Zhou Q, Li K, Jun X, Bo L. Role and functions of beneficial microorganisms in sustainable aquaculture. Bioresour Technol 2009;100:3780-6.https://doi.org/10.1016/j.biortech.2008.12.037

7. Langston WJ. Toxic effects of metals and the incidence of the marine ecosystem. In: Plmess RW, Rainbow PS, editors. Heavy Metals in the Marine Environment. New York: CAC Press; 1990. p. 256.

8. KraaK MH, Wink YA, Stuijzand SC, Buckert-De Jong MC, De Groot CJ, Admiraal W. Chronic ecotoxicity of Zn and Pb to the zebra mussel Dreissena polymorpha. Aquatic Toxicol 1994;30:77-89.https://doi.org/10.1016/0166-445X(94)90007-8

9. Soliman MF, El-Shenawy NS, Ghobashy MA. Parasitology aspects and biochemical changes of infected cultured Tilapia (Oreochromis hybrid). Acta Ichthyol Piscatorial 2004;34:21-32.https://doi.org/10.3750/AIP2004.34.1.03

10. Canli M, Erdem C. Mercury toxicity and effects of exposure concentration and period on mercury accumulation in tissues of a tropical fish Tilapia nilotica (L). Tr J Zool 1994;I:233-9.

11. American Public Health Association. Standard Methods for the Examination of Water and Wastewater. 22nd ed. Washington, DC: APHA, AWWA and WEF; 2012.

12. Litchfield JR, Wilcoxon F. A simplified method of evaluating dose-effect experiments. J Pharmacol Exp Ther 1949;96:99-113.

13. Alkobaby AI, Abd El-Wahed RK. The acute toxicity of copper to Nile tilapia (Oreochromis niloticus) fingerlings and its effects on gill and liver histology. J Aquac Res Dev 2017;8:465.https://doi.org/10.4172/2155-9546.1000465

14. Garcia-Santos S, Fontaínhas-Fernandes A, Wilson JM. Cadmium tolerance in the Nile tilapia (Oreochromis niloticus) following acute exposure: Assessment of some ionoregulatory parameters. Environ Toxicol 2006;21:33-46.https://doi.org/10.1002/tox.20152

15. Ullah A, Hameed U, Alam Z, Ziafat R, Saeed A, Mujaddad U, et al. Determination of 96-Hr LC50 of lead nitrate for a fish, Oreochromis niloticus. J Entomol Zool Stud 2016;4:1216-8.

16. Bradford MM. Rapid and sensitive method for quantitating microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-54.https://doi.org/10.1016/0003-2697(76)90527-3

17. Reitman S, Frankel SA. A colourimetric method for determining serum glutamic oxaloacetic and glutamic pyruvic transaminases. Am J Clin Pathol 1957;28:56-63.https://doi.org/10.1093/ajcp/28.1.56

18. Henry RJ, Cannon DC, Winkelman JW. Clinical Chemistry, Principles and Techniques. 2nd ed. New York, USA: Harper and Row; 1974. p. 541-53.

19. Barham D, Trinder P. Enzymatic determination of uric acid. Analyst 1972;97:142-5.https://doi.org/10.1039/an9729700142

20. Selma K, Hatice P. The effects of pollution on haematological parameters of black goby (Gobius niger L., 1758) in Foca and Aliaga Bays, Turkey. EU J Fish Aquat Sci 2004;21:113-7.

21. Dacie SJ, Lewis SM. Practical Haematology. 11th ed. United Kingdom: Churchill Livingstone; 2002.

22. Statistical Analysis System. SAS/STAT User's Guide, Version 9.1. Cary, NC, USA: SAS Institute Inc.; 2006.

23. Steel RG, Torrie JH. Principles and Procedures of Statistics: A Biometrical Approach. 2nd ed. New York, USA: McGraw-Hill Inc.; 1980. p. 633.

24. Gupta P, Saxena KK. Biochemical and haematological studies in freshwater fish Channa punctatus exposed to synthetic pyrethroids. Pollut Res 2006;25:499-502.

25. Hued AC, Bistoni MA. Development and validation of a biotic index for evaluation of environmental quality in the central region of Argentina. Hydrobiologia 2005;543:279-98.https://doi.org/10.1007/s10750-004-7893-1

26. Guezgouz N, Costantino P, Boubsil S, Gaetano G, Hana SA, Guerriero G. Heavy metals assessment in the Medjerda river basin (Northeastern Algeria): A preliminary water analysis and toad skin biopsy. Proc Zool Soc 2020;74:104-13.https://doi.org/10.1007/s12595-020-00342-6

27. American Public Health Association. Standard Methods for the Examination of Water and Wastewater. 20th ed. Washington, DC: APHA; 2005. p. 1193-2950.

28. Gupta A, Rai DK, Pandey RS, Sharma B. Analysis of some heavy metals in the riverine water, sediments and fish from river Ganges at Allahabad. Environ Monit Assess 2009;157:449-58.https://doi.org/10.1007/s10661-008-0547-4

29. El-Sayed AF. Tilapia Culture in Salt Water: Environmental Requirements, Nutritional Implications and Economic Potentials. 8th Simposium Internacional de Nutricion Acuicola. Monterrey: Universidad Autonoma de Nuevo Leon Anais Monterrey; 2006.

30. Osman AG, Kloas W. Water quality and heavy metal monitoring in water, sediments, and tissues of the African catfish Clarias gariepinus (Burchell, 1822) from the River Nile, Egypt. J Environ Protec 2010;1:389-400.https://doi.org/10.4236/jep.2010.14045

31. F?rat Ö, Karg?n F. Response of Cyprinus carpio to copper exposure: Alterations in reduced glutathione, catalase and proteins electrophoretic patterns. Fish Physiol Biochem 2010;36:1021-8.https://doi.org/10.1007/s10695-010-9380-0

32. Mercaldo-Allen R, Dawson MA, Kuropat CA, Kapareiko D. Variability in the Blood Chemistry of Yellowtail Flounder, Limanda ferruginea, with Regard to Sex, Season, and Geographic Location. NOAA Technical Memorandum NMFS-NE-180; 2003.

33. Mallesh B, Pandey PK, Kumar K, Vennila A, Kumar S. Bioconcentration

of hexavalent chromium in Cirrhinus mrigala (Ham 1822): Effect on haematological parameters. J Bio Earth Sci 2015;5:59-67.

34. Shahjahan M, Uddin MH, Bain V, Haque MM. Increased water temperature altered hemato-biochemical parameters and structure of peripheral erythrocytes in striped catfish Pangasianodon hypophthalmus. Fish Physiol Biochem 2018;44:1309-18.https://doi.org/10.1007/s10695-018-0522-0

35. Hrubec TC, Cardinale JL, Smith SA. Hematology and plasma chemistry reference intervals for cultured Tilapia (Oreochromis hybrid). Vet Clin Pathol 2000;29:7-12.https://doi.org/10.1111/j.1939-165X.2000.tb00389.x

36. Coles EH. Veterinary Clinical Pathology. Philadelphia, PA: WB Saunders; 1986. p. 10-42.

37. O'Connor DV, Fromm PO. The effect of methyl mercury on gill metabolism and blood parameters of rainbow trout. Bull Environ Contam Toxicol 1975;13:406-11.https://doi.org/10.1007/BF01721843

38. Çiftçi1 N, Karayakar F, Ay Ö, Click B, Erdem C. Effects of copper and lead on some haematological parameters of Oreochromis niloticus. Fresenius Environ Bull 2015;24:2771-5.

39. Al-Asgah NA, Abdel-Warith AA, Younis EM, Allam HY. Haematological and biochemical parameters and tissue accumulations of cadmium in Oreochromis niloticus exposed to various concentrations of cadmium chloride. Saudi J Biol Sci 2015;22:543-50.https://doi.org/10.1016/j.sjbs.2015.01.002

40. Shahi J, Singh A. Genotoxic and haematological effect of commonly used fungicide on fish Clarias batracus. J Biol Earth Sci 2014;4:B137-43.

41. Kotsanis N, Iliopoulou-Georgudaki J, Kapata-Zoumbos K. Changes in selected haematological parameters at early stages of the rainbow trout, Oncorhynchus mykiss, subjected to metal toxicants: Arsenic, cadmium and mercury. J Appl Ichthyol 2000;16:276-8.https://doi.org/10.1046/j.1439-0426.2000.00163.x

42. Datta S, Ghosh D, Saha DR, Bhattacharaya S, Mazumder S. Chronic exposure to low concentration of arsenic is immunotoxic to fish: Role of head kidney macrophages as biomarkers of arsenic toxicity to Clarias batrachus. Aquat Toxicol 2009;92: 86-94.https://doi.org/10.1016/j.aquatox.2009.01.002

43. Shalaby AM. Biochemical and Physiological Studies on Metal Contamination in the Common Carp (Cyprinus carpio L). Ph. D.Thesis, Zagazig University: Faculty of Science, Benha Branch; 1997. p. 268.

44. Yamawaki K, Hashimoto W, Fujii K, Koyama J, Ikeda Y, Ozaki H. Hemochemical changes in carp (Cyprinus carpio) exposed to low cadmium concentrations. Nippon Suisan Gakkaishi Bull 1986;52:459-66.https://doi.org/10.2331/suisan.52.459

45. Chen CY, Wooster GA, Getchell RG, Bowser PA, Timmons MB. Blood chemistry of healthy, nephrocalcinosis-affected and ozone-treated tilapia in a recirculating system, with application of discriminant analysis. Aquaculture 2003;218:89-102.https://doi.org/10.1016/S0044-8486(02)00499-4

46. Öner M, Atli G, Canli M. Effects of metal (Ag, Cd, Cr, Cu, Zn) exposures on some enzymatic and non-enzymatic indicators in the liver of Oreochromis niloticus. Bull Environ Contam Toxicol 2009;82:317-21.https://doi.org/10.1007/s00128-008-9577-4

47. Mensinger AF, Walsh PJ, Hanlon RT. Blood biochemistry of the oyster toadfish. J Aquat Anim Health 2005;17:170-6.https://doi.org/10.1577/H04-021.1

48. Abdel-Tawwab M, Wafeek M. Evaluation of the response of Nile tilapia, Oreochromis niloticus (L.) to environmental cadmium toxicity during organic selenium supplementation. World Aquacult Soci 2010;41:106-14.https://doi.org/10.1111/j.1749-7345.2009.00317.x

49. Yousuf R, Mir SH, Tanveer S, Chishti MZ, Darzi MM, Mir MS. Comparative biochemical evaluation of Schizothorax niger and Cyprinus carpio from River Jhelum of Kashmir Valley. Res J Pharm Biol Chem Sci 2012;3:116-31.