Cover Image

An integrated use of histological and ultra-structural biomarkers in Mugil cephalus for assessing heavy metal pollution in east Berbice-Corentyne, Guyana

Sivakumar Rajeshkumar*; Dhivya Karunamurthy; Grayson Halley and Natesan Munuswamy


Bioaccumulation of heavy metals and its associated histopathological perturbations were studied in various tissues of Mugil cephalus collected from polluted and compared with the fish collected from less polluted of Corentyne coast. The concentration of copper, lead, zinc, cadmium, manganese and iron were quantified in gills, liver and muscle. The results showed marked differences between the two sites as well as significant variations within the tissues. The decreasing trend of metals in the tissues of fish sampled from both polluted and less polluted sites was in the order of Fe >Mn > Zn > Cu > Pb > Cd. Overall, the highest metal concentrations were found in the fish collected from polluted site. The accumulation in the gills and liver of M. cephalus was found to be quite high in comparison with the muscle. These tissues were further investigated by light and electron microscopy and the results were compared with the reference site (Less polluted). The presence of large lipid droplets in liver and increase of mucous cell in gill were some of the most noticeable alterations observed and were related to heavy metal contaminates. It is concluded that histopathological and ultrastructural biomarkers provide reliable and discriminatory data to augment heavy metal pollution in polluted site of Coretyne coast. Therefore, long-term monitoring is necessary to assess the untreated waste water discharged directly and indirectly into the water ways of Corentyne coast led to a reduction in waste assimilative capacity of the coastal marine waters, which provide accurate, reliable measurements of environmental quality.


Bioaccumulation; Heavy metals; Mugil cephalus; Histopathology; Ultrastructure.

Full Text:



Alan G Heath. “Water Pollution and Fish Physiology”. CRP press, Florida (1987): P. 245.

Almeida. “Feeding ecology of Liza ramada (Risso, 1810) (Pisces, Mugilidae) in a south-western estuary of Portugal”. Estuarine Coastal and Shelf Science 57 (2003): 313-323.

Al-Yousuf, El-Shahawi, and Al-Ghais. “Trace metals in liver, skin and muscle of Lethrinus lentjan fish species in relation to body length and sex”. Science of the Total Environment 256 (2000): 87-94.

Anderson, Law, Shariff, and Nash. “A parvo-like virus in the giant freshwater prawn, Macrobrachium rosenbergii”. Journal of Invertebrrate Pathology 55 (1990): 447-449.

Bernet, Schmidt, Meier, Burkhardt-Holm, and Wahli. "Histopathology in fish: proposal for a protocol to assess aquatic pollution”. Journal of Fish Diseases 22 (1999): 25-34.

Bernet, Schmidt-Posthaus, Wahli, and Burkhardt Holm. “Evaluation of two monitoring approaches to assess effects of waste disposal on histological alterations in fish”. Hydrobiology 524 (2004): 53-66.

Bervoets, Blust, and Verheyen. “Accumulation of metals in the tissues of three spined stickelback (Gasterosteus aculeatus) from natural fresh waters”. Ecotoxicology Environmental Safety 48(2) (2001): 117-127.

Blasco, Arias, and Saenz. “Heavy metals in organisms of the River Guadalquivir estuary: possible incidence of the Aznalcollar disaster”. Science of the Total Environment 242 (1999): 249-259.

Braunbeck, and Appelbaum. “Ultrastructural alterations in the liver and intestine of carp Cyprinus carpio induced orally by ultra-low doses of endosulfan”. Disease of Aquatic Organisms 36 (1999): 183-200.

Canbek Mediha, Temir Ali Demir, Mustafa Uyanoglu, Go¨khan Bayramoglu, O¨ zgu¨r Emiroglu, and Naime Arslan, et al. “Preliminary assessment of heavy metals in water and some cyprinidae species from the Porsuk river”. Turkey Journal of Applied Biological Science 1(3) (2007): 91-95.

Carmona, Garcia-Gallego, Sanz, Domezain, and Ostos-Garredo. “Chloride cells and pavement cells in gill epithelia of Acipenser naccaril: ultrastuctural modifications in seawater acclimated specimens”. Journal of Fish and Biology 64 (2004): 553-566.

Casas, Gonzalez, Andral, and Cossa. “Relation between metal concentration in water and metal content of marine mussels (Mutilus galloprovincialis): impact of physiology”. Environmental Toxicology and Chemistry 27 (7) (2008): 1543-1552.

Cerqueira, and Fernandes. “Gill tissue recovery after cooper exposure and blood parameter responses in the tropical fish Prochilodus scrofa”. Ecotoxicological and Environmental Safety 52 (2002): 83-91.

Chale. “Trace metal concentration in water, sediments and fish tissue from lake Tanganyika”. Science of the Total Environment 299 (2002): 115-121.

Chang, Zdanowicz, and Murchelano. “Associations between liver lesions in winter flounder (Pleuronectes americanus) and sediment chemical contaminants from north-east United States estuaries”. Journal of Marine Science 55 (1998): 954-969.

Chen YC, and Chen MH. “Heavy metal concentrations in nine species of fish caught in coastal waters off Ann-Ping, SW Taiwan”. Journal of Food Drug Analysis 9 (2001): 107-114.

Cid, Bioa, Pombo, and Rebelo. “Determination of trace metals in fish species of the Ria de Aveiro (Portugal) by electro thermal atomic adsorption spectrometry”. Food Chemistry 75 (1) (2001): 93-100.

Couch, and Harshbarger. “Effects of carcinogenic agents on aquatic animals: an environmental and experimental overview”. Environmental Carcinogenesis Reviews 3 (1985): 63-105.

Coutinho, and Gokhale. “Selected oxidative enzymes and histopathological changes in the gills of Cyprinus carpio and Oreochromis mossambicus cultured in secondary sewage effluent”. Water Research 34 (2000): 2997-3004.

David E Hinton, and Lauren OJ. “Liver structural alterations accompanying chronic toxicity in fishes”: potential biomarkers of exposure. In: Biomarkers of environmental contamination. J. F. McCarthy and L. R. Shugart (Eds.,) MI Lewis Publishers 1990, p.12- 68.

David E Hinton, Baumann PC, Gardner GR, Hawkins WE, Hendricks JD, Murchelano RA, and Okihiro MS. “Histopathologic biomarkers”. In: Hugget, R, Kimerle, R, Mehrle P, H. Bergman (Eds.). Biomarkers - biochemical, physiological and histological markers of anthropogenic stress. Boca Raton, Lewis Publishers 1992, p.155-195.

David Evans, Dedoo, and Hanson. “Trace element concentrations in fish livers. Implications of variations with fish size in pollution monitoring”. Marine Pollution Bulletin 26(6) (1993): 329-334.

David Evans. “The fish gill: site of action and model for toxic effects of environmental pollutants”. Environmental Health Perspective 71 (1987): 47-58.

Deys. Papillomas in the Atlantic eel, Anguilla vulgaris. “In A Symposium on neoplasms and related disorders of invertebrate and lower vertebrate animals”. Ed. by C. J. Dawe and J. C. Harshbarger. National Cancer Institute Monograph 31 (1969): 187-193.

Doris Au. "The application of histo-cytopathological biomarkers in marine pollution monitoring: a review". Marine Pollution Bulletin 48 (2004): 817-834.

Dyrynda, Pipe, and Ratclitte. “Sub populations of haemocytes in the adult and developing marine mussel, myticus edulis, identified by use of monoclonal antibodies”. Cell Tissue Research 289 (3) (1997): 527 - 36.

Eateves. Fundanentod de limologia Rio de Janeiro, Interciencia. FINEP (1988).

Eckwert, and Kohler. “The induction of stress proteins (HSP) in Oniscus asellus (Isopoda) as a molecular marker of multiple heavy metal exposure”. Toxicology to Assessment of Ecotoxicology 6 (1997): 249-262.

Ekamaram Padmini, and Usha Rani Munuswamy. “Thioredoxin and HSP 90α modulate ASK1-JNK1/2 signalling in stressed hepatocytes of Mugil cephalus”. Comparative Biochemistry Physiology Part C. 151 (2010): 187- 193.

Ekamaram Padmini, Kavitha Murgan. “Contaminant induced stress impact on biochemical changes in brain of estuarine grey mullets”. Pollution Research 24 (2005): 647- 651.

Emilio Carpene, and Vasak Milan. “Hepatic Metallothionein from Goldfish (Carassius auratus)”. Comparative. Biochemistry and Physiology 92B (1989): 463-468.

Engelhardt, Wong, and Duey. “Hydromineral balance and gill morphology in rainbow trout Salmo gairdneri, acclimated to fresh and sea water as affected by petroleum exposure”. Aquatic Toxicology 1 (1981): 175-186.

Eu. Commission Regulation (Ed.), No 466/2001. Setting Maxiumum Levels for Certain Contaminants in Food Chemistry 75 (1) (2001): 93-100.

Evans Fanta, Rios Fanta, Romão Vianna and Freiberger. “Histopathology of the fish Corydoras paleatus contaminated with sublethal levels of organophosphorus in water and food”. Ecotoxicology and Environmental Safety 54 (2003): 119-130.

Fernandes, Fontainhas, Monteiroand, and Salgado Ali. “Changes in plasma electrolytes and gill histopathology in wild Liza saliens from the Esmoriz-Paramos coastal lagoon”. Bulletin Environmental Contamination and Toxicology 79 (2007): 301-305.

Folmar Gardner, Schreibman Magluilo-Cepriano, Mills Zaroogian, Gutjahr-Gobell Haebler, and Horowitz Denslow. “Vitellogenin-induced pathology in male summer flounder (Paralichthys dentatus)”. Aquatic Toxicology 51 (2001): 431-441.

Food and agricultural organization (FAO). Compliation of legal limits for hazardous substances in fish and fishery products. FAO Fish Crick 464. (1983): 5-100.

Fournie, Summers, and Weisberg. “Prevalence of gross pathological abnormalities in estuarine fishes”. Transactions of the American Fisheries Society 125 (1996): 581-590.

Francis Henry, Amara Rama, Courcot, Lacouture Daniel, and Bertho. “Heavy metals in four fish species from the French coast of the eastern English Channel and southern bight of the North Sea”. Environmental International 30 (2004): 675-683.

Gernhofer, Pawet, Schramm, Müller, and Triebskorn. “Ultrastructural biomarkers as tools to characterize the health status of fish in contaminated streams”. Journal of Aquatic Ecosystems 8 (2001): 241-260.

Gil, Allen and Martynov. “Heavy metals burdens in nine species of freshwater and anadromous fish from the Pechora River, northern Russia”. Science of the Total Environment 160-161 (1995): 653-659.

Guven K, Ozbay C, Unlu E, Star A. “Acute lethal toxicity and accumulation of copper in Gammarus pulex (L.) (Amphipoda)”. Turkey Journal of Biology 23 (1999): 513-521.

Guyana Times. Kaieteur News, February 2013; 23: Guyana. P 5.

Haaparanta, Valtonen, and Hoffmann. “Gill anomalies of perch and roach from four lakes differing in water quality”. Journal of Fish Biology 50 (1996): 575-591.

Halim, Abbas, and Ali Fagr. “Study the effect of hexavalent chromium on some biochemical, cytological and histolopathological aspects of Orechromis spp Fish”. Pakistan Journal Biological Sciences 10 (2007): 3973-3982.

Hogstrand C, and Haux C. “Binding and detoxification of heavy metals in lower vetrebrats with reference to metallothionein”. Comparative Biochemistry and Physiology 100 (1/2). (1991): 137-141.

Hughes DA. “The role of responses to light in the selection and maintenance of microhabitat by the nymphs of two species of mayfly”. Anita Bahavan 14 (1966): 17-33.

Hulya Karadede, and Unlu Erhan. “Concentrations of some heavy metals in water, sediment and fish species from the Ataturk Dam Lake (Euphrates), Turkey”, Chemosphere 41 (9) (2000): 1371-1376.

Hulya Karadede, Oymak Seyit Ahmet, Unlu Erthan. “Heavy metals in mullet, Liza abu and Cat fish, Silurus triostegus, from the Ataturk Dam Lake Euphrates, Turkey”. Environmental International 30 (2004): 183-188.

Humphry Bowen. “Environmental chemistry of the elements”. London: Academic Press 1979, pp. 269.

Jiraungkoorskul W, Sahaphong S, and Kangwanrangsan N. “Toxicity of copper in butterfish (Poronotus triacanthus): tissues accumulation and ultrastructural changes”, Environmental Toxicology 22 (2007): 92-100.

JM Hellawell. “Biological Indicators of Freshwater Pollution and Environmental Management”. Amsterdam: Elsevier Publications (1986): 546-554.

Jordao CP, Pereira MG, Bellato CR, Pereira JL, and Matos AT. “Assesssment of water systems for contaminants from domestic and industrial sewages”. Environmental Monitoring Assessment 79 (1) (2002): 75-100.

Jordi Floch, Lees, Stanley Scoane. “A simple method for the isolation and purification of total lipids from animal tissues”. Journal of Biological Chemistry 226 (1957): 497-508.

Kalay M, and Canil M. “Elimination of essential (Cu, Zn) and non-essential (Cd, Pb) metals from tissue of a freshwater fish Tilapia zilli”. Turkish Journal of Zoology 24 (2000): 429-436.

Kargin, and Erdem Cahit. “Accumulation of copper in liver, spleen, stomach, intestine, gill and muscle of Cyprinus carpio. Doga. Turkey”. Journal of Zoology 15 (1999): 306-14.

Karlsson-Norrgren L, Runn P, Haux C, and Forlin L. “Cadmium induced changes in gill morphology of zebrafish, Brachydynio rerio (Hamilton-Buchanan), and rainbow trout, Salmo gairdneri”. Journal of Fish Biology 27 (1985): 81-95.

Kikuchi M, Wakabayashi M, Kojima H, and Yoshida T. “Uptake, distribution and elimination of sodium linear alkylbenzene sulfonate and sodium alkyl sulfate in carp”. Ecotoxicology and Environmental Safety 2 (1978): 115-127.

Kumaraguru AK, Beamish FWH, and Ferguson HW. “Direct and circulatory paths of Permethrin (NRDC-143) causing histopathological changes in the gills of rainbow trout, Salmogairdneri Richardson”. Journal of Fish Biology 20 (1982): 87-91.

Lakshmanan PT, and Nambisan RNK. “Seasonal variation in trace metal content in bivalve molluscs, Villorita cyprinoides var. cochinensis (Hanley), Meretrix casta (Chemnitz) and Perna viridis (Linnaeus)”. Indian Journal of Marine Science 12 (1983): 100-103.

Laurent P, and Hebibi N. “Gill morphometry and fish osmoregulation”. Canadian Journal of Zoology 67 (1988): 3055-3063.

LL Johnson, Stehr CM, Olson OP, Myers MS, Pierce SM, Wigren CA, McCain BB, and Varanasi U. “Chemical contaminants and hepatic lesions in winter flounder (Pleuronectes americanus) from the northeastern coast of the United States”. Environmental Science and Technology 27 (1993): 2759-2771.

Longwell AC, Chang S, and Gadbois DF. “A complete analysis of winter flounder (Pleuronectes americanus) egg contaminants with respect to early reproduction with a review of their toxicity and other environmental concentrations”. Reviews in Fisheries Science 4 (1996): 339-386.

Longwell AC, Chang S, Hebert A, Hughes JB, and Perry DM. “Pollution and developmental abnormalities of Atlantic fishes”. Environmental Biology Fishery 35 (1992): 1-21.

Lourdraj Arockia Vasanthi, Revathi Peranandam, Mini Jayaprakash, Munuswamy Natesan. “Integrated use of histological and ultrastuctural biomarkers in Mugil cephalus for assessing heavy metal pollution in Ennore estuary, Chennai”. Chemosphere 91(8) (2013): 1156-1164.

Malins D, McCain BB, Brown DW, Chan SL, Myers MM, Landahl J, Prohaska P, Friedman A S, Rhodes L, Burrow DG, Gronlund W, and Hodgins H. “Chemical pollutants in sediments and diseases of bottomdwelling fish in Puget Sound, Washington”. Environmental Science and Technology 18 (1984): 705-713.

Mallatt J. “Fish gill structural changes induced by toxicants and other irritants: a statistical review”. Canadian Journal of Fish Aquatic Science 42 (1985): 630-648.

Mansour SA, and Sidky MM. Ecotoxicological studies: “Heavy metals contaminating water and fish from Fayoum Governorate Egyptian”. Food Chemistry 78 (2002): 15-22.

Marcovecchio JE. “The use of Micropogonias furnieri and Mugil liza as bioindicators of heavy metals pollution in La Plata river estuary, Argentina”. Science of the Total Environment 323 (2004): 219-226.

Marina M P Camargo, and Claudia B R Martinez. “Biochemical and physiological biomarkers in Prochilodus lineatus submitted to in situ tests in an urban stream in southern Brazil”. Environmental Toxicology and Pharmacology 21 (2006): 61-69.

Martinez CBR, Nagae MY, Zaia CTBV, and Zaia DAM. “Morphological and physiological acute effects of lead in the neotropical fish Prochilodus lineatus. Brazil”. Journal of Biology 64 (4) (2004): 797-807.

Mazon AF, Pinheiro GHD, and Fernandes MN. “Hematological and physiological changes induced by short-term exposure to copper in the freshwater fish, Prochilodus scrofa. Braz”. Journal of Biology 62 (4A) (2002): 621-631.

Mc Donald DG, Freda J, Cavdek V, Gonzalez R, and Zia S. “Interspecific differences in gill morphology of freshwater fish in relation to tolerance of low-pH environments”. Physiology of Zoology 64 (1) (1991): 124-144.

McCain BB, Pierce KV, Wellings SR, and Miller BS. “Hepatomas in marine fish from an urban estuary”. Bulletin of Environ Contamination Toxicology 18 (1977): 1-12.

Mendil D, Uluozlu OD, Hasdemir E, Tuzen M, Sari H, and Suicmez M. “Determination of trace metal levels in seven fish species in lakes in Tokat, Turkey”. Food Chemistry 90 (2005): 175-179.

Mix MC. “Cancerous diseases in aquatic animals and their association with environmental pollutants: a critical review”. Marine Environmental Research 20 (1986): 1-141.

Mohammed A, May T, Echols K, Walther M, Manoo A, Maraj D, Agard J, and Orazio C. “Metals in sediments and fish from Sea Lots and Point Lisas Harbors, Trinidad and Tobago”. Marine Pollution Bulletin 64 (2012): 169-173.

Monteiro Fernandes, and Mazon Fernandes. “Environmental pollution and fish gill morphology”. In: Val, A. L. & B. G. Kapoor (Eds.). Fish adaptations. Enfield, Science Publishers (2003): 203-231.

Moore MJ, Shea D, Hillman R, and Stegeman JJ. “Trends in hepatic tumours and hydropic vacuolation, fin erosion, organic chemicals and stable isotope ratios in winter flounder from Massachusetts, USA”. Marine Pollution Bulletin 32 (1996): 458-470.

Mormede S, and Davis IM. “Heavy metal concentrations in commercial deep sea fish from the Rockall Trough”. Contamination of Shelf Research 21 (8-10) (2001): 899-916.

Morsey MG, and Protasowicki M. 1990. “Cadmium bioaccumulation and its effects on some hematological and histological aspects in carp, Cyprinus carpio (L.) at selected temperature”. Acta Ichthyology of Piscat XX Fasc. 1.

Murat Karakoc. “Effects of salinity on the accumulation of copper in liver, gill and muscle tissues of Tilapia nilotica. Turkey”. Journal of Zoology 23 (1999): 299-303.

Murthy RKV, and Rao BK, “Survey of meiofauna in the Gautami - Godavari estuary”. Journal of Marine Biology and Association of India 29 (1987): 37-44.

Mustafa Canli, and Atli Guluzar. “The relationships between heavy metal (Cd, Cr, Cu, Fe, Pb, Zn) levels and size of six Mediterranean fish species”. Environmental Pollution 121 (1) (2003): 129-136.

Myers MS, Stehr CM, Olson OP, Johnson LL, McCain BB, Chan SL, and Varanasi U. “Relationships between toxicopathic hepatic lesions and exposure to chemical contaminants in English sole (Pleuronectes vetulus), starry flounder (Platichthys stellatus), and white croaker (Genyonemus lineatus) from selected marine sites on the Pacific coast, USA. Environmental Health Perspectives 102 (1994): 200-215.

Nair M, Jayalakshmy KV, Balachandran KK, and Joseph T. “Bioaccumulation of toxic metals by fish in a semi-enclosed tropical ecosystem”. Environmental Forensics 7 (2006): 197-206.

Obasohan EE. “Heavy metals concentrations in the offal, gill, muscle and liver of a freshwater mudfish (Parachanna obscura) from Ogba River, Benin city, Nigeria”. African Journal of Biotechnology 6(22) (2007): 2620-2627.

Oliveira Ribeiro CA, Pelletier E, Pfeiffer WC, and Rouleau C. “Comparative uptake, bioaccumulation, and gill damages of inorganic mercury in tropical and nordic freshwater fish”. Environmental Research 83 (2000): 286-292.

Oliveria M, Maria VL, Ahmad L, Serafim A, Bebianno MJ, Pacheco M, and Santos MA. “Contamination assessment of a coastal lagoon (Ria de Aveiro, Portugal) using defence and damage biochemical indicators in gill of Liza aurata an integrated biomarkers approach”. Environmental Pollution 157 (3) (2009): 59-967.

Oliveria M, Pacheco M, and Santos MA. “Cytochrome P4501A, genotoxic and stress responses in golden grey mullet (Liza aurata) following short-term exposure to phenanthrene”. Chemosphere 66 (2007): 1284-1291.

Pacheco M, and Santos MA. “Biotransformation, genotoxic and histopathological effects of environmental contaminants in European eel (Anguilla anguilla L.)”. Ecotoxicology and Environmental Safety 53 (2002): 331-347.

Pandey S, Parvez S, Sayeed I, Haque R, Bin-Hafeez B, and Raisuddin S. “Biomarkers of oxidative stress: a comparative study of river Yamuna fish Wallago att (Bl. & Schn.)”. Science of the Total environment 309 (2003): 105-115.

Paul MJ, and Meyer JL. “Streams in the urban landscape”. Annual Review of Ecology and Systematic 32 (2001): 333-65.

Peters G. “Seasonal fluctuations in the incidence of epidermal papillomas of the European eel (Anguilla anguilla)”. Journal of Fish Biology 7 (1975): 415-422.

Poleksic V, and Mitrovic-Tutundzic V. 1994. “Fish gills as a monitor of sublethal and chronic effects of pollution”. Pp. 339-352. In: Müller, R. & R. Lloyd (Eds.). Sublethal and Chronic effects of pollutants on freshwater fish. Oxford, Fishing News Books.

Pratap HB, and Wendelaar Bonga SE. “Effect of ambient and dietary cadmium on pavement cells, chloride cells and Na+ K+ ATPase activity in the gills of the freshwater Teleost Oreochromis mossambicus at normal and high calcium levels in the ambient water”. Aquatic Toxicology 26 (1993): 133-150.

Rao LM, and Padmaja G. “Bioaccumulation of heavy metals in M. cyprinoids from the harbour waters of Visakhapatnam”. Bulletin of Pure and Applied Science 19A (2) (2000): 77-85.

Rashed MN. “Monitoring of environmental heavy metals in fish from Nasser Lake”. Environ. Internation 27 (2001): 27-33.

Roe JH. “The determination of sugar in blood and spinal fluid with anthrone reagent”. Journal of Biological Chemistry 212 (1955): 335-343.

Rosety-Rodríguez M, Ordoñez FJ, Rosety M, Rosety J M, Ribelles A, and Carrasco C. “Morpho-histochemical changes in the gills of turbot, Scophthalmus maximus L., induced by sodium dodecyl sulphate”. Ecoloxicology and Environnemental Safety 51 (2002): 223-228.

Sankar TV, Zynudheen AA, Anandan R, and Viswanathan Nair PG. “Distribution of organochlorine pesticides and heavy metal residues in fish and shellfish from Calicut region, Kerala, India”. Chemosphere 65 (2006): 583-590.

Sauves S, Handaui M, Brousseau P, and Fournier M. “Phagocytic response of terrestrial and aquatic invertebrates following in vitro exposure to trace elements”. Ecoloxicology and Environnemental Safety 52 (1) (2002): 21-9

Scharenberg W P, and Gramann WH. “Bioaccumulation of heavy metals and organochlorines in a lake ecosystems with special reference to bream (Abramis brama. L)”. Science of the Total. Environment 155(2) (1994): 187-97.

Schwaiger J, Wanke R, Adam S, Pawert M, Honnen W, and Triebskorn R. “The use of histopatological indicators to evaluate contaminant-related stress in fish”. Journal of Aquatic Ecosystem, Stress and Recovery 6 (1997): 75-86

Senthilnathan S, and Balasubramanian T. “Heavy metal concentration in oyster Crassostrea madrasensis (Bivalvia anisomyaria) from the Uppanar, velar and Kaduviar estuaries of Southeast Coast of India”. Journal of Marine Science 27 (1998): 211-216.

Sindermann CJ. “Pollution-associated diseases and abnormalities of fish and shellfish: a review”. Fishery Bulletin, U.S 76. (1979): 717-748.

Singh V, and Chandel CPS. “Analytical study of heavy metals of industrial effluents at Jaipur, Rajasthan, India”. Journal of Environmental Science and Engineering 48 (2006): 103-108.

Sivakumar Rajeshkumar, and Munuswamy Natesan. “Impact of metals on histopathology and expression of HSP70 in different tissues of Milk fish (Chanos chanos) of Kaattuppalli Island, South East Coast, India”. Chemosphere 83 (2011): 415-421.

Sivakumar Rajeshkumar, and Munuswamy Natesan. “Infection of acanthocephalan parasite Neoechinorhynchus agilis sp in the grey mullet, (Mugil cephalus) a candidate species from - Corentyne coast, Berbice, Guyana”. World Journal of Pharmaceutical Research 2 (2013): Issue 6.

Sivakumar Rajeshkumar, Dhivya Karunamurthy and Munuswamy Natesan. “Heavy metal pollution in East Berbice-Corentyne Coast, Guyana”. ID #120590, ISBN 978-3-659-69368-7). In: Lambert Academic Publishing, Germany. (2015) P. 1-72

Sivakumar Rajeshkumar, Mini Jayaprakash, and Munuswamy Natesan. “Effects of heavy metals on antioxidents and expression of HSP70 in different tissues of Milk fish (Chanos chanos) of Kaattuppalli Island, Chennai, India”. Ecotoxicology and Environmental Safety 98 (2013): 8-18.

Sivaperumal P, Sankar TV, and Viswanathan Nair PG. “Heavy metal concentrations in fish, shellfish and fish products from internal markets of India vis-à-vis international standards”. Food Chemistry 102 (2007): 612-620.

Smith C, Peck T, Klauda R, and McLaren J. “Hepatomas in Atlantic tomcod, Microgadus tomcod (Walbaum), collected in the Hudson River estuary in New York”. Journal of Fish Diseases 2 (1979): 313-319.

Sultana R, and Rao DP, “Bioaccumulation patterns of zinc, copper, lead and cadmium in grey mullet Mugil Cephalus from harbour waters of Visakhapatnam India”. Bulletin Environmental Contamination and Toxicology 60 (1998): 949-955.

Sunlu U, Ozdemir E, and Basaran A. “The red mullet Mullus barbatus (Linnaeus 758) as an indicator for heavy metal pollution in Izmir Bay (Turkey)”. 36th Ciesm Congress Proceedings, Monaco: Monte Carlo (2001).

Takashima F, and Hibya T. 1995. “An atlas of fish histology: normal and pathological features”, 2nd ed. Tokyo, Kodansha.

Teh SJ, Adams SM, and Hinton DE. “Histopathological biomarkers in feral freshwater fish populations exposed to different types of contaminant stress”. Aquatic Toxicology 37 (1997): 57-70.

Temmink J, Bowmieister P, Jong P, and Van der Berg J. “An ultra-structural study of chromate-induced hyperplasia in the gill of rainbow trout, Salmo gairdneri”. Aquatic Toxicology 4 (1983): 165-179.

Thophon S, Kruatrachue M, Upathan ES, Pokethitiyook P, Sahaphong S, and Jarikhuan S. “Histopathological alterations of white seabass, Lates calcarifer in acute and subchronic cadmium exposure”. Environmental Pollution 121 (2003): 307-320.

Triebskorn R, Kohler, HR, Honnen W, Schramm M, Adams SM, and Muller EF. “Induction of heat shock proteins, changes in liver ultrastructure, and alterations of fish behaviour: Are these biomarkers related and are they useful to reflect the state of pollution in the field”. Journal of Aquatic Ecosystems Stress Recovery 6 (1997): 57-73.

Turkmen M, Turkmen A, Akyurt I, Tepe Y. Limpet. “Patella caerulea Linnaeus, 1758 and Barnacle, Balanus sp., as biomonitors of trace metals availabilities in Iskenderun Bay, Northern East Mediterranean Sea”. Bulletin Environmental Contamination and Toxicology 74 (2005): 301-307.

Valentina G. Caccia, and Frank J. Millero. “The distribution of trace metals in Florida Bay sediments”. Marine Pollution Bulletin 46 (2003): 1420-1433.

Vander Oost R, Beyer J, and Vermeulen NPE. “Fish bioaccumulation and biomarkers in environmental risk assessment: A review”. Environmental Toxicology and Pharmacology 13 (2003): 57-149.

Vethaak AD, and Wester PW. “Diseases of flounder (Platychthys flesus) in Dutch coastal and estuarine waters, with particular reference to environmental stress factors 2 Liver histopathology”. Diseases of Aquatic Organisms 26 (1996): 99-116.

Vogelbein WK, Fournie JW, van Veld PA, and Hugett RJ. “Hepatic neoplasms in the mummichug (Fundulus heteroclitus) from a creosote-contaminated site”. Cancer Research 50. (1990): 5978-5986.

Wagner A, and Boman,J. “Biomonitoring of trace elements in Vietnamese freshwater mussels”. Spectrochimica Acta 59 (2004): 1125-1132.

Wester PW, and Canton JH. “The usefulness of histopathology in aquatic toxicity studies”. Comparative Biochemistry and Physiology 100 (1991): 115-117.

Wester PW, Van der Ven LTM, Vethaak AD, Grinwis GCM, and Vos JG. “Aquatic toxicology: opportunities for enhancement through histopathology”. Environmental Toxicology and Pharmacology 11 (2002): 289-295.

William Fischer, Bianchi George. “FAO Identification Sheets for Fishery Purposes”. Western Indian Ocean, FAO, Rome (1984).

William W Au, Carlos H Sierra Torres, Salazar Nohelia Cojas, and Salama A Salama. "Inheritance of polymorphic metabolizing genes and environmental disease and quality of life”. Mutation Research 428 (1999): 131-140.

Winkaler EU, Silva AG, Galindo HC, and Martinez CBR. “Biomarcadores histológicos e fisiológicos para o monitoramento da saúde de peixes de ribeirões de Londrina, Estado do Paraná”. Acta Scientiarum 23 (2001): 507-514.

Wright RT. 2001. Environmental Science toward Sustainable Future. Ninth Edition: Prentice - Hall of India Private Limited, New Delhi. 11p.

Yazkan M, Ozdemir F, and Golukcu M. “Cu, Zn, Pb and Cd content in some fish species caught in the Gulf of Antalya”. Turkey Journal of Veterinary and Animal Science 26 (6) (2002): 1309-1315.

Zyadah M, and Chouikhi A. “Heavy metal accumulation in Mullus barbatus, Merluccius merluccius and Boops boops fish from the Aegean Sea, Turkey”. International journal of food sciences and nutrition 50 (6) (1999): 429-434.



  • There are currently no refbacks.

Copyright (c) 2015 International Journal of Bioassays

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

International Journal of Bioassays is a member of the Publishers International Linking Association, Inc. (PILA), CROSSREF and CROSSMARK (USA). Digital Object Identifier (DOI) will be assigned to all its published content.