Parasite communities in the red mullet, Mullus barbatus L., respond to small-scale variation in the levels of polychlorinated biphenyls in the Western Mediterranean

Marine Pollution Bulletin

Volumn 64, Issue 9, 2012, Pages 1853-1860

  Carreras Aubets, Marta ^a   Montero, Francisco Esteban ^b   Kostadinova, Aneta ^c,d   Carrassón, Maite ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSITY OF VALENCIA   (Spain)

^c INSTITUTE OF PARASITOLOGY   (Czech Republic)

^d INSTITUTE OF BIODIVERSITY AND ECOSYSTEM RESEARCH   (Bulgaria)

Author keywords

Abundance; Mullus barbatus; Parasite communities; Polychlorinated biphenyls; Similarity; Western Mediterranean

Indexed keywords

ABUNDANCE; MULLUS BARBATUS; PARASITE COMMUNITIES; SIMILARITY; WESTERN MEDITERRANEAN;

ORGANIC POLLUTANTS; SEDIMENTOLOGY;

POLYCHLORINATED BIPHENYLS;

POLYCHLORINATED BIPHENYL DERIVATIVE;

ABUNDANCE; BIOMARKER; COMMUNITY DYNAMICS; COMMUNITY STRUCTURE; FISH; LIFE CYCLE; NEMATODE; PARASITE; PCB; POPULATION DYNAMICS; SHELF SEDIMENT;

ARTICLE; BIOLOGICAL MONITORING; COMMUNITY STRUCTURE; CONCENTRATION (PARAMETERS); ECTOPARASITE; ENDOPARASITE; FISH; HYSTEROTHYLACIUM; HYSTEROTHYLACIUM FABRI; INDICATOR ORGANISM; MULLUS BARBATUS; NONHUMAN; OPECOELOIDES FURCATUS; PARASITE; PARASITE EXAMINATION; PARASITE IDENTIFICATION; PARASITE TRANSMISSION; POPULATION ABUNDANCE; SPECIES COMPOSITION; SPECIES DIVERSITY;

ANIMALS; ENVIRONMENTAL MONITORING; HELMINTHS; MEDITERRANEAN SEA; PARASITES; POLYCHLORINATED BIPHENYLS; SEASONS; SMEGMAMORPHA; WATER POLLUTANTS, CHEMICAL; WATER POLLUTION, CHEMICAL;

MEDITERRANEAN SEA; MEDITERRANEAN SEA (WEST);

HYSTEROTHYLACIUM; MULLIDAE; MULLUS BARBATUS; OPECOELOIDES FURCATUS;

EID: 84865394109     PISSN: 0025326X     EISSN: 18793363     Source Type: Journal    
DOI: 10.1016/j.marpolbul.2012.06.008     Document Type: Article

References (66)

1. Anderson R.C. Nematode Parasites of Vertebrates. Their Development and Transmission 2000, CAB International, Wallingford, Oxon, UK. 2nd ed.
2. Anderson M.J., Gorley R.N., Clarke K.R. PERMANOVA+ for PRIMER: Guide to software and statistical methods 2008, PRIMER-E, Plymouth, UK.
3. Bartoli P., Gibson D.I., Bray R.A. Digenean species diversity in teleost fish from a nature reserve off Corsica, France (Western Mediterranean), and a comparison with other Mediterranean regions. Journal of Natural History 2005, 39:47-70.
4. Bavel B.v., Näf C., Bergqvist P-A., Broman D., Lundgren K., Papakosta O., Rolff C., Strandberg B., Zebühr Y., Zook D., Rappe C. Levels of PCBs in the aquatic environment of the Gulf of Bothnia: benthic species and sediments. Marine Pollution Bulletin 1995, 32:210-218.
5. Blanar C.A., Munkittrick K.R., Houlahan J. Pollution and parasitism in aquatic animals: a meta- analysis of effect size. Aquatic Toxicology 2009, 93:1828.
6. Bocio A., Domingo J.L., Falcó G., Llobet J.M. Concentrations of PCDD/PCDFs and PCBs in fish and seafood from the Catalan (Spain) market: estimated human intake. Environment International 2007, 33:170175.
7. Broeg K., Zander S., Diamant A., Körting W., Krüner G., Paperna I., Westernhagen H.v. The use of fish metabolic, pathological and parasitological indices in pollution monitoring, I. North Sea. Helgoland Marine Research 1999, 53:171194.
8. Bush A.O., Lafferty K.D., Lotz J.M., Shostak A.W. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 1997, 83:575583.
9. Carreras-Aubets M., Repullés-Albelda A., Kostadinova A., Carrassón M. A new cryptic species of Aponurus Looss, 1907 (Digenea: Lecithasteridae) from Mediterranean goatfish (Teleostei: Mullidae). Systematic Parasitology 2011, 79:145179.
10. Castells P., Parera J., Santos J.F., Galceran M.T. Occurrence of polychlorinated naphthalenes, polychlorinated biphenyls and short-chain chlorinated paraffins in marine sediments from Barcelona (Spain). Chemosphere 2008, 70:15521562.
11. Chu F.-L.E., Soudant P., Hale R.C. Relationship between PCB accumulation and reproductive output in conditioned oysters Crassostrea virginica fed a contaminated algal diet. Aquatic Toxicology 2003, 65:293-307.
12. Della Torre C., Corsi I., Nardi F., Perra G., Tomasino M.P., Focardi S. Transcriptional and post-transcriptional response of drug-metabolizing enzymes to PAHs contamination in red mullet (Mullus barbatus, Linnaeus, 1758): a field study. Marine Environmental. Research 2010, 70:95101.
13. FAO/UNEP, 1993. Report of the FAO/UNEP/IAEA. Training workshop on the design of monitoring programmes and management of data concerning chemical contaminants in marine organisms, Athens, Greece, 22-26, pp. 247.
14. FAO/UNEP, 1997. Report of the meeting of experts to review the MEDPOL biomonitoring programme. Athens, Greece, Document UNEP-(OCA)/MED WG. 132/7. UNEP, Athens.
15. Froese, R., Pauly, D. (Eds.), 2012. FishBase. Available at: (last accessed on March 2012). http://www.fishbase.org.
16. Guerao G., Hernández E., Urzúa á. Early zoeal development of the shrimp Hippolyte leptocerus (Decapoda, Caridea, Hippolytidae). Zootaxa 2011, 2988:53-65.
17. Halcrow W., Mackay O.W., Bogan J. PCB levels in Clyde marine sediments and fauna. Marine Pollution Bulletin 1974, 5:134136.
18. Insausti D., Carrassón M., Maynou F., Cartes J.E., Solé M. Biliary fluorescent aromatic compounds (FACs) measured by fixed wavelength fluorescence (FF) in several marine fish species from the NW Mediterranean. Marine Pollution Bulletin 2009, 58:16351642.
19. Jousson O., Bartoli P. The life cycle of Opecoeloides columbellae (Pagenstecher, 1863) n. comb, (Digenea, Opecoelidae): evidence from molecules and morphology. International Journal for Parasitology 2000, 30:747-760.
20. Jousson O., Bartoli P., Pawlowski J. Molecular identification of developmental stages in Opecoelidae (Digenea). International Journal for Parasitology 1999, 29:1853-1858.
21. Khan R.A. Length-mass relationship, histopathology, and parasitism in winter flounder (Pleuronectes americanus) living near a PCB-contaminated naval facility in Newfoundland. Canadian Journal of Zoology 1999, 77:381388.
22. Khan R.A. Health of flatfish from localities in Placenta Bay, Newfoundland, contaminated with peroleum and PCBs. Archives of Environmental Contamination and Toxicology 2003, 44:485-492.
23. Knickmeyer R., Steinhart H. Cyclic organochlorines in the whelks Buccinum undatum and Neptunea antiqua from the North sea and the Irish sea. Marine Pollution Bulletin 1989, 20:433-437.
24. Lafferty K.D. Environmental parasitology: what can parasites tell us about human impacts on the environment?. Parasitology Today 1997, 13:251255.
25. Lafferty K.D., Holt R.D. How should environmental stress affect the population dynamics of disease?. Ecology Letters 2003, 6:654-664.
26. Le Pommelet E., Bartoli P., Silan P. Biodiversité des digènes et autres helminthes intestinaux des Rougets: synthèse pour Mullus surmuletus (Linné 1758) et M. barbatus (L. 1758) dans le bassin méditerranén. Annales des Sciences Naturelles-Zoologie et Biologia Animale 1997, 18:117-133.
27. Machias A., Labropoulou M. Intra-specific variation in resource use by Red mullet, Mullus barbatus. Estuarine Coastal ans Shelf Science 2002, 55:565578.
28. MacKenzie K. Parasites as pollution indicators in marine ecosystems: a proposed early warning system. Marine Pollution Bulletin 1999, 38:955-959.
29. MacKenzie K., Williams H.H., McVicar A.H., Siddal R. Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Advances in Parasitology 1995, 35:85-144.
30. Marcogliese D.J. Parasites of the superorganism: are they indicators of ecosystem health?. International Journal for Parasitology 2005, 35:705-716.
31. Martín-Sánchez J., Díaz M., Artacho M.E., Valero A. Molecular arguments for considering Hysterothylacium fabri (Nematoda: Anisakidae) a complex of sibling species. Parasitology Research 2003, 89:214-220.
32. Moles A., Wade T.L. Parasitism and phagocytic function among sand lance Ammodytes hexapterus Pallas exposed to crude oil-laden sediments. Bulletin of Environmental Contamination and Toxicolgy 2001, 66:528-535.
33. Morley N.J., Irwin S.W.B., Lewis J.W. Pollution toxicity to the transmission of larval digeneans through their molluscan hosts. Parasitology 2003, 126:S5-S26.
34. Morley N.J., Lewis J.W., Hoole D. Pollutant-induced effects on immunological and physiological interactions in aquatic host-trematode systems: implications for parasite transmission. Journal of Helminthology 2006, 80:137-149.
35. Morrisey D.J., Turner S.J., Mills G.N., Williamson R.B., Wise B.E. Factors affecting the distribution of benthic macrofauna in estuaries contaminated by urban runoff. Marine Environmental Research 2003, 55:113-136.
36. Nikolaeva V.M., Naidenova N. Nematodes of pelagic and bathypelagic fishes in the seas of the Mediterranean basin. Trudy Sevastopol'skoi Biologicheskoi Stantzii 1964, 17:125-158. (In Russian).
37. Peakall, D.B., Thompson, H., Baatrup, E., 2002. Relationship between behaviour and the biochemical/physiological biomarkers of exposure to environmental pollutants, In: Dell'Omo, G. (Ed.), Behavioural ecotoxicology. John Wiley & Sons Ltd, Chichester, UK.
38. Pérez-del Olmo A., Raga J.A., Kostadinova A., Fernández M. Parasite communities in Boops boops (L.) (Sparidae) after the Prestige oil-spill: detectable alterations. Marine Pollution Bulletin 2007, 54:266-276.
39. Pérez-del-Olmo A., Montero F.E., Raga J.A., Fernández M., Kostadinova A. Follow-up trends of parasite community alteration in a marine fish after the Prestige oil-spill: shifting baselines?. Environmental Pollution 2009, 157:221-228.
40. Petter, A.-J., Maillard, C. 1988. Larves d'ascarides parasites de poissons en Méditerranée occidentale. Bulletin du Museum National d'Histoire Naturelle, 4e série, section A 10, 347-369.
41. Petter, A.-J., Radujković, B.M., 1986. Nématodes parasites de poissons de la mer Adriatique. Bulletin du Museum National d'Histoire Naturelle, 4e série, Section A 8, pp. 487-499.
42. Petter, A.-J., Lébre, C., Radujković, B.M., 1984. Nématodes parasites de poissons de la mer Adriatique. Bulletin du Museum National d'Histoire Naturelle, 4e série, Section A 8, pp. 487-499.
43. Pietrock M., Marcogliese D.J. Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 2003, 19:293-299.
44. Porte C., Albaigés J. Bioaccumulation patterns of hydrocarbons and polychlorinated biphenyls in bivalves, crustaceans, and fishes. Archives of Environmental Contamination and Toxicology 1993, 26:273-281.
45. Poulin R. Toxic pollution and parasitism in freshwater fish. Parasitology Today 1992, 8:58-61.
46. Radujković B.M., Raibaut A. Parasites des poissons marins du Montenegro: liste des espèces de poissons avec leurs parasites. Acta Adriatica 1989, 30:307-320.
47. Rinderhagen, M., Ritterhoff, J., Zauke, G.-P., 2000. Crustaceans as bioindicators. In: Gerhardt, A. (Ed.), Biomonitoring of Polluted Water. Reviews on Actual Topics. Trans Tech Publications - Scitech Publications, Environmental Research Forum, vol. 9, pp. 161-194.
48. Roach A.C., Jones A.R., Murray A. Using benthic recruitment to assess the significance of contaminated sediments: the influence of taxonomic resolution. Environmental Pollution 2001, 112:131-143.
49. Roberts D.A., Johnston E.L., Poore A.G.B. Contamination of marine benthic habitats and effects upon associated epifauna. Marine Pollution Bulletin 2008, 56:1057-1065.
50. Sanchez-Hernandez J.C. Wildlife exposure to organophosphorus insecticides. Reviews of environmental contamination and toxicology 2001, vol. 172:21-64. Springer-Verlag, NY, USA.
51. Siddall R., Pike A.W., McVicar A.H. Parasites of Buccinum undatum (Mollusca: Prosobranchia) as biological indicators of sewage-sludge dispersal. Journal of the Marine Biological Association of the United Kingdom 1993, 73:931-948.
52. Smit N.J., Basson L., Van As J.G. Life cycle of the temporary fish parasite, Gnathia africana (Crustacea: Isopoda: Gnathiidae). Folia Parasitologica 2003, 50:135-142.
53. Solé M., Rodrígues S., Papiol V., Maynou F., Cartes J.E. Xenobiotic metabolism markers in marine fish with different trophic strategies and their relationship to ecological variables. Comparative Biochemistry and Physiology C 2009, 149:83-89.
54. Solé M., Antó M., Baena M., Carrassón M., Cartes J.E., Maynou F. Hepatic biomarkers of xenobiotic metabolism in eighteen marine fish from NW Mediterranean shelf and slope waters in relation to some of their biological and ecological variables. Marine Environmental Research 2010, 70:181-188.
55. Solé M., Baena M., Arnau S., Carrasson M., Maynou F., Cartes J.E. Muscular cholinesterase activities and lipid peroxidation levels as biomarkers in several Mediterranean marine fish species and their relationship with ecological variables. Environment International 2010, 36:202-211.
56. Sures B. Accumulation of heavy metals by intestinal helminths in fish: an overview and perspective. Parasitology 2003, 126:S53-S60.
57. Sures B. Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends in Parasitology 2004, 20:170-177.
58. Sures B. Host-parasite interactions in polluted environments. Journal of Fish Biology 2008, 73:2133-2142.
59. Manual on the biomarkers recommended for the MED POL biomonitoring programme 1999, UNEP/RAMOGE, UNEP, Athens, Greece, pp. 39.
60. Valero A., Paniagua M.I., Hierro I., Díaz V., Valderrama M.J., Benítez R., Adroher F.J. Anisakid parasites of two forkbeards (Phycis blennoides and Phycis phycis) from the Mediterranean coasts of Andalucía (Southern Spain). Parasitology International 2006, 56:1-5.
61. van der Oost R., Beyer J., Vermeulen N.P.E. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environmental Toxicology and Pharmacology 2003, 13:57-149.
62. Vidal-Martínez V.M., Pech D., Sures B., Purucker S.T., Poulin R. Can parasites really reveal environmental impact?. Trends in Parasitology 2009, 26:44-51.
63. Williams C. Combating marine pollution from land-based activities: Australian initiatives. Ocean & Coastal Management 1996, 33:87-112.
64. Williams H.H., MacKenzie K. Marine parasites as pollution indicators: an update. Parasitology 2003, 126:S27-S41.
65. Zorita I., Apraiz I., Ortiz-Zarragoitia M., Orbea A., Cancio I., Soto M., Marigómez I., Cajaraville M.P. Assessment of biological effects of environmental pollution along the NW Mediterranean Sea using mussels as sentinel organisms. Environmental pollution 2007, 148:236-250.
66. Zorita I., Ortiz-Zarragoitia M., Apraiz I., Cancio I., Orbea A., Soto M., Marigómez I., Cajaraville M.P. Assessment of biological effects of environmental pollution along the NW Mediterranean Sea using red mullets as sentinel organisms. Environmental pollution 2008, 153:157-168.