Role of Parasitic Helminths in Bioremediating Some Heavy Metal Accumulation in the Tissues of Lethrinus mahsena

Fish take up metals from the aquatic ecosystem and accumulate it in their muscle tissues and organs. The aim of thepresent study was to determine the role of intestinal helminths in bioremediating the accumulation of some heavy metals inthe muscle tissues of the emperor fish, Lethrinu smahsena. A total of 130 fish were collected randomly from Raas Mehsen inthe Red Sea, Jeddah coast, during the period of November 2015 to May 2016. The percent of total infection in L. mahsenafish was found to be 62%. Four species of Trematoda, one cestode larva and three species of Nematoda were recorded fromthe small intestine. Element concentrations in the infected and non-infected fish and parasites were analyzed using flameatomic absorption spectrometry. Mean concentration of individual heavy metals in trematode parasites was in the order ofAs> Fe> Zn> Pb> Cu> Cd. For cestodes, it was As > Fe> Zn> Pb> Cu> Cd. While in nematodes, it was in the order of As>Fe> Zn> Pb> Cd> Cu. Most heavy metals exhibit a significant decrease in fish tissues infected with helminthes.Bioaccumulation factors indicated much higher concentrating capacity of cestode parasites than fish organs. Thereby, cestodeand nematode infections in marine fish could be considered to be a biological indicator of heavy metal pollution and at thesame time could also minimize the bioaccumulation of heavy metals in fish tissues.

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Abul-Naja, W.M. (1996). Comparative study of trace metals accumulated in the muscle tissues of the most marketable seafood in Alexandria waters. International Journal Environmental Health Research. 6(4), 289-300.

Ali, A.A., Elazein, E.M., & Alian, M.A. (2011a). Determination of Heavy Metals in four common Fish, Water and Sediment Collected from Red Sea at Jeddah Isalmic Port Coast. Journal of Applied Environmental and Biological Sciences, 1(10), 453- 459.

Ali, A.A., Elazein, E.M., & Alian, M.A. (2011b). Investigation of Heavy Metals Pollution in Water, Sediment and Fish at Red Sea-Jeddah Coast-KSA at two different locations. Journal of Applied Environmental Biological Sciences, 1, 630-637.

Akinsanya, B., Otubanjo, O.A., & Ibidapo, C.A. (2007). Helminth Bioload of Chrysichthys nigrodigitatus (Lacepede 1802) from Lekki Lagoon Lagos, Nigeria. Turkish Journal of Fisheries and Aquatic Sciences, 7, 83-87.

Azmat, R., Fayyaz, S., Kazi, N., Mahmood, S. J., & Uddin, F. (2008). Natural bioremediation of heavy metals through nematode parasite of fish. Biotechnology,7(1),139-143. http://dx.doi.org/10.3923/biotech.2008.139.143.

Banat, I.M., Nigam, P., Singh, D., Marchant, R., & McHaleA, P. (1998). Review: Ethanol production at elevated temperatures and alcohol concentrations: Part I–yeasts in general. World Journal of Microbiology and Biotechnology, 14(6), 809-821. http://dx.doi.org/10.1023/A:1008802704374.

Barber, I., Hoare, D., & Krause, J. (2000). Effects of parasites on fish behavior: a review and evolutionary perspective. Reviews in Fish Biology and Fisheries, 10(2), 131–165. http://dx.doi.org/10.1023/A:1016658224470.

Baruš, V., Tenora, F., Krácmar, S., & Dvorácek, J. (1999). Contents of several inorganic substances in European eel infected and uninfected by Anguillicola crassus (Nematoda). Diseases of Aquatic Organisms, 37(2), 135-137. http://dx.doi.org/10.3354/dao 037135.

Baruš, V., Tenora, F., Proke, M., & PeAz, M. (2001). Heavy metals in parasites host system: Tapeworm vs. fish in Czech. Ochranazdraviryb (Health protection of fish).Vodaany, pp: 20-28. http://dx.doi.org/10.2754/avb201281030313.

Baruš, V., Jarkovský, J., & Prokeš, M., (2007). Philometra ovata (Nematoda: Philometroidea): a potential sentinel species of heavy metal accumulation. Parasitology Research, 100(5), 929-933. http://dx.doi.org/10.1007/s00436-006-0384-8.

Beckage, N. E. (1993). Endocrine and neuro-endocrine host–parasite relationships. Receptor, 3(3), 233–245.

Beeby, A. (2001). What do sentinels stand for? Environmental Pollution, 112(2), 285-298. http://dx.doi.org/10.1016/S0269-7491(00)00038-5.

Brand, T. (1973). Biochemistry of parasites, 2nd edn. New York, Academic Press. 512 pp.

Conte, F., Copat, C., Longo, S., Conti, G.O., Grasso, A., Arena, G., Brundo, M.V., & Ferrante, M. (2015). "First data on trace elements in Haliotis tuberculata (Linnaeus, 1758) from southern Italy: Safety issues." Food and Chemical Toxicology, 81,143-150. http://dx.doi.org/10.1016/j.fct.2015.04.020.

De Buron, I., James, E., Riggs-Gelasco, P., Ringwood, A.H., Rolando, E., & Richardson, D. (2009). Overview of the status of heavy metal accumulation by helminths with a note on the use of in vitro culture of adult acanthocephalans to study the mechanisms of bioaccumulation. Neotropical Helminthology, 3(2), 101-110.

Dzik, J.M. (2005). Molecules released by helminth parasites involved in host colonization. Acta Biochimica Polonica, 53(1), 33-64.

Eissa, I.A.M., Gehan, I.S., Wafeek, M., & Nashwa, A.S. (2012). Bioremediation for heavy metals in some Red Sea fishes in Suez, Egypt. SCVMJ, XVII, (2), 341- 356.

Evans, D.W., Irwin, S.W.B., & Fitzpatrick, S. (2001). The effect of digenean (Platyhelminthes) infections on heavy metal concentrations in Littorina littorea. Journal of the Marine Biological Association of the UK, 81 (02), 349-350. http://dx.doi.org/10.1017/S0025315401003873.

Forstner, U., & Wittmann, G.T. (1979). Metal pollution in the aquatic environment. Springer-Verlag, New York, 486pp. http://dx.doi.org/10.1002/iroh.19810660232.

Gabrashanska, M., & Nedeva, I. (1996).Content of heavy metals in the system fish-cestodes. Parassitologia, 38, 58.

Hassan, A.A., Akinsanya, B., & Olakolu, F.C. (2013). Heavy metal concentrations in nematode parasites of Clarias gariepinus and Synodontis clarias from Lekki Lagoon, Lagos, Nigeria. Journal of Marine Science: Research and Development, 14, 1 – 8.

Hassan, A., Al-Zanbagi, N., & Al-Nabati, E. (2016). Impact of nematode helminths on metal concentrations in the muscles of koshar fish, Epinephelus summana, in Jeddah, Saudi Arabia. The Journal of Basic & Applied Zoology, 74, 56-61. http://dx.doi.org/10.1016/j.jobaz.2016.09.001.

Jobling, S., & Tyler, C.R. (2003). Endocrine disruption, parasites and pollutants in wild freshwater fish. Parasitology, 126(07), S103-S108. http://dx.doi.org/10.1017/S0031182003003652.

Kelly, J.M., & Janz, D. (2008). Altered energetics and parasitism in juvenile northern pike (Esoxlucius) inhabiting metal-mining contaminated lakes. Ecotoxicology and Environmental Safety, 70, 357– 369. http://dx.doi.org/10.1016/j.ecoenv.2008.01.022.

Khan, R., & Thulin, J. (1991). Influence of pollution on parasites of aquatic animals. Advances in Parasitology, 30, 201-238. http://dx.doi.org/10.1016/S0065-308X (08)60309-7.

Malek, M., Haseli, M., Mobedi, I., Ganjali, M.R., & Mackenzie, K. (2007). Parasites as heavy metal bioindicators in the shark Carcharhinus dussumieri from the Persian Gulf. Parasitology, 134(07), 1053- 1056. http://dx.doi.org/10.1017/S0031182007002508.

Minguez, L., Meyer, A., Molloy, D.P., & Giambérini, L. (2009). Interactions between parasitism and biological responses in zebra mussels (Dreissena polymorpha): importance in ecotoxicological studies. Environmental Research, 109(7), 843-850. http://dx.doi.org/10.1016/j.envres.2009.07.012.

Moore, J.W., & Ramamoorthy, S. (2012). Heavy metals in natural waters: Applied monitoring and impact assessment: Springer Science & Business Media., 268 pp. http://dx.doi.org/10.1461252105, 9781461252108.

Mziray, P.K., & Kimirei, I.A. (2016). Bioaccumulation of heavy metals in marine fishes (Siganus sutor, lethrinus harak, and Rastrelliger kanagurta) from Dar es Salaam Tanzania. Regional Studies in Marine Science, (7), 72-80. http://dx.doi.org/10.1016/j.rsma.2016.05.014.

Nachev, M., Schertzinger, G., & Sures, B. (2013). Comparison of the metal accumulation capacity between the acanthocephalan Pomphorhynchus laevis and larval nematodes of the genus Eustrongylides sp. infecting barbel (Barbusbarbus). Parasites and Vectors, 6, 1-8. http://dx.doi.org/10.1186/1756-3305- 6-21.

Navratil, S., Palikova, M., & Klement, R. (1999). Anguilicolosis of eels in water reservoirs of the Morava River basin. Helminthologia, 36, 129.

Oyoo-Okoth, E., Admiraal, W., Osano, O., Hoitinga, L., & Kraak, M.H. (2010). Metal specific partitioning in a parasite–host assemblage of the cestode Ligula intestinalis and the cyprinid fish Rastrineobola argentea. Science of the Total Environment, 408(7), 1557-1562 . http://dx.doi.org/10.1016/j.scitotenv.2009.11.054.

Oyoo-Okoth, E., Admiraal, W., Osano, O., Kraak, M.H., Gichuki, J., & Ogwai, C. (2012). Parasites modify sub-cellular partitioning of metals in the gut of fish. Aquatic Toxicology, 106, 76-84. http://dx.doi.org/10.1016/j.aquatox.2011.10.014.

Pascoe, D., & Cram, P. (1977). The effect of parasitism on the toxicity of cadmium to the three‐spined stickleback, Gasterosteus aculeatus l. Journal of Fish Biology, 10(5), 467-472. http://dx.doi.org/10.1111/j.1095-8649.1977.tb04079.

Pascual, S., & Abollo, E. (2003). Accumulation of heavy metals in the whale worm Anisakis simplex s. l. (Nematoda: Anisakidae). Journal of the Marine Biological Association of the United Kingdom, 83(5), 905-906. http://dx.doi.org/10.224150999accountid=142908.

Poulin, R. (1998). Evolutionary ecology of parasites: from individuals to community. Chapman and Hall Ltd., London. UK. Country of publication, London., 360 pp.

Retief, N.R., Avenant-Oldewage, A., & Du Preez, H.H. (2009). Seasonal study on Bothriocephalus as indicator of metal pollution in yellow fish, South Africa. Water SA, 35(3), 315- 322.

Rosenberg, D.M., & Resh, V.H. (1993). Freshwater biomonitoring and benthic macroinvertebrates. Chapman and Hall Ltd., New York., 488 pp. http://dx.doi.org/10.1002/aqc.3270040110.

Samuel, D., & George, P.V. (2000). Mineral constituents of freshwater fish Channa striatus infected with acanthocephalan parasite, Pallisentis nagpurensis. Indian Journal of Fisheries, 47(3), 215-224.

Schulz, R.S., & Gvozdev, E.V. (1972). Fundaments of general helminthology.Pub1 House Nauka, Moscow (in Russian) Snedecor, G.W, Cochran, W.G (1967) Statistical methods, 6th edn. Iowa State University Press., Ames, 251 pp.

Shreadah, M.A., Abdel Fattah, L.M., & Fahmy, M.A. (2015). Heavy metals in some fish species and bivalves from the Mediterranean coast of Egypt. Journal of Environmental Protection, 6(01), 1-9. http://dx.doi.org/10.4236/jep.2015.61001.

Sures, B. (2002). Competition for minerals between Acanthocephalus lucii and its definitive host perch (Perca fluviatilis). International journal for parasitology, 32(9), 1117-1122. http://dx.doi.org/10.1016/S0020-7519 (02)00083-8.

Sures, B. (2003). Accumulation of heavy metals by intestinal helminths in fish: An overview and perspective. Parasitology, 126(7), S53. http://dx.doi.org/10.1017/S003118200300372X.

Sures, B. (2004). Environmental parasitology: Relevancy of parasites in monitoring environmental pollution. Trends in Parasitology, 20(4), 170-177. http://dx.doi.org/10.1016/j.pt.2004.01.014.

Sures, B. (2007). Host-parasite interactions from an ecotoxicological perspective. Parassitologia, 49(3), 173-176. http://dx.doi.org/10.1155/2012/237280.

Sures, B., & Roy, S. (2001). Comparison between lead accumulation of Pomphorhynchus laevis (palaeacanthocephala) in the intestine of chub (Leuciscus cephalus) and in the body cavity of goldfish (Carassius auratus auratus). International Journal for Parasitology, 31(7), 669-673. http://dx.doi.org/10.1016/S0020-7519(01)00173-4.

Sures, B., Bahram, S.D., & Harald, F.K. (2003). The intestinal parasite Pomphorhynchus laevis (acanthocephala) interferes with the uptake and accumulation of lead (210 Pb) in its fish host chub (Leuciscus cephalus). International Journal for Parasitology, 33(14), 1617-1622. http://dx.doi.org/10.1016/S0020-7519(03)00251-0.

Sures, B., Taraschewski, H., & Rydlo, M. (1997). Intestinal fish parasites as heavy metal bioindicators: A comparison between Acanthocephalus lucii (Palaeacanthocephala) and the zebra mussel, Dreissena polymorpha. Bulletin of Environmental Contamination and Toxicology, 59(1), 14-21. http://dx.doi.org/10.1007/s001289900437.

Sures, B., Siddall, R., & Taraschewski, H. (1999). "Parasites as accumulation indicators of heavy metal pollution."Parasitology Today, 15 (1), 16-21. http://dx.doi.org/10.1016/S0169-4758(98)01358-1.

Tenora, F., Baruš, V., & Prokes, M. (2002). Next remarks to the knowledge of heavy metal concentrations in gravid tapeworm species parasitizing aquatic birds. Helminthologia, 39(3), 143-148. http://dx.doi.org/10.1016/S0169-4758(98)01358-1.

Thielen, F., Zimmermann, S., Baska, F., Taraschewski, H., & Sures, B. (2004). The intestinal parasite Pomphorhynchus laevis (Acanthocephala) from barbel as a bioindicator for metal pollution in the Danube River near Budapest, Hungary. Environmental Pollution, 129(3), 421-429. http://dx.doi.org/10.1016/j.envpol.2003.11.011.

Torres, M.J., Eira, C., Miquel, C.J., & Feliu, J.C. (2012). Heavy metal accumulation by intestinal helminths of vertebrates. In: Diego Muñoz-Torrero, Diego Haro and Joan Vallès (ed). Recent Advances in Pharmaceutical Sciences II, Transworld Research Network., Chapter 10, 169-181 pp.

Uçkun, A.A., (2017). Ecotoxicological Evaluation of Pesticide Pollution in Ataturk Dam Lake (Euphrates River), Turkey, Turkish Journal of Fisheries and Aquatic Sciences. 17, 313-321. http://dx.doi.org/10.4194/1303-2712-v17_2_10.

Velusamy, A., Satheesh, K.P., Ram, A., & Chinnadurai, S. (2014). Bioaccumulation of heavy metals in commercially important marine fishes from Mumbai Harbor, India. Marine Pollution Bulletin, 81(1), 218- 24. http://dx.doi.org/10.1016/j.marpolbul.2014.01.049.

Wahbeh, M.I., & Mahasneh, D.M. (1987). Concentrations of Metals in the Tissues of Six Species of Fish from Aqaba, Jordan. Dirasat, 14, 119-129.

Williams, M.A., Penlington, M.C., King, J.A., Hoole, D., & Arme, C. (1998). Ligula intestinalis (Cestoda) infections of roach (Rutilus rutilus) (Cyprinidae): immunocytochemical investigations into the salmonand chicken-II type gonadotrophin-releasing hormone (GnRH) systems in host brains. Acta Parasitologica, 43, 232–5.

Zaghloul, K.H., Abd El-Monem, S., Fayed, H.M., & Mohamed, H. A. (2001). Fish parasites as biological indicators of pollution with heavy metals. Journal of Union of Arab Biologists, 15, 533–561.
Turkish Journal of Fisheries and Aquatic Sciences-Cover
  • ISSN: 1303-2712
  • Başlangıç: 2015
  • Yayıncı: Su Ürünleri Merkez Araştırma Enstitüsü - Trabzon
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