Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
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Effects of antioxidant enzymes and bioaccumulation in eels (Anguilla japonica) by acute exposure of waterborne cadmium

  • Ahn, Tae-Young (Gyeonggi Province Maritime and Fisheries Research Institute) ;
  • Park, Hee-Ju (Department of Aquatic Life Medicine, Pukyong National University) ;
  • Kim, Jun-Hwan (National Institute of Fisheries Science, West Sea Fisheries Research Institute) ;
  • Kang, Ju-Chan (Department of Aquatic Life Medicine, Pukyong National University)
  • Received : 2020.05.15
  • Accepted : 2020.07.13
  • Published : 2020.08.31
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Abstract

This study was conducted to evaluate the acute effects of waterborne cadmium exposure on bioaccumulation and antioxidant enzymes in eels (Anguilla japonica) and to determine the median lethal concentration (LC50). Fish were exposed to different cadmium concentrations (0, 0.15, 0.30, 0.61, 1.83, 3.08, 3.67, 4.29, and 5.51 mg L-1) for 96 h. The LC50 of A. japonica to cadmium was 3.61 mg L-1. Cadmium accumulation generally increased in tissues with increasing waterborne cadmium concentrations. At ≥ 1.83 mg L-1 exposure, all tissues accumulated significant cadmium concentrations compared with the control group, in the order of kidney > liver > gill > spleen > muscle. Measurements of variation in actual cadmium concentrations showed that a reduction of the metal in experimental water was related to cadmium accumulation in tissues. As activity alteration of antioxidant enzymes for reactive oxygen species, superoxide dismutase and catalase activities increased at ≥ 0.61 mg L-1 significantly, glutathione peroxidase and glutathione S-transferase activities were not significantly changed. The results of this study suggest that acute exposure to waterborne cadmium is potentially fatal to A. japonica due to the metal's major accumulation in various tissues and the effect of antioxidant enzyme activity.

Keywords

References

  1. Adriano DC. Trace elements in terrestrial environments. New York: Springer; 2001. p. 867.
  2. Aldoghachi MAJ, Rahman MM, Yusoff I, Sofian-Azirun M. Acute toxicity and bioaccumulation of heavy metals in red tilapia fish. J Anim Plant Sci. 2016;26:507-13.
  3. Andaya AA, Gotopeng EU. Cadmium toxicity and uptake in Tilapia nilotica. Kalikasan. 1982;11:309-18.
  4. Atli G, Alptekin O, Tukel S, Canli M. Response of catalase activity to $Ag^+$, $Cd^{2+}$, $Cr^{6+}$, $Cu^{2+}$ and $Zn^{2+}$ in five tissues of freshwater fish Oreochromis niloticus. Comp Biochem Physiol Part C. 2006;143:218-24. https://doi.org/10.1016/j.cbpc.2006.02.003.
  5. Atli G, Canli M. Enzymatic responses to metal exposures in a freshwater fish Oreochromis niloticus. Comp Biochem Physiol Part C. 2007;145:282-7. https://doi.org/10.1016/j.cbpc.2006.12.012.
  6. Batool M, Abdullah S, Abbas K. Antioxidant enzymes activity during acute toxicity of chromium and cadmium to Channa marulius and Wallago attu. Pak J Agric Sci. 2014;51:1017-23.
  7. Bradford MM. A rapid and sensitive method for the quantitation of 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.
  8. Bryan GW. Some aspects of heavy metal tolerance in aquatic organisms. In: Lockwood APM, editor. Effects of Pollutants on Aquatic Organisms. London: Cambridge University Press; 1976. p. 7-35.
  9. Choi CY, An KW, Nelson ER, Habibi HR. Cadmium affects the expression of metallothionein (MT) and glutathione peroxidase (GPX) mRNA in goldfish, Carassius auratus. Comp Biochem Physiol Part C. 2007;145:595-600. https://doi.org/10.1016/j.cbpc.2007.02.007.
  10. Chowdhury MJ, Baldisserotto B, Wood CM. Tissue-specific cadmium and metallothionein levels in rainbow trout chronically acclimated to waterborne or dietary cadmium. Arch Environ Contam Toxicol. 2005;48:381-90. https://doi.org/10.1007/s00244-004-0068-2.
  11. Cicik B, Ay O, Karayakar F. Effects of lead and cadmium interactions on the metal accumulation in tissue and organs of the Nile tilapia (Oreochromis niloticus). Bull Environ Contam Toxicol. 2004;72:141-8. https://doi.org/10.1007/s00128-003-0252-5.
  12. Cirillo T, Amodio Cocchieri R, Fasano E, Lucisano A, Tafuri S, Ferrante MC, Carpene E, Andreani G, Isani G. Cadmium accumulation and antioxidant responses in Sparus aurata exposed to waterborne cadmium. Arch Environ Contam Toxicol. 2012;62:118-26. https://doi.org/10.1007/s00244-011-9676-9.
  13. Crupkin AC, Menone ML. Changes in the activities of glutathione-S-transferases, glutathione reductase and catalase after exposure to different concentrations of cadmium in Australoheros facetus (Cichlidae, Pisces). Ecotoxicol Environ Contam. 2013;8:21-5. https://doi.org/10.5132/eec.2013.01.003.
  14. Dabas A, Nagpure NS, Kumar R, Kushwaha B, Kumar P, LakraWS. Assessment of tissuespecific effect of cadmium on antioxidant defense system and lipid peroxidation in freshwater murrel, Channa punctatus. Fish Physiol Biochem. 2012;38:469-82. https://doi.org/10.1007/s10695-011-9527-7
  15. De Smet H, Blust R. Stress responses and changes in protein metabolism in carp Cyprinus carpio during cadmium exposure. Ecotoxicol Environ Saf. 2001;48:255-62. https://doi.org/10.1006/eesa.2000.2011
  16. Dudley RE, Klaassen CD. Changes in hepatic glutathione concentration modify cadmium-induced hepatotoxicity. Toxicol Appl Pharmacol. 1984;72:530-8. https://doi.org/10.1006/eesa.2000.2011.
  17. Farag AM, Stansburgh MA, Hogstrand C, MacConnell E, Bergman HL. The physiological impairment of free-ranging brown trout exposed to metals in the Clark Fork River, Montana. Can J Fish Aquat Sci. 1995;52:2038-50. https://doi.org/10.1139/f95-795.
  18. Gomes LC, Chippari-Gomes AR, Oss RN, Fernandes LFL, de Almedia Magris R. Acute toxicity of copper and cadmium for piaucu, Leporinus macrocephalus, and curimata, Prochilodus vimboides. Acta Sci Biol Sci. 2009;31:313-5. https://doi.org/10.4025/actascibiolsci.v31i3.5069.
  19. Hammond PB, Foulkes EC. Metal ion toxicity in man and animals. In: Sigel H, editor. Metal Ions in Biological Systems. New York: Marcel Deeker Inc.; 1986. p. 157-200.
  20. Handy RD. The assessment of episodic metal pollution. I. Use and limitation of tissue contaminant analysis in rainbow trout (Oncorhynchus mykiss) after short waterborne exposure to cadmium or copper. Arch Environ Contam Toxicol. 1992;22:74-81. https://doi.org/10.1007/BF00213304.
  21. Handy RD. The effect of acute exposure to dietary Cd and Cu on organ toxicant concentrations in rainbow trout, Oncorhynchus mykiss. Aquat Toxicol. 1993;27:1-14. https://doi.org/10.1016/0166-445X(93)90043-Z.
  22. Haux C, Larsson A. Long-term sublethal physiological effects on rainbow trout, Salmo gairdneri, during exposure to cadmium and after subsequent recovery. Aquat Toxicol. 1984;5:129-42. https://doi.org/10.1016/0166-445X(84)90004-3.
  23. Huang X, Feng Y, Fan W, Duan J, Duan Y, Xiong G, Wang K, Deng Y, Geng Y, Ouyang P, Chen D, Yang S. Potential ability for metallothionein and vitamin E protection against cadmium immunotoxicity in head kidney and spleen of grass carp (Ctenopharyngodon idellus). Ecotoxicol Environ Saf. 2019;170:246-52. https://doi.org/10.1016/j.ecoenv.2018.11.134.
  24. Javed M. Relationships among water, sediments and plankton for the uptake and accumulation of metals in the river Ravi. Indus J Plant Sci. 2003;2:326-31.
  25. Karaytug S, Sevgiler Y, Karayakar F. Comparison of the protective effects of antioxidant compounds in the liver and kidney of Cd- and Cr-exposed common carp. Environ Toxicol. 2011;29:129-37. https://doi.org/10.1002/tox.20779.
  26. Larsson A, Bengtsson BE, Haux C. Disturbed ion balance in flounder, Platichthys flesus L., exposed to sublethal levels of cadmium. Aquat Toxicol. 1981;1:19-35. https://doi.org/10.1016/0166-445X(81)90004-7.
  27. Lee SY, Bang IC, Nam YK. Molecular characterization of metallothionein gene of the Korean bitterling Acheilognathus signifier (cyprinidae). Kor J Ichthyol. 2011;23:10-20.
  28. Liu J, Qu W, Kadiiska MB. Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicol Appl Pharmacol. 2009;238:209-14. https://doi.org/10.1016/j.taap.2009.01.029.
  29. Livingstone DR. Oxidative stress in aquatic organisms in relation to pollution and aquaculture. Revue Med Vet. 2003;154:427-30.
  30. Mason CF. Biology of freshwater fishes. New York: Longman Scientific and Technical Publications; 1991. p. 315.
  31. Okorie OE, Bae JY, Lee JH, Lee SH, Park GH, Mohseni M, Bai SC. Effects of different dietary cadmium levels on growth and tissue cadmium content in juvenile parrotfish, Oplegnathus fasciatus. Asian-Australas J Anim Sci. 2014;27:62-8. https://doi.org/10.5713/ajas.2011.11222.
  32. Oz M. Effects of garlic (Allium sativum) supplemented fish diet on sensory, chemical and microbiological properties of rainbow trout during storage at $-18^{\circ}C$. LWT. 2018;92:155-60. https://doi.org/10.1016/j.lwt.2018.02.030.
  33. Oz M, Inanan BE, Dikel S. Effect of boric acid in rainbow trout (Oncorhynchus mykiss) growth performance. J Appl Anim Res. 2018;46:990-3. https://doi.org/10.1080/09712119.2018.1450258.
  34. Pannetier P, Caron A, Campbell PGC, Pierron F, Baudrimont M, Couture P. A comparison of metal concentrations in the tissues of yellow American eel (Anguilla rostrata) and European eel (Anguilla anguilla). Sci Total Environ. 2016;569-570:1435-45. https://doi.org/10.1016/j.scitotenv.2016.06.232.
  35. Pinot F, Kreps SE, Bachelet M, Hainaut P, Bakonyi M, Polla BS. Cadmium in the environment: sources, mechanisms of biotoxicity, and biomarkers. Rev Environ Health. 2000;15:299-323. https://doi.org/10.1515/REVEH.2000.15.3.299.
  36. Rand GM, Wells PG, McCarty LS. Fundamental of aquatic toxicology: effects, environmental fate and risk assessment. 2nd ed. Florida: Taylor & Francis; 1995. p. 1083.
  37. Rastgoo L, Alemzadeh A. Biochemical responses of Gouan (Aeluropus littoralis) to heavy metals stress. Aust J Crop Sci. 2011;5:375-83.
  38. Reddy SJ, Reddy DC. Impact of cadmium toxicity on behavioural and haematological biomarkers of freshwater fish, Catla catla. Int J Bioassays. 2013;2:1199-204.
  39. Rehwoldt R, Menapace LW, Nerrie B, Alessandrello D. The effect of increased temperature upon the acute toxicity of some heavy metal ions. Bull Environ Contam Toxicol. 1972;8:91-6. https://doi.org/10.1007/BF01684513.
  40. Romeo M, Bennani M, Gnassia-Barelli M, Lafaurie M, Girard JP. Cadmium and copper display different response towards oxidative stress in the kidney of the sea bass Dicentrarchus labrax. Aquat Toxicol. 2000;48:185-94. https://doi.org/10.1016/S0166-445X(99)00039-9.
  41. Safari R. Toxic effects of cadmium on antioxidant defense systems and lipid peroxidation in Acipenser persicus (Borodin, 1897). Int J Aquat Biol. 2015;3:425-32. https://doi.org/10.22034/ijab.v3i6.8.
  42. Saglam D, Atli G, Dogan Z, Baysoy E, Gurler C, Eroglu A. Response of the antioxidant system of freshwater fish (Oreochromis niloticus) exposed to metals (Cd, Cu) in differing hardness. Turk J Fish Aquat Sci. 2014;14:43-52. https://doi.org/10.4194/1303-2712-v14_1_06.
  43. Sampaio FG, Boijink CL, Oba ET, Santos LRB, Kalinin AL, Rantin FT. Antioxidant defenses and biochemical changes in pacu ( Piaractus mesopotamicus) in response to single and combined copper and hypoxia exposure. Comp Biochem Physiol Part C. 2008;147:43-51. https://doi.org/10.1016/j.cbpc.2012.07.002.
  44. Sangalang GB, Freeman HC. Tissue uptake of cadmium in brook trout during chronic sublethal exposure. Arch Environ Contam Toxicol. 1979;8:77-84. https://doi.org/10.1007/BF01055142.
  45. Schreck CB, Moyle PB. Methods for fish biology. Maryland: American Fisheries Society Bethesda; 1990. p. 694.
  46. Shuhaimi-Othman M, Yakub N, Ramle NA, Abas A. Comparative toxicity of eight metals on freshwater fish. Toxicol Ind Health. 2015;31:773-82. https://doi.org/10.1177/0748233712472519.
  47. Sjobeck M-L, Haux C, Larsson A, Lithner G. Biochemical and hematological studies on perch, Perca fluviatilis, from the cadmium contaminated river Eman. Ecotoxicol Environ Saf. 1984;8:303-12. https://doi.org/10.1016/0147-6513(84)90035-6.
  48. Souid G, Souayed N, Yaktiti F, Maaroufi K. Effect of acute cadmium exposure on metal accumulation and oxidative stress biomarkers of Sparus aurata. Ecotoxicol Environ Saf. 2013;89:1-7. https://doi.org/10.1016/j.ecoenv.2012.12.015.
  49. Verbost PM, Flik G, Lock RAC, Wendelaar Bonga SE. Cadmium inhibition of $Ca^{2+}$ uptake in rainbow trout gills. Am J Phys. 1987;253:216-21. https://doi.org/10.1152/ajpregu.1987.253.2.R216.
  50. Verbost PM, Flik G, Lock RAC, Wendelaar Bonga SE. Cadmium inhibits plasma membrane calcium transport. J Membr Biol. 1988;102:97-104. https://doi.org/10.1007/BF01870448.
  51. Verbost PM, van Roij J, Flik G, Lock RAC, Wendelaar Bonga SE. The movement of cadmium through freshwater trout branchial epithelium and its interference with calcium transport. J Exp Biol. 1989;145:185-97. https://doi.org/10.1242/jeb.145.1.185
  52. Vinodhini R, Narayanan M. Bioaccumulation of heavy metals in organs of fresh water fish Cyprinus carpio (Common carp). Int J Environ Sci Technol. 2008;5:179-82. https://doi.org/10.1007/BF03326011.
  53. Woo PTK, Sun YM, Wong MK. The effects of short-term acute cadmium exposure on blue tilapia, Oreochromis aureus. Environ Biol Fish. 1993;37:67-74. https://doi.org/10.1007/BF00000714.
  54. Yang HN, Chen HC. Uptake and elimination of cadmium by Japanese eel, Anguilla japonica, at various temperatures. Bull Environ Contam Toxicol. 1996;56:670-6. https://doi.org/10.1007/s001289900098.
  55. Yilmaz M, Gul A, Karakose E. Investigation of acute toxicity and the effect of cadmium chloride ($CdCl_2{\cdot}H_2O$) metal salt on behavior of the guppy (Poecilia reticulata). Chemosphere. 2004;56:375-80. https://doi.org/10.1016/j.chemosphere.2003.11.067.

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