Metal concentrations and pathological responses of wild native fish exposed to sewage discharge in a Mediterranean river

Science of the Total Environment

Volumn 449, Issue , 2013, Pages 9-19

  Maceda Veiga, Alberto ^a   Monroy, Mario ^a   Navarro, Elisenda ^a   Viscor, Ginés ^a   de Sostoa, Adolfo ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Haematology; Liver histology; Metals; Native fish; Sewage discharge

Indexed keywords

BIOACCUMULATION PATTERNS; BLOOD ANALYSIS; BLOOD CELLS; BODY CONDITION; CU CONCENTRATIONS; DEVELOPMENT STAGES; DIAGNOSTIC TOOLS; EARLY WARNING SIGNS; ENVIRONMENTAL CONDITIONS; ERYTHROCYTIC NUCLEAR ABNORMALITIES; EXPOSED TO; FISH COMMUNITIES; FISH POPULATIONS; FISH SIZES; FISH SPECIES; FISH TISSUE; HAEMATOCRIT; HAEMATOLOGY; HAEMOGLOBINS; HEALTH DIAGNOSIS; ICHTHYOFAUNA; LEUKOCYTE COUNTS; MEDITERRANEAN RIVERS; METAL CONCENTRATIONS; METALS CONCENTRATIONS; NATIVE FISHES; NATURAL VARIABILITY; NON-LETHAL; PATHOLOGICAL RESPONSE; PB CONCENTRATION; REFERENCE RANGE; SEWAGE DISCHARGES; WATER FRAMEWORK DIRECTIVES;

BIOCHEMISTRY; COPPER; DIAGNOSIS; DIAGNOSTIC PRODUCTS; DISCHARGE (FLUID MECHANICS); ENVIRONMENTAL REGULATIONS; FISH; FISHERIES; HISTOLOGY; LAWS AND LEGISLATION; METALS; MUSCLE; SEWAGE; WATER CONSERVATION;

BLOOD;

CADMIUM; COPPER; IRON; LEAD; MERCURY; NICKEL; ZINC;

BIOACCUMULATION; CONCENTRATION (COMPOSITION); DEVELOPMENTAL STAGE; DISEASE; ENVIRONMENTAL IMPACT; FISH; HEMATOLOGY; HISTOLOGY; PHYSIOLOGICAL RESPONSE; POLLUTION EXPOSURE; RIVER POLLUTION; SEWAGE; TRACE METAL;

ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BIOLOGICAL MONITORING; BLOOD ANALYSIS; BLOOD CELL COUNT; CONCENTRATION (PARAMETERS); ENVIRONMENTAL EXPOSURE; FRESHWATER FISH; HABITUAL ADAPTATION; LIVER HISTOLOGY; NONHUMAN; PRIORITY JOURNAL; RISK ASSESSMENT; SEWAGE; STREAM (RIVER); WATER POLLUTION;

ANIMALS; FISHES; MEDITERRANEAN SEA; METALS; RIVERS; SEWAGE;

MEDITERRANEAN REGION;

EID: 84873528235     PISSN: 00489697     EISSN: 18791026     Source Type: Journal    
DOI: 10.1016/j.scitotenv.2013.01.012     Document Type: Article

References (85)

1. Agamy E. Histopathological liver alterations in juvenile rabbit fish (Siganus canaliculatus) exposed to light Arabian crude oil, dispersed oil and dispersant. Ecotoxicol Environ Saf 2012, 75:171-179.
2. Agtas S., Gey H., Gul S. Concentration of heavy metals in water and chub, Leuciscus cephalus (Linn.) from the river Yildiz, Turkey. J Environ Biol 2007, 28:845-849.
3. Akbulut A., Akbulut N. The study of heavy metal pollution and accumulation in water, sediment, and fish tissue in Kizilirmak River Basin in Turkey. Environ Monit Assess 2010, 167:521-526.
4. Allen-Gil S.M., Martynov V.G. Heavy metal burdens in nine species of freshwater and anadromous fish from the Pechora River, northern Russia. Sci Total Environ 1995, 160:653-659.
5. Almeida J.S., Meletti P.C., Martinez C.B.R. Acute effects of sediments taken from an urban stream on physiological and biochemical parameters of the neotropical fish Prochilodus lineatus. Comp Biochem Physiol Comp Pharmacol 2005, 140:356-363.
6. Altindaǧ A., Yiǧit S. Assessment of heavy metal concentrations in the food web of lake Beyşehir, Turkey. Chemosphere 2005, 60:552-556.
7. Aras M., Bayir A., Sirkecioglu A.N., Polat H., Bayir M. Seasonal variations in serum lipids, lipoproteins and some haematological parameters of chub (Leuciscus cephalus). Ital J Anim Sci 2008, 7:439-448.
8. Bajc Z., Šinigoj-Gačnik K., Jenčič V., Doganoc D.Z. The contents of Cu, Zn, Fe, and Mn in Slovenian freshwater fish. Slov Vet Res 2005, 42(1/2):15-21.
9. Barata C., Fabregat M.C., Cotín J., Huertas D., Solé M., Quirós L., et al. Blood biomarkers and contaminant levels in feathers and eggs to assess environmental hazards in heron nestlings from impacted sites in Ebro basin (NE Spain). Environ Pollut 2010, 158:704-710.
10. Barbour MT, Gerritsen J, Snyder BD, Stribling JB. Rapid Bioassessment Protocols for Use in Streams and Wadeable Rivers: Periphyton, Benthic Macroinvertebrates and Fish, 2a edició. U.S. Environmental Protection Agency, Office of Water, Washington, DC (EPA 841-B-99-002), 1999.
11. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 1995, 57:289-300.
12. Bernet D., Schmidt H., Meier W., Burkhardt-Holm P., Wahli T. Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 1999, 22:25-35.
13. Bervoets L., Blust R. Metal concentrations in water, sediment and gudgeon (Gobio gobio) from a pollution gradient: relationship with fish condition factor. Environ Pollut 2003, 126:9-19.
14. BOE195 ORDEN (Spanish Legislation) 2 Agosto de 1991 por la que se aprueban las normas microbiológicas, los límites de contenido en metales pesados y los métodos analíticos para la determinación de metales pesados para los productos de pesca y de la acuicultura 1991.
15. Bolognesi C., Hayashi M. Micronucleus assay in aquatic animals. Mutagenesis 2011, 26:205-213.
16. Bordajandi L.R., Gómez G., Fernández M.A., Abad E., Rivera J., González M.J. Study on PCBs, PCDD/Fs, organochlorine pesticides, heavy metals and arsenic content in freshwater fish species from the River Turia (Spain). Chemosphere 2003, 53:163-171.
17. Bubb J.M., Lester J.N. Anthropogenic heavy metal inputs to lowland river systems, a case study. The River Stour, U.K. Water Air Soil Pollut 1994, 78:279-296.
18. Campbell L., Verburg P., Dixon D.G., Hecky R.E. Mercury biomagnification in the food web of lake Tanganyika (Tanzania, East Africa). Sci Total Environ 2008, 402:184-191.
19. Casals F. Les comunitats íctiques dels rius mediterranis. Relació amb les condicions ambientals (Fish assemblages of Mediterranean rivers. Relationship with environmental conditions) (In Catalan). PhD Dissertation. University of Barcelona. (2005).
20. Cazenave J., Bacchetta C., Parma M.J., Scarabotti P.A., Wunderlin D.A. Multiple biomarkers responses in Prochilodus lineatus allowed assessing changes in the water quality of Salado River basin (Santa Fe, Argentina). Environ Pollut 2009, 157:3025-3033.
21. Çogun H.Y., Yuzereroglu T.A., Firat O., Gök G., Kargin F. Metal concentrations in fish species from the northeast Mediterranean Sea. Environ Monit Assess 2006, 121:431-438.
22. Costa P.M., Diniz M.S., Caeiro S., Lobo J., Martins M., Ferreira A.M., et al. Histological biomarkers in liver and gills of juvenile Solea senegalensis exposed to contaminated estuarine sediments: a weighted indices approach. Aquat Toxicol 2009, 92:202-212.
23. Croteau M.N., Luoma S.N., Stewart A.R. Trophic transfer of metals along freshwater food webs: evidence of cadmium biomagnification in nature. Limnol Oceanogr 2005, 50:1511-1519.
24. Damásio J.B., Fernández-Sanjuan M., Sánchez-Ávila J., Lacorte S., Prat N., Rieradevall M., et al. Multi-chemical responses of benthic macroinvertebrate species as a complementary tool to diagnose the cause of community impairment in polluted rivers. Water Res 2011, 45:3599-3613.
25. Davis A.K., Maney D.L., Maerz J.C. The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 2008, 22:760-772.
26. Demirak A., Yilmaz F., Levent Tuna A., Ozdemir N. Heavy metals in water, sediment and tissues of Leuciscus cephalus from a stream in southwestern Turkey. Chemosphere 2006, 63:1451-1458.
27. Di Giulio R.T., Hinton D.E. Fish toxicology 2008, CRC Press. Taylor & Francis Group, LLC.
28. Doadrio I., Kottelat M., De Sostoa A. Squalius laietanus, a new species of cyprinid from north-eastern Spain and southern France (Teleostei: Cyprinidae). Ichthyol Explor Freshw 2007, 18:247-256.
29. Dyer S.D., Wang X. A comparison of stream biological responses to discharge from wastewater treatment plants in high and low population density areas. Environ Toxicol Chem 2002, 21:1065-1075.
30. EC Regulation 466/2001 Setting maximum levels for certain contaminants in foodstuffs 2001, [8 March].
31. EC Regulation 78/2005 Amending Regulation (EC) No 466/2001 as regards heavy metals (Pb, Cd and Hg) 2005, [19 January].
32. Ergene S., Cavas T., Celik A., Koleli N., Kaya F., Karahan A. Monitoring of nuclear abnormalities in peripheral erythrocytes of three fish species from the Goksu Delta (Turkey): genotoxic damage in relation to water pollution. Ecotoxicology 2007, 16:385-391.
33. European Commission Directive 2000/60/EC of the European parliament of the council of 23 October 2000 establishing a framework for Community action in the field of water policy. J Eur Communities 2000, L327:1-72.
34. Faller P., Kobler B., Peter A., Sumpter J.P., Burkhardt-Holm P. Stress status of gudgeon (Gobio gobio) from rivers in Switzerland with and without input of sewage treatment plant effluent. Environ Toxicol Chem 2003, 22:2063-2072.
35. Figuerola B., Maceda-Veiga A., De Sostoa A. Assessing the effects of sewage effluents in a Mediterranean creek: fish population features and biotic indices. Hydrobiologia 2012, 694:75-86.
36. García L.V. Escaping the Bonferroni iron claw in ecological studies. Oikos 2001, 1:1.
37. Guilherme S., Válega M., Pereira M.E., Santos M.A., Pacheco M. Erythrocytic nuclear abnormalities in wild and caged fish (Liza aurata) along an environmental mercury contamination gradient. Ecotoxicol Environ Saf 2008, 70:411-421.
38. Gupta A., Rai D., Pandey R., Sharma B. Analysis of some heavy metals in the riverine water, sediments and fish from river Ganges at Allahabad. Environ Monit Assess 2009, 157:449-458.
39. Hinton D.E., Laurén D.J. Integrative histopathological approaches to detecting effects of environmental stressors on fishes. Am Fish Soc Symp 1990, 8:51-66.
40. Hooke J.M. Human impacts on fluvial systems in the Mediterranean region. Geomorphology 2006, 79:311-335.
41. Houston A.H. Review: are the classical hematological variables acceptable indicators of fish health?. Trans Am Fish Soc 1997, 126:879-894.
42. Jorgensen S.E. Handbook of ecological models used in ecosystem and environmental management 2011, Copenhagen University, Denmark.
43. Karadede H., Oymak S.A., Ünlü E. Heavy metals in mullet, Liza abu, and catfish, Silurus triostegus, from the Atatürk Dam Lake (Euphrates). Turk Environ Int 2004, 30:183-188.
44. Koca S., Koca Y., Yildiz Å., Gürcü B. Genotoxic and histopathological effects of water pollution on two fish species, Barbus capito pectoralis and Chondrostoma nasus in the Büyük Menderes River, Turkey. Biol Trace Elem Res 2008, 122:276-291.
45. Lamková K., Simková A., Palíková M., Jurajda P., Lojek A. Seasonal changes of immunocompetence and parasitism in chub (Leuciscus cephalus), a freshwater cyprinid fish. Parasitol Res 2007, 101:775-789.
46. Lavado R., Thibaut R., Raldua D., Martin R., Porte C. First evidence of endocrine disruption in feral carp from the Elbro River. Toxicol Appl Pharmacol 2004, 196:247-257.
47. Lavado R., Ureña R., Martin-Skilton R., Torreblanca A., Ramo J., Raldúa D., et al. The combined use of chemical and biochemical markers to assess water quality along the Ebro River. Environ Pollut 2006, 139:330-339.
48. Legendre P., Legendre P. Numerical ecology 1998, Elsevier Science. 2nd English ed.
49. Linde A.R., Sánchez-Galán S., Izquierdo J.I., Arribas P., Marañón E., García-Vázquez E. Brown trout as biomonitor of heavy metal pollution: effect of age on the reliability of the assessment. Ecotoxicol Environ Saf 1998, 40:120-125.
50. Llorente M.T., Martos A., Castaño A. Detection of cytogenetic alterations and blood cell changes in natural populations of carp. Ecotoxicology 2002, 11:27-34.
51. Lukin A., Sharova J., Belicheva L., Camus L. Assessment of fish health status in the Pechora River: effects of contamination. Ecotoxicol Environ Saf 2011, 74:355-365.
52. Maceda-Veiga A. Towards the conservation of freshwater fish: Iberian rivers as an example of threats and management practices. Rev Fish Biol Fish 2012, 10.1007/s11160-012-9275-5.
53. Maceda-Veiga A., De Sostoa A. Observational evidence of the sensitivity of some fish species to environmental stressors in Mediterranean rivers. Ecol Indic 2011, 11:311-317.
54. Maceda-Veiga A., Salvadó H., Vinyoles D., De Sostoa A. Outbreaks of Ichthyophthirius multifiliis in Redtail Barbs Barbus haasi in a Mediterranean Stream during Drought. J Aquat Anim Health 2009, 21:189-194.
55. Maceda-Veiga A., Monroy M., Viscor G., De Sostoa A. Changes in non-specific biomarkers in the Mediterranean barbel (Barbus meridionalis) exposed to sewage effluents in a Mediterranean stream (Catalonia, NE Spain). Aquat Toxicol 2010, 100:229-237.
56. Maceda-Veiga A., Monroy M., De Sostoa A. Metal bioaccumulation in the Mediterranean barbel (Barbus meridionalis) in a Mediterranean River receiving effluents from urban and industrial wastewater treatment plants. Ecotoxicol Environ Saf 2012, 76:93-101.
57. Majno G., Joris I. Cells, tissues and disease 2004, Oxford University Press.
58. Marcovecchio J.E., Moreno V.J., Pérez A. Metal accumulation in tissues of sharks from the Bahía Blanca estuary, Argentina. Mar Environ Res 1991, 31:263-274.
59. Mas-Martí E., García-Berthou E., Sabater S., Tomanova S., Muñoz I. Comparing fish assemblages and trophic ecology of permanent and intermittent reaches in a Mediterranean stream. Hydrobiologia 2010, 657:167-180.
60. Mendiguchía C., Moreno C., García-Vargas M. Evaluation of natural and anthropogenic influences on the Guadalquivir River (Spain) by dissolved heavy metals and nutrients. Chemosphere 2007, 69:1509-1517.
61. Miller P.A., Munkittrick K.R., Dixon D.G. Relationship between concentrations of copper and zinc in water, sediment, benthic invertebrates, and tissues of white sucker (Catastomus commersoni). Can J Fish Aquat Sci 1992, 49:978-984.
62. Navarro A., Font X. Discriminating different sources of groundwater contamination caused by industrial wastes in the Besós River Basin, Barcelona, Spain. Appl Geochem 1993, 8:277.
63. Ozmen M., Ayas Z., Güngördü A., Ekmekci G.F., Yerli S. Ecotoxicological assessment of water pollution in Sariyar Dam Lake, Turkey. Ecotoxicol Environ Saf 2008, 70:163-173.
64. Pacheco M., Santos M.A. Biotransformation, genotoxic, and histopathological effects of environmental contaminants in European eel (Anguilla anguilla L.). Ecotoxicol Environ Saf 2002, 53:331-347.
65. Prat N., Munné A. Water use and quality and stream flow in a Mediterranean stream. Water Res 2000, 34:3876-3881.
66. R Development Core Team R: a language and environment for statistical computing 2012, R Foundation for Statistical Computing, Vienna, Austria, [http://www.R-project.org/].
67. Revelle W. Psych: procedures for personality, psychometric, and psychological research. R package version 1.0-58 2008.
68. Ribeiro C.A.O., Vollaire Y., Sanchez-Chardi A., Roche H. Bioaccumulation and the effects of organochlorine pesticides, PAH and heavy metals in the Eel (Anguilla anguilla) at the Camargue Nature Reserve, France. Aquat Toxicol 2005, 74:53-69.
69. Ricart M., Guasch H., Barceló D., Brix R., Conceição M.H., Geiszinger A., et al. Primary and complex stressors in polluted Mediterranean rivers: pesticide effects on biological communities. J Hydrol 2010, 383:52-61.
70. Rough K.M., Nowak B.F., Reuter R.E. Haematology and leukocyte morphology of wild caught Thunnus maccoyii. J Fish Biol 2005, 66:1649-1659.
71. Sabater S., Muñoz I., Feio M.J., Romaní A.M., Graça M.A.S. The Iberian rivers. Rivers of Europe 2009, Chapter 4, Elsevier Science and Technology, Amsterdam. K. Tockner, C.T. Robinson, U. Uehlinger (Eds.).
72. Singh N., Srivastava A. Haematological parameters as bioindicators of insecticide exposure in teleosts. Ecotoxicology 2010, 19:838-854.
73. Smith K.G., Darwall W.R.T. The status and distribution of freshwater fish endemic to the Mediterranean basin 2006, IUCN, Gland, Switzerland/Cambridge, UK.
74. Sörme L., Lagerkvist R. Sources of heavy metals in urban wastewater in Stockholm. Sci Total Environ 2002, 298:131-145.
75. Sostoa A., Vinyoles D., Casals F., et al. Història Natural dels Països Catalans. Peixos 1990, 487. Fundació Enciclopèdia, Catalana, Barcelona.
76. Sostoa A., Maceda-Veiga A., Figuerola B., Vinyoles D. Study of the biodiversity, ecological status and water quality of Ripoll River in Sabadell. Ajuntament de Sabadell. Technical report 2007, 42. (In Catalan).
77. Takashima F., Hibiya T. An atlas of fish histology. Normal and pathological features, Tokyo, Japan 1995.
78. Tavares-Dias M. A morphological and cytochemical study of erythrocytes, thrombocytes and leukocytes in four freshwater teleosts. J Fish Biol 2006, 68:1822-1833.
79. Van der Oost R., Lopes S.C.C., Komen H., Satumalay K., van den Bos R., Heida H., et al. Assessment of environmental quality and inland water pollution using biomarker responses in caged carp (Cyprinus carpio): use of a bioactivation: detoxication ratio as a Biotransformation Index (BTI). Mar Environ Res 1998, 46:315-319.
80. Van der Oost R., Beyer J., Vermeulen N.P.E. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 2003, 13:57-149.
81. Van Rijn J.A., Reina R.D. Distribution of leukocytes as indicators of stress in the Australian swellshark Cephaloscyllium laticeps. Fish Shellfish Immunol 2010, 29:534-538.
82. Vié J., Hilton-Taylor C., Stuart S.N. Wildlife in a changing world-an analysis of the 2008 IUCN Red List of threatened species 2009, IUCN, Gland.
83. Vörösmarty C.J., McIntyre P.B., Gessner M.O., Dudgeon D., Prusevich A., Green P., et al. Global threats to human water security and river biodiversity. Nature 2010, 467:555-561.
84. Yilmaz F., Özdemir N., Demirak A., Tuna A.L. Heavy metal levels in two fish species Leuciscus cephalus and Lepomis gibbosus. Food Chem 2007, 100:830-835.
85. Yilmaz A.B., Sangün M.K., Yaǧlioǧlu D., Turan C. Metals (major, essential to non-essential) composition of the different tissues of three demersal fish species from Iskenderun Bay, Turkey. Food Chem 2010, 123:410-415.