Sains Malaysiana 45(1)(2016): 119–127

Bioaccumulation and Histopathological Changes induced by Toxicity of Mercury (HgCl₂) to Tilapia Fish Oreochromis niloticus  

(Perubahan Bioakumulasi dan Histopatologi Teraruh oleh Ketoksikan Merkuri (HgCl₂) pada Ikan Tilapia Oreochromis niloticus)

 

MOHAMMED A. JASIM¹, MOHD SOFIAN-AZIRUN¹, YUSOFF, I..² & M. MOTIOR RAHMAN¹*

 

¹Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603 Kuala Lumpur, Wilayah Persekutuan, Malaysia

 

²Department of Geology, Faculty of Science, University of Malaya, 50603 Kuala Lumpur, Wilayah Persekutuan, Malaysia

 

Received: 8 July 2014/Accepted: 24 November 2014

 

ABSTRACT

In this paper we have studied the acute toxicity effect of Hg on hybrid tilapia (Oreochromis niloticus). For this, the tissues of tilapia have been digested by means of acids in microwave oven and was analyzed by flameless atomic absorption spectrophotometer (FAAS). We have identified that the levels of Hg varied significantly in different tissues and the metal concentration was in the following order: liver > gills > muscles; of which the maximum level recorded for Hg was 0.799 mg/kg. We have also observed the alterations towards histopathological aspects in the gills and liver of treated fishes were studied using light and electron microscopy, subjected to the exposure of Hg for 24 h and furthermore we have also noticed the extent of the increased alterations during the 96 h of exposure to median lethal concentration LC₅₀ (0.3 mg/L) a severe disorganization of epithelial cells and modifications of the structure of the secondary lamellae. Moreover the severity has also found to increase to sub-lethal concentration (0.03 mgHg/L) in 21 days of exposure; Liver was slightly affected by the contamination of Hg. Ultimately, histopathology is considered as a sensitive technique of bioaccumulation and for the observing the potential damage from Hg exposure.

 

Keywords: Acute exposure; bioaccumulation; histopathology; Mercury; Oreochromis niloticus

 

 

ABSTRAK

Dalam penyelidikan ini, kami mengkaji kesan ketoksikan akut Hg pada tilapia hibrid (Oreochromis niloticus). Tisu tilapia telah dicerna menggunakan asid di dalam ketuhar gelombang mikro dan telah dianalisis menggunakan spektrofotometer atom serapan tidak bernyala (FAAS). Kami telah mengenal pasti bahawa, paras Hg berubah dengan ketara dalam tisu yang berbeza dan susunan kepekatan logam adalah seperti berikut: hati> insang> otot; dengan paras maksimum Hg yang direkodkan adalah 0.799 mg/kg. Kami juga dapati perubahan terhadap aspek histopatologi dalam insang dan hati ikan terawat dan kajian dijalankan menggunakan mikroskop cahaya dan elektron, tertakluk kepada pendedahan Hg selama 24 jam. Kami turut mengenal pasti peningkatan perubahan semasa 96 jam pendedahan terhadap kepekatan maut LC₅₀ (0.3 mg/L) ketidakaturan sel-sel epitelium yang rosak dan pengubahsuaian struktur lamela sekunder, kerosakan teruk juga berlaku pada kepekatan sub-maut (0.03 mgHg/L) dalam masa 21 hari pendedahan; kesan pencemaran Hg terhadap hati hanya sedikit sahaja. Histopatologi dianggap sebagai teknik yang sensitif bagi bioakumulasi dan pemerhatian terhadap potensi kerosakan akibat pendedahan Hg.

 

Kata kunci: Bioakumulasi; histopatologi; Merkuri; Oreochromis niloticus; pendedahan akut

 

REFERENCES

Adams, D.H. & Sonne, C. 2013. Mercury and histopathology of the vulnerable goliath grouper, Epinephelus itajara, in U.S. waters: A multi-tissue approach. Environmental Research 126: 254-263.

Ahmed, Q., Yousuf, F., Sarfraz, M., Mohammad, Q.A., Balkhour, M., Safi, S.Z. & Ashraf, M.A. 2015. Euthynnus affinis (little tuna): Fishery, bionomics, seasonal elemental variations, health risk assessment and conservational management. Frontiers in Life Science 8(1): 71-96.

Ahmed, Q., Yousuf, F., Sarfraz, M., Bakar, N.K.A., Balkhour, M.A. & Ashraf, M.A. 2014. Seasonal elemental variations of Fe, Mn, Cu and Zn and conservational management of Rastrelliger kanagurta fish from Karachi fish harbour, Pakistan. Journal of Food, Agriculture and Environment 12(3&4): 405-414.

Alhashemi, A.H., Karbassi, A., Kiabi, B.H., Monavari, S.M. & Sekhavatjou, M.S. 2012. Bioaccumulation of trace elements in different tissues of three commonly available fish species regarding their gender, gonadosomatic index, and condition factor in a wetland ecosystem. Environmental Monitoring and Assessment 184: 1865-1878.

AOAC 1995. Official Methods of Analysis of AOAC. 16th ed. Rockville: AOAC International.

APHA; AWWA; WPCF. 1998. Standard Methods for the Examination of Water and Waste Water. 20th ed. Washington, D.C.: APHA – American Public Health Association; AWWA-American Water Works Association; WPCF- Water Pollution Control Federation. p. 140.

Ashraf, M.A., Maah, M.J. & Yusoff, I. 2012. Bioaccumulation of heavy metals in fish species collected from former tin mining catchment. International Journal of Environmental Research 6(1): 209-218.

Ashraf, M.A., Maah, M.J. & Yusoff, I. 2011. Assessment of heavy metals in the fish samples of mined out ponds Bestari Jaya, Peninsular Malaysia. Proceedings of the Indian National Science Academy 77(1): 57-67.

Agency for Toxic Substances & Disease Registry (ATSDR). 2004. Hazardous substances emergency events surveillance. Division of health studies surveillance and registries branch Atlanta, Georgia. http://www.atsdr.cdc.gov/HS/HSEES.

Buhl, K.J. 1997. Relative sensitivity of three endangered fishes, Colorado Squawd fish, Bony tail, and Razorback Sucker, to selected metal pollutants. Ecotoxicology and Environmental Safety 37: 186-192.

Carvalho, C.S. & Fernandes, M.N. 2006. Effect of temperature on copper toxicity and hematological responses in the neotropical fish Prochilodus scrofa at low and high pH. Aquaculture 251: 109-117.

Cerqueira, C.C. & Fernandes, M. 2002. Gill tissue recovery after copper exposure and blood parameter responses in the tropical fish Prochilodus scrofa. Ecotoxicology and Environmental Safety 52: 83-91.

Chang, I.C., Wei, Y., Chou, F. & Hwang, P. 2003. Stimulation of Cl- uptake and morphological changes in gill mitochondria rich cells in fresh water tilapia (Oreochromis mossambicus) Physiological and Biochemical Zoology 76: 544-552.

Costa, M.F., Barbosa, S.C., Barletta, M., Dantas, D., Kehrig, H., Seixas, T. & Malm, O. 2009. Seasonal differences in mercury accumulation in Trichiurus lepturus (catlassfish) in relation to length and weight in a northest Brazilian estuary. Environmental Science and Pollution Research 16: 423-430.

Couture, P. & Pyle, G. 2011. Homeostasis and toxicology of essential metals, 9 - Field studies on metal accumulation and effects in fish. Fish Physiology. Vol 31, Part A. pp. 417-473.

DiFrancesco, D.T. & Shinn, Jr. R.C. 2002. New Jersey mercury task force report. Exposure and Impacts. Volume II , January. p. 147.

DOE-UM. 1986. Water quality criteria and standards for Malaysia. Executive Summary. Final Report. Department of Environment, Ministry of Science, Technology and Environment, Malaysia Consultant group on water quality, Institute of Advanced Studies, Univ. of Malaya, Kuala Lumpur, Malaysia, 1, V-Xl1.

Fisheries and Aquaculture Department (FAO). 2007. The state of world fisheries and aquaculture 2006. Food and Agriculture Organization of the United Nations. Electronic publishing policy and support Branch, Rome. ISSN 1020- 5489.

Fernandes, C., Fontainhas-Fernandes, A., Rocha, E. & Salgado, M. 2008. Monitoring pollution in Esmoriz- Paramos lagon, Portugal: Liver histological and biochemical effects in Liza saliens. Environmental Monitoring and Assessment 145: 315-322.

Firat, O. & Kargin, F. 2010. Individual and combined effects of heavy metals on serum biochemistry of nile tilapia Oreochromis niloticus. Archives of Environmental Contamination and Toxicology 58: 151-157.

Friberg, L. & Vostal, D. 1974. Mercury in the Environment, an Epidemiological and Toxicological Appraisal. Boca Raton: CRC press. p. 215.

Gehringer, D.B., Finkelstein, M.E., Coale, K.H., Stephenson, M. & Geller, J.B. 2013. Assessing mercury exposure and biomarkers in largemouth bass (Micropterus salmoides) from a contaminated river system in California. Archives of Environmental Contamination and Toxicology 64: 484-493.

Greenfield, B.K., Swee, J., Teh, S.J., Ross, J.R., Hunt, J., Zhang, G.H., Davis, J.A., Ichikawa, G., Crane, D., Hung, S., Deng, D., Teh, F. & Green, P. 2008. Contaminant concentrations and histopathological effects in sacramento splittail (Pogonichthys macrolepidotus). Archives of Environmental Contamination and Toxicology 55: 270-281.

Hamid, M.A., Mansor, M. & Nor, S.A.M. 2015. Length-weight relationship and condition factor of fish populations in Temengor reservoir: Indication of environmental health. Sains Malaysiana 44(1): 61-66.

Harada, M. 1995. Minamata disease: Methylmercury poisoning in Japan caused by environmental pollution. Critical Reviews in Toxicology 25(1): 1-24.

Ishikawa, N.M., Ranzani-Paiva, M. & Lombardi, J. 2007. Acute toxicity of mecury (HgCl2) to Nile tilapia Oreochromis niloticus. B. Inst. Pesca, Sao Paulo 33(1): 99-104.

Jalaludeen, M.D., Arunachalam, M., Raja, M., Nandagopal, S., Bhat, A. & Sundar, S. 2012. Histopathology of the gill, liver and kidney tissue of the fresh water fish tilapia mossambica exposed to cadmium sulphate. International Journal of Advance Biological Research 2(4): 572-578.

Kaewamatawong, T., Rattanapinyopituk, K., Ponpornpisit, A., Pirarati, N., Ruangwises, S. & Rungsipipat, A. 2013. Short-term exposure of Nile tilapia Oreochromis niloticus to mercury histopathological changes, mercury bioaccumulation, and protective role of metallothioneins in different exposure routes. Toxicologic Pathology 41: 470-479.

Kaoud, H.A. & Mekawy, M.M. 2011. Bioremediation the toxic effect of mercury-exposure in Nile tilapia (Oreochromis niloticus) by using Lemna gibba L. Journal of American Science 7(3): 336-343.

Low, K.H., Zain, S.Md. & Abas, M.R. 2011. Evaluation of metal concentrations in red tilapia (Oreochromis spp) from three sampling sites in Jelebu, Malaysia using principal component analysis. Food Analytical Methods 4: 276-285.

Ministry of Health Malaysia. 2012. Food Act 1983 and Food regulations 1985. Updated until December 2011 (P.U.(A) 435/2010). Kuala Lumpur, Malaysia. fsq.moh.gov.my.

Mohan, M., Deepa, M., Ramasamy, E.V. & Thomas, A.P. 2012. Accumulation of mercury and other heavy metals in edible fishes of Cochin backwaters, Southwest India . Environmental Monitoring and Assessment 184: 4233-4245.

Mokhtar, M.B., Aris, A.Z., Munusamy, V. & Praveena, S.M. 2009. Assessment level of heavy metals in Penaeus monodon and Oreochromis spp. in selected aquaculture ponds of high densities development area. European Journal of Scientific Research 30(3): 348-360.

Montaser, M., Mahfouz, M., El-Shazly, S., Abdel-Rahman, G. & Bakry, S. 2010. Toxicity of heavy metals on fish at Jeddah Coast KSA: Metallothionein expression as a biomarker and histopathological study on liver and gills. World Journal of Fish and Marine Sciences 2(3): 174-185.

Nandlal, S. & Pickering, T. 2004. Tilapia Fish Farming in Pacific Island Countries. Vol. 1. Tilapia Hatchery Operation. Noumea, New Caledonia: Secretariat of the Pacific Community.

Nguyen, H.L., Leermakersa, M., Kurunczic, S., Bozod, L. & Baeyens, W. 2005. Mercury distribution and speciation in Lake Balaton, Hungary. Science of the Total Environment 340: 231-246.

Oliveira-Ribeiro, C.A., Belger, L., Pelletier, E. & Rouleau, C. 2002. Histopathological evidence of inorganic mercury and methyl mercury toxicity in the arctic charr (Salvelinus alpinus). Environmental Research 90: 217-225.

Oliveira Ribeiro, C.A., Pelletier, E., Pfeiffer, W.C. & Rouleau, C. 2000. Comparative uptake, bioaccumulation, and gill damages of inorganic mercury in tropical and nordic freshwater fish. Environmental Research Section A 83: 286 -292.

Oliveira Ribeiro, C.A., Fanta, E., Turcatti, N.M., Cardoso, R.J. & Carvalho, C.S. 1996. Lethal effects of inorganic mercury on cells and tissues of Trichomycterus brasiliensis (Pisces, Siluroidei). Biocell 20: 171-178.

Osman, A.G. 2012. Biomarkers in Nile tilapia Oreochromis niloticus niloticus (Linnaeus, 1758) to assess the impacts of river Nile pollution: Bioaccumulation, biochemical and tissues biomarkers. Journal of Environmental Protection 3: 966-977.

Pandey, S., Parvez, S., Ansari, R., Ali, M., Kaur, M., Hayat, F., Ahmad, F. & Raisuddin, S. 2008. Effects of exposure to multiple trace metals on biochemical, histological and ultrastructural features of gills of afreshwater fish, Channa punctata Bloch. Chemico-Biological Interactions 174: 183-192.

Pandey, S., Kumar, R., Sharma, S., Nagpure, N., Srivastava, S. & Verma, M. 2005. Acute toxicity bioassays of mercuric chloride and malathion on air-breathing fish Channa punctatus (Bloch). Ecotoxicology and Environmental Safety 61: 114-120.

Pereira, S., Pinto, A.L., Cortes, R., Fontaı´nhas-Fernandes, A., Coimbra, A.M. & Monteiro, S.M. 2013. Gill histopathological and oxidative stress evaluation in native fish captured in Portuguese northwestern rivers. Ecotoxicology and Environmental Safety 90: 157-166.

Ponzoni, R.W., Khaw, H.L. & Yee, H.Y. 2010. GIFT: The Story since Leaving ICLARM (now known as the World Fish Center – Socioeconomic, Access and Benefit Sharing and Dissemination Aspects. Fridtj of Nansen Institute FNI Report 14/2010. p. 47.

Ponzoni, R.W., Hamzah, A., Tan, S. & Kamaruzzaman, N. 2005. Genetic parameters and response to selection for live weight in the GIFT strain of Nile tilapia (Oreochromis niloticus). Aquaculture 247: 203-210.

Qiu, Y-W., Lin, D., Liu, J. & Zeng, E. 2011. Bioaccumulation of trace metals in farmed fish from South China and potential risk assessment. Ecotoxicology and Environmental Safety 74: 284-293.

Rainbow, P.S. 2002. Trace metal concentrations in aquatic invertebrates: Why and so what? Environmental Pollution 120: 497-507.

Raldu´a, D.; Dı´ez, S.; Bayona, J. M.; and Barcelo, D., 2007. Mercury levels and liver pathology in feral fish living in the vicinity of a mercury cell chlor-alkali factory. Chemosphere 66: 1217-1225.

Senthamilselvan, D., Chezhian, A., Kabilan, N. & Sureshkumar, T. 2011. Synergistic impact of heavy metals (Ni and Hg) and histopathological alterations in the organ (gill) of the fish, Lates calcarifer (Bloch, 1790). European Journal of Experimental Biology 1(2): 198-205.

Sharma, R.R., Pandey, A.K. & Shukla, G.R. 2001. Histopathological alterations in fish tissues induced by toxicity. Aquaculture 2(1): 31-43.

Silva, G.S., Neto, F.F., Assis, H.C., Bastos, W.R. & Oliveira Ribeiro, C.A. 2012. Potential risks of natural mercury levels to wild predator fish in an Amazon reservoir. Environmental Monitoring and Assessment 184: 4815-4827.

Sloman, K.A. 2007. Effects of trace metals on almonid fish: The role of social hierarchies. Applied Animal Behaviour Science 104: 326-345.

Sunderland, E.M. & Chmura, G.L. 2000 An inventory of historical mercury emissions in Maritime Canada: Implications for present and future contamination. The Science of the Total Environment 256: 39-57.

Triebskorn, R., Telcean, I., Casper, H., Farkas, A., Sandu, C., Stan, G., Colarescu, O., Dori, T. & Kohler, H.R. 2008. Monitoring pollution in river Mures, Romania, part II: Metal accumulation and histopathology in fish. Environmental Monitoring and Assessment 141: 177-188.

U.S. Environmental Protection Agency. 2002. Methods for measuring the acute toxicity of effluents and receiving water to fresh water and marine organisms, 5th ed. EPA -821-R-02- 012. Final report, Office of water, Washington, D.C.

Velcheva, I., Tomova, E., Arnaudova, D. & Arnaudov, A. 2010. Morphological investigation on gills and liver of fresh water fish from Dam lake ‘Studen Kladenets’. Bulgarian Journal of Agricultural Science 16(3): 364-368.

Vergilio, C.S., Carvalho, C.E. & Melo, E.J. 2012. Accumulation and histopathological effects of mercury chloride after acute exposure in tropical fish Gymnotus carapo. Journal of Chemical Health Risks 2(4): 01-08.

Watanabe, W.O., Wicklund, R.I., Olla, B.I. & Head, W.D. 1997. Saltwater culture of the Florida red and other saline tolerant tilapias: A review. In Tilapia Aquaculture in the Americans. Vol. 1, edited by Costa-Pierce, A.B. & Rakocy, J.E. Baton Rouge, Louisiana: World Aquaculture Society. pp. 54-141.

World Health Organization (WHO). 2012. Mercury and Health. Fact sheet N°361. http://www.who.int/mediacentre/ factsheets/fs361/en. Accessed on April 2012.

Wu, S.M., Ding, H., Lin, L. & Lin, Y. 2008. Juvenile tilapia (Oreochromis mossambicus) strive to maintain physiological functions after waterborne copper exposure. Archives of Environmental Contamination and Toxicology 54: 482-492.

Yacoub, A.M. 2007. Study on some heavy metals accumulated in some organs of three river Nile fishes from Cairo and Kalubia Governorates. African Journal of Biological Science 3: 9-21.

Yang, J.L. & Chen, H.C. 2003. Serum metabolic enzyme activities and hepatocyte ultrastructure of common carp after gallium exposure. Zoological Studies 42: 455-461.

Zahir, F., Rizwi, S.J., Haq, S.K. & Khan, R.H. 2005. Low dose mercury toxicity and human health. Environmental Toxicology and Pharmacology 20(2): 351-360.

 

 

*Corresponding author; email: m_dogachi71@yahoo.com