The use of protozoa in ecotoxicology: Application of multiple endpoint tests of the ciliate E. crassus for the evaluation of sediment quality in coastal marine ecosystems

Science of the Total Environment

Volumn 442, Issue , 2013, Pages 534-544

  Gomiero, A ^a,b   Dagnino, A ^b   Nasci, C ^c   Viarengo, A ^b  

^a CNR   (Italy)

^b UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^c THETIS S P A   (Italy)

Author keywords

Biomarkers; Endocytosis rate; Protozoa; Sediment risk assessment; Toxic pressure index; Trace elements

Indexed keywords

ADDITIVE EFFECTS; ADVERSE EFFECT; BIOLOGICAL RESPONSE; COASTAL MARINE ECOSYSTEMS; COASTAL MARINE SYSTEMS; CONTAMINATED SEDIMENT; CONTAMINATION LEVELS; ECO-TOXICOLOGY; ENDOCYTOSIS RATE; ENVIRONMENTAL RISKS; HIGH POTENTIAL; LYSOSOMAL MEMBRANES; MARINE CILIATES; MARINE ORGANISMS; PRESSURE COEFFICIENTS; PRESSURE INDEX; SEDIMENT QUALITY; SEDIMENT TOXICITY; TEST ORGANISMS; VENICE LAGOON;

BIOCHEMISTRY; BIOMARKERS; ECOLOGY; MARINE BIOLOGY; MARINE POLLUTION; MOLECULAR BIOLOGY; POLLUTION DETECTION; PROTOZOA; SEDIMENTS; TRACE ELEMENTS;

SEDIMENTOLOGY;

METAL;

BIOMARKER; COASTAL SEDIMENT; ECOTOXICOLOGY; MARINE ECOSYSTEM; MORTALITY; PROTOZOAN; SEDIMENT ANALYSIS; SEDIMENT POLLUTION; SUBLETHAL EFFECT; BIOASSAY; BIOAVAILABILITY; CHEMICAL ANALYSIS; ENVIRONMENTAL RISK; RISK ASSESSMENT; TOXICITY; TRACE ELEMENT;

ARTICLE; BIOAVAILABILITY; COASTAL WATERS; CONTROLLED STUDY; ECOTOXICOLOGY; ENDOCYTOSIS; ESTUARY; EUPLOTES; EUPLOTES CRASSUS; ITALY; LYSOSOME MEMBRANE; MORTALITY; NONHUMAN; POLLUTANT; PRIORITY JOURNAL; REPRODUCTION; RISK ASSESSMENT; SEDIMENT; TOXICITY TESTING; ECOTOXICITY; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL STRESS; PROTOZOON; STRESS; BIOASSAY; CHEMISTRY; DRUG EFFECT; ECOSYSTEM; ENVIRONMENTAL MONITORING; GROWTH, DEVELOPMENT AND AGING; METHODOLOGY; SEA; STATISTICAL ANALYSIS; WATER POLLUTANT;

ITALY; VENETO; VENEZIA [VENETO]; VENICE LAGOON; LIDO; MURANO;

CILIOPHORA; MONEUPLOTES CRASSUS; PROTISTA; PROTOZOA;

BIOLOGICAL ASSAY; DATA INTERPRETATION, STATISTICAL; ECOSYSTEM; ECOTOXICOLOGY; ENDPOINT DETERMINATION; ENVIRONMENTAL MONITORING; EUPLOTES; GEOLOGIC SEDIMENTS; ITALY; OCEANS AND SEAS; WATER POLLUTANTS, CHEMICAL;

EID: 84870168702     PISSN: 00489697     EISSN: 18791026     Source Type: Journal    
DOI: 10.1016/j.scitotenv.2012.10.023     Document Type: Article

References (85)

1. Allen H.E., Fu G., Deng B. Analysis of acid-volatile sulfide (AVS) and simultaneously extracted metals (SEM) for the estimation of potential toxicity in aquatic sediments. Environ Toxicol Chem 1993, 12:1441-1453.
2. Al-Rasheid K.A.S., Sleigh M.A. The effects of heavy metals on the feeding rate of Euplotes mutabilis (Tuffrau, 1960). Eur J Protistol 1994, 30:270-279.
3. Argese E., Bettiol C., Rigo C., Bertini S., Colomban S., Ghetti P.F. Distribution of arsenic compounds in Mytilus galloprovincialis of the Venice lagoon (Italy). Sci Total Environ 2005, 348(1-3):267-277.
4. Attig H., Dagnino A., Negri A., Jebali J., Boussetta H., Viarengo A., et al. Uptake and biochemical responses of mussels Mytilus galloprovincialis exposed to sublethal nickel concentrations. Ecotoxicol Environ Saf 2010, 73(7):1712-1719.
5. Baumard P., Budzinski H., Garrigues P., Dizer H., Hansen P.D. Polycyclic aromatic hydrocarbons in recent sediments and mussels (Mytilus edulis) from the Western Baltic Sea: occurrence, bioavailability and seasonal variations. Mar Env Res 1999, 47(1):17-47.
6. Baumard P., Budzinski H., Garrigues P., Narbonne J.F., Burgeot T., Michel X., Bellocq J. Polycyclic aromatic hydrocarbon (PAH) burden of mussels (Mytilus sp.) in different marine environments in relation with sediment PAH contamination, and bioavailability. Mar Env Res 1999, 47(5):415-439.
7. Belkin S. Microbial whole-cell sensing systems of environmental pollutants. Curr Opin Microbiol 2003, 6:206-212.
8. Bellucci L.G., Frignani M., Paolucci D., Ravanelli M. Distribution of heavy metals in sediments of the Venice Lagoon: the role of the industrial area. Sci Total Environ 2002, 295(1-3):35-49.
9. Belzunce M.J., Solaun O., González Oreja J.A., Millán E., Pérez V. In oceanography and marine environment of the basque country. Chapter 12 contaminants in sediments. Elsevier Oceanogr Ser 2004, 70:283-315.
10. Benedetti M., Ciaprini F., Piva F., Onorati F., Fattorini D., Notti A., et al. A multidisciplinary weight of evidence approach for classifying polluted sediments: integrating sediment chemistry, bioavailability, biomarkers responses and bioassays. Environ Int 2011, 38(1):17-28.
11. Bernardello M., Secco T., Pellizzato F., Chinellato M., Sfriso A., Pavoni B. The changing state of contamination in the Lagoon of Venice. Part 2: heavy metals. Chemosphere 2006, 64(8):1334-1345.
12. Cajaraville M.P., Bebianno M.J., Blasco J., Porte C., Sarasquete C., Viarengo A. The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian peninsula: a practical approach. Sci Total Environ 2000, 247:295-311.
13. Camus L., Pampanin D.M., Volpato E., Delaney E., Sanni S., Nasci C. Total oxyradical scavenging capacity responses in Mytilus galloprovincialis transplanted into the Venice lagoon (Italy) to measure the biological impact of anthropogenic activities. Mar Pollut Bull 2004, 49(9-10):801-808.
14. Canesi L., Ciacci C., Lorusso L.C., Betti M., Gallo G., Pojana G., et al. Effects of Triclosan on Mytilus galloprovincialis hemocyte function and digestive gland enzyme activities: possible modes of action on non target organisms. Comp Biochem Physiol C 2007, 145:464-472.
15. Christiansen C., Edelvang K., Emeis K., Graf G., Jähmlich S., Kozuch J., et al. Material transport from the nearshore to the basinal environment in the southern Baltic Sea: I. Processes and mass estimates. J Mar Syst 2002, 35(3-4):133-150.
16. Clarke K.R., Ainsworth M. A method of linking multivariate community structure to environmental variables. Mar Ecol Prog Ser 1993, 92:205-219.
17. Clarke K.R., Gorley R.N. Primer v6: user manual/tutorial, Primer E: Plymouth 2006, Plymouth Marine Laboratory, Plymouth, UK.
18. Coccioni R., Frontalini F., Marsili A., Mana D. Benthic foraminifera and trace element distribution: a case-study from the heavily polluted lagoon of Venice (Italy). Mar Pollut Bull 2009, 59(8-12):257-267.
19. Coppellotti O. Sensitivity to copper in a ciliate as possible component of biological monitoring in the lagoon of Venice. Arch Environ Contam Toxicol 1998, 35:417-425.
20. Da Ros L., Moschino V., Guerzoni S., Halldorsson H.P. Lysosomal responses and metallothionein induction in the blue mussel Mytilus edulis from the south-west coast of Iceland. Environ Int 2007, 33:362-369.
21. Dagnino A., Sforzini S., Dondero F., Fenoglio S., Bona E., Jensen J., et al. A "Weight-of-Evidence" approach for the integration of environmental "Triad" data to assess ecological risk and biological vulnerability. Integrated Environ Assess Man 2008, 4(3):314-326.
22. Delmonte Corrado M.U., Trielli F., Amaroli A., Ognibene M., Falugi C. Protists as tools for environmental biomonitoring: importance of cholinesterase enzyme activities. Water Pollution: New Research 2005, 181-200. Nova Science Publishers, Hauppauge, NY. A.R. Burk (Ed.).
23. Depledge M.H., Aagaard A., Gyorkos P. Assessment of trace metal toxicity using molecular, physiological and behavioural biomarkers. Mar Biol Bull 1995, 31:19-27.
24. Díaz S., Martín-González A., Gutiérrez J.C. Evaluation of heavy metal acute toxicity and bioaccumulation in soil ciliated protozoa. Environ Int 2006, 32:711-717.
25. Dini F. Relationship between breeding systems and resistance to mercury in Euplotes crassus (Ciliophora, Hypotrichida). Mar Ecol Prog Ser 1981, 4:195-202.
26. Dondero F., Cavaletto M., Ghezzi A.R., La Terza A., Banni M., Viarengo A. Biochemical characterization and quantitative gene expression analysis of the multi-stress inducible metallothionein of Tetrahymena thermophila. Protist 2004, 155:157-168.
27. Donnini F., Dinelli E., Sangiorgi F., Fabbri E. A biological and geochemical integrated approach to assess the environmental quality of a coastal lagoon (Ravenna, Italy). Environ Int 2007, 33:919-928.
28. U.S.EPA Procedures for the derivation of equilibrium partitioning sediment benchmarks (ESBs) for the protection of benthic organisms: metal mixtures (cadmium, copper, lead, nickel, silver and zinc) 2005, Office of Research and Development, Washington, DC, EPA-600-R-02-011.
29. Evans S.M., Samosir A.M. Behavioural bioassay using the marine ciliate Euplotes vannus (Müller) 1990. Mar Freshw Behav Physiol 1990, 17(4):247-254.
30. Fleury A., Fryd-Versavel G. Donne'es nouvelles sur quelques processus morphogénétiques chez les Hypotriches, notamment dans le genera Euplotes: leur contribution a' l'approche evolutionniste du probleme de la regulation de l'activite' morphogenetique chez les Cilies. J Protozool 1981, 28:283-291.
31. Frignani M., Bellucci L.G., Carraro C., Favotto M. Accumulation of polychlorinated dibenzo-p-dioxins and dibenzofurans in sediments of the Venice Lagoon and the industrial area of Porto Marghera. Mar Pollut Bull 2001, 42(7):544-553.
32. Frignani M., Bellucci L.G., Carraro C., Favotto M. Accumulation of polychlorinated biphenyls in sediments of the Venice Lagoon and the industrial area of Porto Marghera. Chemosphere 2004, 54(10):1563-1572.
33. Galloway T.S., Brown R.J., Browne M.A., Dissanayake A., Lowe D., Jones M.B., et al. A multibiomarker approach to environmental assessment. Environ Sci Technol 2004, 38(6):1723-1731.
34. Gilron D.L., Lynn D.H. Ciliated protozoa as test organism in toxicity assessment. Microscale Testing in Aquatic Toxicology 1998, 323-336. CRC Press, Boca Raton. P.G. Wells, K. Lee, C. Blaise (Eds.).
35. Giusti L., Zhang H. Heavy metals and arsenic in sediments, mussels and marine water from Murano (Venice, Italy). Environ Geochem Health 2002, 24(1):47-65.
36. Gomiero A., Sforzini S., Dagnino A., Nasci C., Viarengo A. The use of multiple endpoints to assess cellular responses to environmental contaminants in the interstitial marine ciliate Euplotes crassus. Aquat Toxicol 2012, 114-115:206-216.
37. Gutierrez J.C., Martin-Gonzalez A., Diaz S., Ortega R. Ciliates as potential source of cellular and molecular biomarkers/biosensors for heavy metal pollution. Eur J Protistol 2003, 39:461-467.
38. Hausmann K., Hulsmann N., Radek R. Protistology 2003, Springer-Verlag, Berlin.
39. ISO 10253-2006. Water quality - Marine algal growth inhibition test with Skeletonema costatum and Phaeodactylum tricornutum. International Organization of Standardization eds.
40. Italian Government Ministero dell'ambiente e della tutela del territorio e del mare, Decreto 14 aprile 2009, no. 56. Regolamento recante i criteri tecnici per il monitoraggio dei corpi idrici e l'identificazione delle condizioni di riferimento per la modifica delle norme tecniche del decreto legislativo 3 aprile 2006, no. 152, recante norme in materia ambientale, predisposto ai sensi dell'articolo 75, comma 3, del decreto legislativo medesimo 2009.
41. Jiménez-Tenorio N., Morales-Caselles C., Kalman J., Salamanca M.J., de Canales ML González, Sarasquete C., et al. Determining sediment quality for regulatory proposes using fish chronic bioassays. Environ Int 2007, 33:474-480.
42. Losso C., Volpi Ghirardini A. Overview of ecotoxicological studies performed in the Venice Lagoon (Italy). Environ Int 2010, 36:92-121.
43. MacDonald D.D., Carr R.S., Calder F.D., Long E.R., Ingersoll C.G. Development and evaluation of sediment quality guidelines for Florida coastal waters. Ecotoxicology 1996, 5(4):253-278.
44. Madoni P. Benthic ciliates in Adriatic Sea lagoons. Eur J Protistol 2006, 42:165-173.
45. Madoni P., Esteban G., Gorbi G. Acute toxicity of cadmium, copper, mercury, and zinc to ciliates from activated sludge plants. Bull Environ Contam Toxicol 1992, 49:900-905.
46. Marigómez I., Baybay-Villacorta L. Pollutant-specific and general lysosomal responses in digestive cells of mussels exposed to model organic chemicals. Aquat Toxicol 2003, 64(3):235-257.
47. Moore M.N. Biocomplexity: the post-genome challenge in ecotoxicology. Aquat Toxicol 2002, 59(1-2):1-15.
48. Moore M.N., Mayernik J.A., Giam C.S. Lysosomal responses to a polynuclear aromatic hydrocarbon in a marine snail: effects of exposure to phenanthrene and recovery. Mar Environ Res 1985, 17(2-4):230-233.
49. Moore M.N., Depledge M.H., Readman J.W., Leonard P. An integrated biomarker-based strategy for ecotoxicological evaluation of risk in environmental management. Mutat Res 2004, 552:247-268.
50. Moore M.N., Allen J.I., McVeigh A. Environmental prognostics: an integrated model supporting lysosomal stress responses as predictive biomarkers of animal health status. Mar Environ Res 2006, 61:278-304.
51. Mori G., Erra F., Cionini K., Banchetti R. Sublethal doses of heavy metals and slow-down pattern of Euplotes crassus (Ciliophora, Hypotrichia): a behavioural bioassay. Ital J Zool 2003, 70:23-30.
52. Nasci C., Nesto N., Monteduro R.A., Da Ros L. Field application of biochemical markers and a physiological index in the mussel, Mytilus galloprovincialis: transplantation and biomonitoring studies in the lagoon of Venice (NE Italy). Mar Environ Res 2002, 54(3-5):811-816.
53. Nendza M. Inventory of marine biotest methods for the evaluation of dredged material and sediments. Chemosphere 2002, 48(8):865-883.
54. Nesto N., Bertoldo M., Nasci C., Da Ros L. Utilizzo del trapianto di Tapes philippinarum (Adams & Reeve, 1850) come strumento di valutazione della qualità ambientale in laguna di Venezia: problemi e prospettive. Biol Mar Med 2004, 11(2):517-520.
55. Nesto N., Romano S., Moschino V., Mauri M., Da Ros L. Bioaccumulation and biomarker responses of trace metals and micro-organic pollutants in mussels and fish from the Lagoon of Venice, Italy. Mar Pollut Bull 2007, 55(10-12):469-484.
56. Nilsson J.R. Phagotrophy in Tetrahymena. Biochemistry and Physiology of Protozoa 1979, vol. 2:339-379. Academic Press, New York. 2nd edition. M. Levandowsky, S.H. Hutner (Eds.).
57. Nilsson J.R. Effect of copper on phagocytosis in Tetrahymena. Protoplasma 1981, 109:359-370.
58. Nilsson J.R. Tetrahymena in cytotoxicology: with special reference to effects of heavy metals and selected drugs. Eur J Protistol 1989, 25:2-25.
59. Otte J.C., Andersson C., Abrahamson A., Olsman H., Keiter S., Engwall M., et al. A bioassay approach to determine the dioxin-like activity in sediment extracts from the Danube River: Ethoxyresorufin-O-deethylase induction in gill filaments and liver of three-spined sticklebacks (Gasterosteus aculeatus L.). Environ Int 2008, 34:1176-1184.
60. Pampanin D.M., Camus L., Gomiero A., Marangon I., Volpato E., Nasci C. Susceptibility to oxidative stress of mussels (Mytilus galloprovincialis) in the Venice Lagoon (Italy). Mar Pollut Bull 2005, 50(12):1548-1557.
61. Pereira C.D.S., Martin-Díaz M.L., Zanette J., Cesar A., Brasil Choueri R., de Souza Abessa D.M., et al. Integrated biomarker responses as environmental status descriptors of a coastal zone (São Paulo, Brazil). Ecotoxicol Environ Saf 2011, 74(5):1257-1264.
62. Piccinni E. Response to heavy metals of uni- and multicellular organisms: homologies and analogies. Boll Zool 1989, 56:265-271.
63. Picone M., Bergamin M., Arizzi Novelli A., Noventa S., Delaney E., Barbanti A., et al. Evaluation of Corophium orientale as bioindicator for Venice Lagoon: sensitivity assessment and toxicity-score proposal. Ecotoxicol Environ Saf 2008, 70(1):174-184.
64. Rehman A., Shakoori F.R., Shakoori A.R. Heavy metal resistant freshwater ciliate, Euplotes mutabilis, isolated from industrial effluents has potential to decontaminate wastewater of toxic metals. Bioresour Technol 2008, 99(9):3890-3895.
65. ++ on the ethogram of Euplotes vannus (Ciliata, Hypotrichida). Eur J Protistol 1997, 33:63-71.
66. Rice J. Environmental health indicators. Ocean Coast Manag 2003, 46:235-259.
67. Rico D., Martín-González A., Díaz S., de Lucas P., Gutiérrez J.C. Heavy metals generate reactive oxygen species in terrestrial and aquatic ciliated protozoa. Comp Biochem Physiol C 2009, 149:90-96.
68. Roberts R.O., Berk S.G. Development of a protozoan chemoattraction bioassay for evaluating toxicity of aquatic pollutants. Toxicity Assess 2006, 5(3):279-292.
69. Rogerson A., Ying Shiu W., Lan Huang G., Mackay D., Berger J. Determination and interpretation of hydrocarbon toxicity to ciliate protozoa. Aquat Toxicol 1983, 3:215-228.
70. Romeo M., Frasila C., Gnassia-Barelli M., Damiens G., Micu D., Mustata G. Biomonitoring of trace metals in the Black Sea (Romania) using mussels Mytilus galloprovincialis. Water Res 2005, 39:596-604.
71. Ruus A., Schaanning M., Øxnevad S., Hylland K. Experimental results on bioaccumulation of metals and organic contaminants from marinesediments. Aquat Toxicol 2005, 72(3):273-292.
72. Seaman J.C., Bertsch A.J.S., Paul M. Immobilization of nickel and other metals in contaminated sediments by hydroxyapatite. J Environ Qual 2000, 30(2):460-469.
73. Secco T., Pellizzato F., Sfriso A., Pavoni B. The changing state of contamination in the Lagoon of Venice. Part 1: organic pollutants. Chemosphere 2005, 58(3):279-290.
74. Sfriso A., Marcomini A., Zanette M. Heavy metals in sediments, SPM and phytozoobenthos of the lagoon of Venice. Mar Pollut Bull 1995, 30(2):116-124.
75. Shaw J.P., Dondero F., Moore M.N., Negri A., Dagnino A., Readman J.W., et al. Integration of biochemical, histochemical and toxicogenomic indices for the assessment of health status of mussels from the Tamar Estuary, U.K. Mar Environ Res 2011, 72(1-2):13-24.
76. Sherr B.F., Sherr E.B., Hopkinson C.S. Trophic interactions within pelagic microbial communities: interactions of feedback regulation of carbon flow. Hydrobiologia 1988, 159:19-26.
77. Sibley P.K., Legler J., Dixon D.G., Burton D.R. Environmental health assessment of benthic habitat adjacent to a pulp mill discharge. Acute and chronic toxicity of sediments to benthic macroinvertebrates. Arch Environ Contam Toxicol 1997, 32(3):274-284.
78. Solé M., Kopecka-Pilarczyk J., Blasco J. Pollution biomarkers in two estuarine invertebrates, Nereis diversicolor and Scrobicularia plana, from a Marsh ecosystem in SW Spain. Environ Int 2009, 35:523-531.
79. Trielli F., Amaroli A., Sifredi F., Marchi B., Falugi C., Delmonte Corrado M.U. Effects of xenobiotic compounds on the cell activities of Euplotes crassus, a single cell eukaryotic test organism for the study of the pollution of marine sediments. Aquat Toxicol 2007, 83:272-283.
80. U.S.EPA Evaluation of dredged material proposed for ocean disposal testing manual 1991, EPA 503/8-91/001.
81. Viarengo A., Lowe D., Bolognesi C., Fabbri E., Koehler A. The use of biomarkers in biomonitoring: a 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Comp Biochem Physiol CToxicol Pharmacol 2007, 146(3):281-300.
82. Volpi Ghirardini A., Birkemeyer T., Arizzi Novelli A., Delaney E., Pavoni B., Ghetti P.F. An integrated approach to sediment quality assessment: the Venetian lagoon as a case study. Aquat Ecosyst Health Manage 1999, 2(4):435-447.
83. Walne P.R. Culture of bivalve molluscs, 50years experience at Conway 1974, 1-173. Fishing News (Books) Ltd.
84. Zhou L., Li J., Lin X., Khaled A., Al-Rasheid S. Use of RAPD to detect DNA damage induced by nitrofurazone in marine ciliate, Euplotes vannus (Protozoa, Ciliophora). Aquat Toxicol 2011, 103:225-232.
85. Zonta R., Botter M., Cassin D., Pini R., Scattolin M., Zaggia L. Sediment chemical contamination of a shallow water area close to the industrial zone of Porto Marghera (Venice Lagoon, Italy). Mar Pollut Bull 2007, 55(10-12):529-542.