Toxicity of Foroozan crude oil to ornate wrasse (Thalassoma pavo, Osteichthyes, Labridae): ultrastructure and cellular biomarkers

Abstract The present study was conducted to assess the toxicity of Foroozan (Iranian crude oil) on the ornate wrasse Thalassoma pavo (Labridae) using three sub-lethal crude oil concentrations. Gills, selected as target organ being the major route of hydrocarbon uptake, were excised after 48, 96 and 192 hours and analyzed by light and both scanning and transmission electron microscopy. Cellular biomarkers of exposure and/or effect were measured in branchial tissues of T. pavo, and severe lesions such as necrosis, aneurysms and disorganization of the lamellae proportional to the Foroozan exposure periods and concentrations were observed. The main alteration was on the lamellar epithelium, which displayed an irregular profile characterized by pavement cell cytoplasmic protrusion and an alteration of the oxygen chemosensing cells, resulting in impairment of various biological activities. Nevertheless, the ability of specimens to regulate calcium homeostasis and neurotransmission, as well as balance cell turnover, suggests that the species tested to not only survive but also recover in such high crude oil dosage regimen. The identification in gills of histological and neurological changes associated with acute crude oil exposure confirms the utility of the sub-lethal toxicity tests.

[1]  J. Gaddum Probit Analysis , 1948, Nature.

[2]  C. Humphrey,et al.  A simple methylene blue-azure II-basic fuchsin stain for epoxy-embedded tissue sections. , 1974, Stain technology.

[3]  B. McCain,et al.  Chapter 2 – MARINE FISH AND INVERTEBRATE DISEASES, HOST DISEASE RESISTANCE, AND PATHOLOGICAL EFFECTS OF PETROLEUM , 1977 .

[4]  B. McCain,et al.  Bioavailability of Crude Oil from Experimentally Oiled Sediments to English Sole (Parophrys vetulus), and Pathological Consequences , 1978 .

[5]  M. Bradley,et al.  A [Ca2+ + Mg2+]-ATPase and active Ca2+ transport in the plasma membranes isolated from ram sperm flagella , 1980 .

[6]  T. Hinds,et al.  CALMODULIN AND THE PLASMA MEMBRANE CALCIUM PIIMP * , 1980, Annals of the New York Academy of Sciences.

[7]  M. Duey,et al.  Hydromineral balance and gill morphology in rainbow trout Salmo gairdneri, acclimated to fresh and sea water. As affected by petroleum exposure , 1981 .

[8]  Y. Bailly,et al.  Neuroepithelial cells in fish gill primary lamellae. , 1982, Journal of applied physiology: respiratory, environmental and exercise physiology.

[9]  R. Overstreet,et al.  Histopathological changes in two estuarine fishes, Menidia beryllina (Cope) and Trinectes maculatus (Bloch and Schneider), exposed to crude oil and its water‐soluble fractions , 1982 .

[10]  R. Averback,et al.  Ion beam mixing at nickel‐silicon interfaces , 1982 .

[11]  J L Nation,et al.  A new method using hexamethyldisilazane for preparation of soft insect tissues for scanning electron microscopy. , 1983, Stain technology.

[12]  G. Flik,et al.  Ca2+-dependent phosphatase and Ca2+-dependent ATPase activities in plasma membranes of eel gill epithelium--III. Stimulation of branchial high-affinity Ca2+-ATPase activity during prolactin-induced hypercalcemia in American eels. , 1984, Comparative biochemistry and physiology. B, Comparative biochemistry.

[13]  J. Mallatt Fish Gill Structural Changes Induced by Toxicants and Other Irritants: A Statistical Review , 1985 .

[14]  M. Prasad Sensitivity of branchial mucous to crude oil toxicity in a freshwater fish,Colisa fasciatus , 1988, Bulletin of environmental contamination and toxicology.

[15]  C. Weber Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms , 1991 .

[16]  M. Prasad SEM study on the effects of crude oil on the gills and air breathing organs of climbing perch,Anabas testudineus , 1991, Bulletin of environmental contamination and toxicology.

[17]  D. Speare,et al.  Fixation of mucus on rainbow trout (Oncorhynchus mykiss Walbaum) gills for light and electron microscopy , 1992 .

[18]  C. Wood Flux measurements as indices of H+ and metal effects on freshwater fish , 1992 .

[19]  A. El-Shaarawi,et al.  Measuring the potency of pulp mill effluents for induction of hepatic mixed-function oxygenase activity in fish. , 1996, Journal of toxicology and environmental health.

[20]  B. Norcross,et al.  Distribution, abundance, morphological condition, and cytogenetic abnormalities of larval herring in Prince William Sound, Alaska, following the Exxon Valdez oil spill , 1996 .

[21]  A. Kushmaro,et al.  METAMORPHOSIS OF HETEROXENIA FUSCESCENS PLANULAE (CNIDARIA: OCTOCORALLIA) IS INHIBITED BY CRUDE OIL : A NOVEL SHORT TERM TOXICITY BIOASSAY , 1997 .

[22]  T. Wahli,et al.  Histopathology in fish: proposal for a protocol to assess aquatic pollution , 1999 .

[23]  B. Mayer,et al.  Neuronal nitric oxide synthase (nNOS) expression in the epithelial neuroendocrine cell system and nerve fibers in the gill of the catfish, Heteropneustes fossilis. , 1999, Acta histochemica.

[24]  D. Holdway,et al.  Metabolic enzyme activities in fish gills as biomarkers of exposure to petroleum hydrocarbons. , 1999, Ecotoxicology and environmental safety.

[25]  A. Hirashima,et al.  Bioremediation on the Shore after an Oil Spill from the Nakhodka in the Sea of Japan. II. Toxicity of a Bioremediation Agent with Microbiological Cultures in Aquatic Organisms , 2000 .

[26]  H. Tsutsumi,et al.  Bioremediation on the Shore after an Oil Spill from the Nakhodka in the Sea of Japan. I. Chemistry and Characteristics of Heavy Oil Loaded on the Nakhodka and Biodegradation Tests by a Bioremediation Agent with Microbiological Cultures in the Laboratory , 2000 .

[27]  B. Das,et al.  A histopathological study of carp (Labeo rohita) exposed to hexachlorocyclohexane. , 2000 .

[28]  R. Stagg,et al.  Sub-Lethal Effects of Exposure of Juvenile Turbot to Oil Produced Water , 2000 .

[29]  P. Albers Petroleum and Individual Polycyclic Aromatic Hydrocarbons , 2003 .

[30]  G. Maga,et al.  Proliferating cell nuclear antigen (PCNA): a dancer with many partners , 2003, Journal of Cell Science.

[31]  S. W. Bonga,et al.  Degeneration and death, by apoptosis and necrosis, of the pavement and chloride cells in the gills of the teleost Oreochromis mossambicus , 2004, Cell and Tissue Research.

[32]  I. Fearon,et al.  Neuroepithelial oxygen chemoreceptors of the zebrafish gill , 2004, The Journal of physiology.

[33]  P. Hodson,et al.  Oil dispersant increases PAH uptake by fish exposed to crude oil. , 2004, Ecotoxicology and environmental safety.

[34]  G. Nilsson,et al.  Cell proliferation and gill morphology in anoxic crucian carp. , 2005, American journal of physiology. Regulatory, integrative and comparative physiology.

[35]  K. Choe,et al.  The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. , 2005, Physiological reviews.

[36]  S. Ferrando,et al.  Stress factors in the gills of Liza aurata (Perciformes, Mugilidae) living in polluted environments , 2005 .

[37]  I. Ekweozor,et al.  Effect of Size on the Acute Toxicity of Crude Oil to the Mangrove Oyster, Carasostrea gasar , 2005 .

[38]  K. Choe,et al.  Neuronal nitric oxide synthase in the gill of the killifish, Fundulus heteroclitus. , 2006, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[39]  S. Mercer,et al.  Isolation and characterization of putative O2 chemoreceptor cells from the gills of channel catfish (Ictalurus punctatus) , 2006, Brain Research.

[40]  C. Fernandes,et al.  Histopathological gill changes in wild leaping grey mullet (Liza saliens) from the Esmoriz‐Paramos coastal lagoon, Portugal , 2007, Environmental toxicology.

[41]  C. Fernandes,et al.  Heavy metals in water, sediment and tissues of Liza saliens from Esmoriz–Paramos lagoon, Portugal , 2007, Environmental monitoring and assessment.

[42]  I. Perrotta,et al.  Effects of a sublethal concentration of sodium lauryl sulphate on the morphology and Na+/K+ ATPase activity in the gill of the ornate wrasse (Thalassoma pavo). , 2008, Ecotoxicology and environmental safety.

[43]  S. Tanabe,et al.  Toxicogenomic analysis of immune system-related genes in Japanese flounder (Paralichthys olivaceus) exposed to heavy oil. , 2008, Marine pollution bulletin.

[44]  W. Milsom,et al.  A comparative analysis of putative oxygen-sensing cells in the fish gill , 2008, Journal of Experimental Biology.

[45]  J. Soengas,et al.  beta-Naphthoflavone and benzo(a)pyrene alter dopaminergic, noradrenergic, and serotonergic systems in brain and pituitary of rainbow trout (Oncorhynchus mykiss). , 2009, Ecotoxicology and environmental safety.

[46]  R. Anadón,et al.  Extensive presence of serotonergic cells and fibers in the peripheral nervous system of lampreys , 2009, The Journal of comparative neurology.

[47]  A. Gbadebo,et al.  Effects of crude oil and spent oil on Clarias garipinus: a typical marine fish. , 2009 .

[48]  C. Okoro Enhanced Bioremediation of Hydrocarbon Contaminated Mangrove Swamp in the Nigerian Oil Rich Niger Delta using Seawater Microbial Inocula amended with Crude Biosurfactants and Micronutrients , 2010 .

[49]  A. Val,et al.  Acute effects of chemically dispersed crude oil on gill ion regulation, plasma ion levels and haematological parameters in tambaqui (Colossoma macropomum). , 2010, Aquatic toxicology.

[50]  Elena De Domenico,et al.  A multibiomarker approach in Coris julis living in a natural environment. , 2010, Ecotoxicology and environmental safety.

[51]  S. Jung,et al.  Effects of crude oil on marine microbial communities in short term outdoor microcosms , 2010, The Journal of Microbiology.

[52]  Mohamed Hasnain Isa,et al.  Effect of Initial Oil Concentration and Dispersant on Crude Oil Biodegradation in Contaminated Seawater , 2010, Bulletin of environmental contamination and toxicology.

[53]  O. Joel,et al.  Dose-Time Effect of Crude Oil and Hydro-test Effluent on Freshwater and Brackish Water Habitats , 2010 .

[54]  S. Fasulo,et al.  Immunohistochemical and molecular biomarkers in Coris julis exposed to environmental contaminants. , 2010, Ecotoxicology and environmental safety.

[55]  E. Brunelli,et al.  Ultrastructural and immunohistochemical investigation on the gills of the teleost, Thalassoma pavo L., exposed to cadmium. , 2011, Acta histochemica.