Abstract
As a component of a large research project to evaluate the effects of contaminants on fish health in the field, histopathological studies have been conducted to help establish causal relationship between pollutants (heavy metals and aromatic polycyclic hydrocarbons—PAHs) and histopathological responses in Senegal sole, Solea senegalensis, from an estuary of SW Spain. Heavy metals (As, Zn, Cd, Pb, Cu and Fe) and 16 PAHs (proprietary USEPA) concentrations in water, sediment and tissues (liver and gills) and histopathological alterations in S. senegalensis from three sampling sites of Ria de Huelva estuary during 2004–2006 years have been analysed. The histopathological studies revealed seasonal and spatial differences in the lesion grade of alterations observing the highest lesion grades in fish from Odiel River and autumn season. No significant differences were observed in the alterations prevalence between sampling sites, but significant differences were observed between seasons observing the highest prevalence in autumn season. However, calculated IPAT demonstrated a low–moderate impact of pollutants on health fish. Correlations between histopathological alterations and pollutants analysed were observed being heavy metals the group that presented a major number of correlations with alterations in several organs of S. senegalensis. In evaluating the general health of fish, the use of histopathological studies in recommended for making more reliable assessment of biochemical responses in fish exposed to a variety of environmental stressors. Statistical analysis using semiquantitative data on pathological lesions can help to establish correlation between cause (stressor) and effect (biomarker).
Similar content being viewed by others
References
Adams SM, Brown AM, Goede RW (1993) A quantitative health assessment index for rapid evaluation of fish condition in the field. T Am Fish Soc 122:63–73
Adams SM, Greeley MS, McHugh Law J, Noga EJ, Zelikoff JT (2003) Application of multiple sublethal stress indicators to assess the health of fish in Pamlico Sound following extensive flooding. Estuaries 26(5):1365–1382
Alazemi BM, Lewis JW, Andrews EB (1996) Gill damage in the freshwater fish Gnathonemus petersii (Family: Mormyridae) exposed to selected pollutants: an ultrastructural study. Environ Technol 17:225–238
Alvarado NE, Quesada I, Hylland K, Marigómez I, Soto M (2006) Quantitative changes in metallothionein expression in target cell-types in the gills of turbot (Scophthalmus maximus) exposed to Cd, Cu, Zn and after a depuration treatment. Aquat Toxicol 77(1):64–77
Arellano JM, Storch V, Sarasquete C (1999) Histological changes and copper accumulation in liver and gills of the Senegal sole, Solea senegalensis. Ecotox Environ Safe 44:62–72
Au DWT (2004) The application of histo-cytopathological biomarkers in marine pollution monitoring: a review. Mar Pollut Bull 48:817–834
Azcue JM (1993) Metales en Sistemas Biológicos: Metales en el medio Ambiente, Ed. PPU, Barcelona
Bartik M, Piskac A (1981) Veterinary toxicology. Elsevier, Amsterdam, pp 82–89
Becker DS, Ginn TC, Landolt ML, Powell DB (1987) Hepatic lesions in English sole (Parophrys vetulus) from Commencement Bay, Washington, DC. Mar Environ Res 23:153–173
Bernet D, Schmidt H, Meier W, Burkhardt-Holm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22:25–34
BOJA (1997) num. 27 de 4/3/1997. Orden de 14 de febrero de 1997, por la que se clasifican las aguas afectadas directamente por vertidos, en desarrollo del Decreto 14/1996, de 16 de enero, por el que se aprueba el Reglamento de calidad de aguas litorales, pp 2591–2598
Bunton TE, Frazier JM (1994) Extrahepatic tissue copper concentrations in white perch with hepatic copper storage. J Fish Biol 45:627–640
Canadian Council of Minister of the Environment (2001) Canadian sediment quality guidelines for the protection of aquatic life: Summary tables. ISBN 1-896997-34-1
CEFAS (1998) Monitoring and surveillance of non-radioactive contaminants in the aquatic environment and activities regulating the disposal of wastes at sea, 1995 and 196. Science Series, Aquatic Environment monitoring Report No. 51. CEFAS, Lowestoft
Chang S, Zdanowicz VS, Murchelano RA (1998) Associations between liver lesions in winter flounder (Pleuronectes americanus) and sediment chemical contaminants from north-east United States estuaries. ICES J Mar Sci 55:954–969
Costa PM, Diniz MS, Caeiro S, Lobo J, Martins M, Ferreira AM, Caetano M, Vale C, DelValls TA, Costa MH (2009) Histological biomarkers in liver and gills of juvenile Solea senegalensis exposed to contaminated estuarine sediments: a weighted indices approach. Aquat Toxicol 92:202–212
Davidson MC, Lorna EW, Ure AM (1999) Effect of sample preparation on the operational speciation of cadmium and lead in freshwater sediment. Fresen J Anal Chem 363:134–136
De Flora S, Bagnasco M, Zanacchi P (1991) Genotoxic, carcinogenic and teratogenic hazards in the marine environment, with special reference to the Mediterranean Sea. Mutat Res 258:285–320
Delatim Simonato J, Guedes CLB, Martínez CBR (2008) Biochemical, physiological, and histological changes in the neotropical fish Prochilodus lineatus exposed to diesel oil. Ecotox Environ Safe 69:112–120
Dinis MT (1992) Aspects of the potential of Solea senegalensis Kaup for aquaculture: larval rearing and weaning to an artificial diet. Aquacult Fish Manage 23:179–183
Drake PA, Arias M, Rodríguez A (1984) Cultivo extensivo de peces marinos en los esteros de las salinas de San Fernando (Cádiz): II. Características de la producción de peces. Fisheries Research Institute (Spain) (Technical Report) 116:1–23
Farag AM, Boese CJ, Woodward DR, Bergman HL (1994) Physiological changes and tissue metal accumulation in rainbow trout exposed to foodborne and waterborne metals. Environ Toxicol Chem 13:2021–2029
Fernandes C, Fontainhas-Fernandes A, Monteiro SM, Salgado MA (2007) Histopathological gill changes in wild leaping grey mullet (Liza saliens) from the Esmoriz-Paramos coastal lagoon, Portugal. Environ Toxicol, pp 443–448
Fernandes C, Fontainhas-Fernandes A, Ferreira M, Salgado MA (2008) Oxidative stress response in gill and liver of Liza saliens, from the Esmoriz-Paramos coastal lagoon, Portugal. Arch Environ Con Tox 55:262–269
Förstner U, Wittmann GTW (1983) Metal pollution in the aquatic environment, second revised edition. Springer, Berlin
Fowle JR Jr, Abernathy CO, Mass MJ, McKinney JD, North DW, Ohanian EV, Uthus E (1992) Arsenic health research needs. In: Beck BD (ed) Trace substances in environmental health, vol XXV., Gradient CorporationCambridge, Massachusetts, pp 257–271
Froese R, Pauly D (2010) Fishbase. Worl Wide Web Electronic Publication. www.fishbase.org
Fu H, Steinbach OM, Van den Hamer CJA, Balm PHM, Lock RAC (1990) Involvement of cortisol and metallothionein-like proteins in the physiological responses to tilapia (Oreochromis mossambicus) to sublethal cadmium stress. Aquat Toxicol 16:257–270
Gagnon MM, Holdway DA (2000) EROD induction and biliary metabolite excretion following exposure to the water accomodated fraction of crude oil and to chemically dispersed crude oil. Arch Environ Contam Toxicol 38:70–77
Giari L, Manera M, Simoni E, Dezfuli BS (2007) Cellular alterations in different organs of European sea bass Dicentrarchus labrax (L.) exposed to cadmium. Chemosphere 67:1171–1181
Gilderhus PA (1966) Some effects of sublethal concentrations of sodium arsenite on bluegills and the aquatic environment. Trans Am Fish Soc 95:289–296
Gutiérrez M (1967) Coloración histológica para ovarios de peces, crustáceos y moluscos. Investigaciones Pesqueras 31(2):265–271
Hemalatha S, Banerjee TK (1997) Histopathological analysis of sublethal toxicity of zinc chloride to the respiratory organs of the airbreathing catfish Heteropneustes fossilis (Bloch). Biol Res 30(1):11–21
Hindmarsh JT, McCurdly RF (1986) Clinical and environmental aspects of arsenic toxicity. CRC Crit Rev Clin Lab Sci 23:315–347
Irwin H, van Mouwerick M, Stevens L, Seese M, Bashman W (1997) Environmental contaminants encyclopaedia: lead, cadmium, zinc, mercury and nickel. National Park Service
Jagoe CH, Faivre A, Newman MC (1996) Morphological and morphometric changes in the gills of mosquitofish (Gambusia holbrooki) after exposure to mercury (II). Aquat Toxicol 34:163–183
Jimenez-Tenorio N, Morales-Caselles C, Kalman J, Salamanca MJ, González de Canales ML, Sarasquete C, Del Valls TA (2007) Determining sediment quality for regulatory proposes using fish chronic bioassays. Environ Int 33:474–480
Jimenez-Tenorio N, Salamanca MJ, Garcia-Luque E, Gonzalez de Canales ML, Del Valls TA (2008) Chronic bioassay in benthic fish for the assessment of the quality of sediments in different areas of the coast of Spain impacted by acute and chronic oil spills. Environ Toxicol 23(5):634–642
Johnson LL, Stehr CM, Olson OP, Myers MS, McCain BB, Chan SL, Varanasi U (1992) National Status and Trends Program, National Benthic Surveillanc Project, Northeast Coast. Fish histopathology and relationships between lesions and chemical contaminants (1987–1989). NOAA Tech Mem NMFS-NWFC-4
Kamer TT (1994) Dutch standards for contaminated sediments. Evaluatienota Water 21(250):27–28
Karlsson-Norrgren L, Runn P, Haux C, Forlin L (1985) Cadmium induced changes in gill morphology of zebrafish, Brachydanio rerio (Hamilton-Buchanan), and rainbow trout, Salmo gairdneri. J Fish Biol 27:81–95
Khan RA (1998) Influence of petroleum at a refinery terminal on winter flounder, Pleuronectes americanus. B Environ Contam Tox 61:770–777
Khan RA (1999) Study of pearl date (Margariscus margarita) inhabiting a Stillwater pond contaminated with diesel fuel. B Environ Contam Tox 62:638–645
Khan RA (2003) Health of flatfish from localities in Placentia Bay, Newfoundland, contaminated with petroleum and PCBs. Arch Environ Con Tox 44:485–492
Kirby MF, Lyons BP, Waldock MJ, Woodhead RJ, Goodsir F, Law RJ, Matthiessen P, Neall P, Stewart C, Thain JT, Tylor T, Feist SW (2000) Biomarkers of polycyclic aromatic hydrocarbon (PAH) exposure in fish and their application in marine monitoring. Centre for Environment, Fisheries and Aquaculture Science, Lowestoft, UK. Science Series Technical. Report 110:30
Kotsanis N, Iliopoulou-Georgudaki J (1999) Arsenic induced liver hyperplasia and kidney fibrosis in rainbow trout (Oncorhynchus mykiss) by microinjection technique: a sensitive animal bioassay for environmental metal-toxicity. Bull Environ Contaminat Toxicol 62:169–178
Lanno RP, Hicks B, Hilton JW (1987) Histological observations on intrahepatocytic copper-containing granules in rainbow trout reared on diets containing elevated levels of copper. Aquat Toxicol 10:251–263
Lauren DJ, McDonald DG (1985) Effects of copper on branchial ionoregulation in the rainbow trout, Salmo gairdneri. Richardson J Comp Physiol 13:635–644
Laurent P, Perry SF (1991) Environmental effects on fish gill morphology. Physiol Zool 53:4–25
Loganathan K, Velmurugan B, Hongray Howrelia J, Selvanayagam M, Patnaik B (2006) Zinc induced histological changes in brain and liver of Labeo rohita (Ham.). J Environ Biol 27(1):107–110
Long ER, MacDonald DD, Smith SL, Calder FD (1995) Incidence of adverse biological effects within ranges of chemical concentrations in marine and estuarine sediments. Environ Manage 19:81–87
MacDonald DD, Ingersoll CG, Berger TA (2000) Development and evaluation of consensus-based sediment quality guidelines for freshwater ecosystem. Arch Environ Contam Toxicol 39:20–31
Mallat J (1985) Fish gill structural changes induced by toxicants and other irritants: a statistical review. Can J Fish Aquat Sci 42:630–648
Malins DC, Krahn MM, Brown DW, Rhodes LD, Myers MS, McCain BB, Chan S-L (1985) Toxic chemicals in marine sediment and biota from Mukilteo, Washington: relationships with hepatic neoplasms and other hepatic lesions in English sole (Parophrys vetulus). J Natl Cancer Inst 74:487–494
Martínez CBR, Nagae MY, Zaia CTBV, Zaia DAM (2004) Acute morphological and physiological effects of lead in the neotropical fish Prochilodus lineatus. Braz J Biol 64(4):797–807
Matthiessen P, Thain JE, Law RJ, Fileman TW (1993) Attempts to assess the environmental hazard posed by complex mixtures of organic chemicals in UK estuaries. 26:90–95. Mar Pollut Bull 26:90–95 Ontario. Can J Fish Aquat Sci 45:2161-2167
McGeachy SM, Dixon DG (1990) Effect of temperature on the chronic toxicity of arsenate to rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 47:2228–2234
Metcalf CD, Cairns VW, Fitzsimons JD (1988) Experimental induction of liver tumours in rainbow trout (Salmo gairdneri) by contaminated sediment from Hamilton harbour Ontario. Can J Fish Aquat Sci 45:2161–2167
Moore MJ, Smolowitz RM, Stegeman JJ (1997) Stages of hydropic vacuolation in the liver of winter flounder Pleuronectes americanus from a chemically contaminated site. Dis Aquat Organ 31:19–28
Myers MS, Rhodes LD, McCain BB (1987) Pathologic anatomy and patterns of occurrence of hepatic neoplasms, putative preneoplastic lesions and other idiopathic hepatic conditions in English sole (Parophrys vetulus) from Puget Sound, Washington, USA. J Natl Cancer I 78:333–363
Myers MS, Olson OP, Johnson LL, Stehr CM, Hom T, Varanasi U (1992) Hepatic lesions other than neoplasms in subadult flatfish from Puget Sound, Washington: relationships with indices of contaminant exposure. Mar Environ Res 34:45–51
Myers MS, Stehr CM, Olson OP, Johnson LL, McCain BB, Chan SL, Varanasi U (1994) 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. Environ Health Persp 102:200–215
Neiboer E, Richardson DHS (1980) The replacement of the nondescript term “heavy metals” by a biologically and chemically significant classification of metal ions. Environ Pollut B 1:3–26
NOOA SQuiRTs (Screening Quick Reference Tables). Office of response and restoration: NOAA’s National Ocean Service. http://response.restoration.noaa.gov
Okada S, Yamanaka K (1994) Induction of lung-specific DNA damage by methylarsenics via the production free radicals. In: Nriagu JO (ed) Arsenic in the environment, Part II, Human Health and Ecosystem Effects. Wiley, London, pp 143–157
Oliva M, Garrido MC, Sales Márquez D, González de Canales ML (2009) Sublethal and lethal toxicity in juvenile Senegal sole (Solea senegalensis) exposed to copper: a preliminary toxicity range-finding test. Exp Toxicol Pathol 61(2):113–121
Oliveira Ribeiro CA, Belger L, Pelletier E, Rouleau C (2002) Histopathological evidence of inorganic mercury and methylmercury toxicity in the arctic charr (Salvelinus alpinus). Environ Res 83:286–292
Oronsaye JAO (1989) Histological changes in the kidneys and gills of the stickleback, Gasterosteus aculeatus L, exposed to dissolved cadmium in hard water. Ecotox Environ Safe 17:279–290
Part P, Svanberg O, Kiessling A (1985) The availability of cadmium to perfused rainbow trout gills in different water qualities. Water Res 19:427–434
Pedlar RM (2000) The accumulation, distribution and toxicological effects of arsenic in lake whitefish (Coregonus clupeaformis) and lake trout (Salvelinus namacycush) exposed by the dietary route of uptake. M. Sc. Thesis. Department of Zoology, University of Manitoba. Winnipeg, Manitoba, p 150
Pedlar RM, Ptashynski MD, Evans R, Klaverkamp JF (2002) Toxicological effects of dietary arsenic exposure in lake whitefish (Coregonus clupeaformis). Aquat Toxicol 57:167–189
Pratap HB, Wendelaar Bonga SE (1993) 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. Aquat Toxicol 26:133–150
Randi AS, Monserrat JM, Rodríguez EM, Romano LA (1996) Histopathological effects of cadmium on the gills of the freshwater fish, Macropsobrycon uruguayanae Eigenmann (Pisces, Atherinidae). J Fish Dis 19:311–322
Rankin MG, Dixon DG (1994) Acute and chronic toxicity of waterborne arsenite to rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 51:372–380
Reid SD, McDonald DG (1991) Metal binding activity of the gills of rainbow trout (Oncohrynchus mykiss). Can J Fish Aquat Sci 48:1061–1068
Robbins SL, Cotran RS (1984) Patología Estructural y Funcional. Intramericana, Madrid, pp 226–228
Roncero V, Vincente JA, Redondo E, Gãzquez A, Duran E (1990) Experimental lead nitrate poisoning: microscopic and ultrastructural study of the gills of tench (Tinca tinca, L.). Environ Health Perspet 89:137–144
Roncero V, Durán E, Soler F, Masot J, Gómez L (1992) Morphometric, structural and ultrastructural studies of tench (Tinca tinca L.) hepatocytes after copper sulphate administration. Environ Res 57:45–58
Roy LA, Steinert S, Bay SM, Greenstein D, Sapozhnikova Y, Bawardi O, Leifer I, Schlenk D (2003) Biochemical effects of petroleum exposure in hornyhead turbot (Pleuronichthys verticalis) exposed to a gradient of sediments collected from a natural petroleum seep in CA, USA. Aquat Toxicol 65:159–169
Sarasquete C, González de Canales ML, Arellano JM, Muñoz-Cueto JA, Ribeiro L, Dinis MT (1998) Histochemical study of skin and gills of Senegal sole, Solea senegalensis larvae and adults. Histo Histopathol 13:727–735
Schwaiger J, Wanke R, Adam S, Pawert M, Honnen W, Triebskorn R (1997) The use of histoapthological indicators to evaluate contaminant-related stress in fish. J Aquat Ecosyst Stress Recovery 6:75–86
Shaw JR, Gabor K, Hand E, Lankowski A, Durant L, Thigodeau R, Stanton C, Barnaby R, Coutermarsh B, Karlson K, Sato D, Hamilton JW, Stanton BA (2007) Role of glucocorticoid receptors in acclimation of killfish (Fundulus heteroclitus) to seawater and effects of arsenic. Am J Physiol 292:1052–1060
Shiomi K, Sugiyama Y, Shimakura K, Nagashima Y (1996) Retention and biotransformation of arsenic compounds administered intraperitoneally to carp. Fish Sci 62:262–266
Simpson MG, Parry M, Kleinkauf D, Swarbreck D, Walker P, Leah RT (2000) Pathology of the liver, kidney and gonad of flounder (Platichthys flesus) from a UK estuary impacted by endocrine disrupting chemicals. Mar Environ Res 50:283–287
Sorenson EMB (1991) Arsenic. In: Sorenson EMB (ed) Metal poisoning in fish. CRC Press, London, pp 61–99
Sorenson EMB, Ramírez-Mitchell R, Harlan CW, Bell JS (1980) Cytological changes in fish liver following chronic, environmental arsenic exposure. Bull Environ Contaminat Toxicol 25:93–99
Spies RB, Davis PH, Stuerner DH (1980) Ecology of a petroleum seep off the California coast. In: Geyer R (ed) Marine environmental pollution. Elsevier, Amsterdam, pp 229–263
Stehr CM, Myers MS, Burrows D, Krahn MM, Meador J, McCain BB, Varanasi U (1997) Chemical contamination and associated liver diseases in two species of fish from San Francisco Bay and Bodega Bay. Ecotoxicology 6:35–65
Stehr CM, Johnson LL, Myers MS (1998) Hydropic vacuolation in the liver of three species of fish from the U.S. West Coast: lesion description and risk assessment associated with contaminant exposure. Dis Aquat Organ 32:119–135
Stentiford GD, Longshaw M, Lyons BP, Jones G, Green M, Feist SW (2003) Histopathological biomarkers in estuarine fish species for the assessment of biological effects of contaminants. Mar Environ Res 55:137–159
Styblo M, Del Razo LM, LeCluyse EL, Hamilton GA, Wang C, Cullen WR, Thomas DJ (1999) Metabolism of arsenic in primary cultures of human and rat hepatocytes. Chem Res Toxicol 12:560–565
The SJ, Adams SM, Hinton DE (1997) Histopathological biomarkers in feral freshwater fish populations exposed to different types of contaminant stress. Aquat Toxicol 37:51–70
Thophon S, Kruatrachue M, Upatham ES, Pokethitiyook P, Ssahaphong S, Jaritkhuan S (2003) Histopathological alterations of white seabass, Lates calcarifer, in acute and subchronic cadmium exposure. Environ Pollut 121:307–320
USEPA (United States Environmental Protection Agency) (2002) National Recommended Water Quality Criteria. EPA-822-R-02-047, Office of Science and Technology
Usha Rani A (1986) Effect of cadmium on some aspects of physiology and histology in the edible freshwater teleost, Tilapia mossambica (Peters). Thesis. Sri Venkateswara University, Tirupati
Usha Rani A, Ramamurthi R (1989) Histopathological alterations in the liver of freshwater teleost tilapia mossambica in response to cadmium toxicity. Ecotox Environ Safe 17:221–226
Van Dyk JC, Pieterse GM, Van Vuren JHJ (2007) Histological changes in the liver of Oreochromis mossambicus (Cichlidae) after exposure to cadmium and zinc. Ecotox Environ Safe 66(3):432–440
Verbost PM, Flik G, Lock RAC, Wendelaar Bonga SE (1987) Cadmium inhibition of Ca2+ uptake in rainbow trout gills. Am J Physiol 253:216–221
Verbost PM, Van Rooij J, Flik G, Lock RAC, Wendelaar Bonga SE (1989) The movement of cadmium through freshwater trout branchial epithelium and its interference with calcium transport. J Exp Biol 145:185–197
Vethaak AD, Wester PW (1996) Diseases of flounder Platichthys flesus in Dutch coastal and estuarine waters, with particular reference to environmental stress factors. II. Liver histopathology. Dis Aquat Org 26:99–116
Vethaak AD, Jol JG, Meijboom A, Eggens ML, Rheinhalt T, Wester PW, Van de Zande T, Bergman A, Dankers N, Ariese F, Baan RA, Everts JM, Opperhuizen A, Marquenie JM (1996) Skin and liver diseases induced in flounder (Platichthys flesus) after long-term exposure to contaminated sediments in large-scale mesocosms. Environ Health Perspect 104:1218–1229
Vicente Martorell JJ, Galindo-Riaño MD, García-Vargas M, Castro-Granado D (2009) Bioavailability of heavy metals monitoring water, sediments and fish species from a polluted estuary. J Hazard Mater 162:823–836
Wangsongsak A, Utarnpongsa S, Kruatrachue M, Ponglikitmongkol M, Pokethitiyook P, Sumranwanich T (2007) Alterations of organ histopathology and metallothionein mRNA expression in silver barb, Puntius gonionotus during subchronic cadmium exposure. J Environ Sci 19:1341–1348
Wicklund-Glynn A, Norrgren L, Mussener A (1994) Differences in uptake of inorganic mercury and cadmium in the gills of the zebrafish, Brachydanio rerio. Aquat Toxicol 30:13–26
Williams GM, Weisburger JH (1986) Chemical carcinogens. In: Klaassen CD, Amdur MO, Doull J (eds) Casarett and Dloull’s toxicology. Macmillan, New York, pp 99–173
Yamauchi H, Fowler BA (1994) Toxicity and metabolism o inorganic and methylated arsenicals. In: Nriagu JO (ed) Arsenic in the environment, Part II: Human health and ecosystem effects. Wiley, London, pp 35–91
Acknowledgments
This work has been supported by Project SEAPAT: “Biomarkers and histopathology in gilthead seabream, Sparus aurata, and Senegal sole, Solea senegalensis,” (CICYT, REN 2003-09361-CO3-03) and by Project SEAMET: “Bioavailability of heavy metals in aquatic ecosystems affected by diffuse pollution” (CICYT, REN 2003-09361-CO3-02, Spain Government). This is the CEIMAR journal publication 15.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Oliva, M., Vicente-Martorell, J.J., Galindo-Riaño, M.D. et al. Histopathological alterations in Senegal sole, Solea Senegalensis, from a polluted Huelva estuary (SW, Spain). Fish Physiol Biochem 39, 523–545 (2013). https://doi.org/10.1007/s10695-012-9717-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-012-9717-y