Responses of biomarkers in wild freshwater mussels chronically exposed to complex contaminant mixtures

Ecotoxicology

Volumn 23, Issue 7, 2014, Pages 1345-1358

  Machado, Anderson Abel De S ^a,b,c,d,e   Wood, Chris M ^b   Bianchini, Adalto ^c   Gillis, Patricia L ^a  

^a ENVIRONMENT CANADA   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

^c FEDERAL UNIVERSITY OF RIO GRANDE   (Brazil)

^d UNIVERSITY OF TRENTO   (Italy)

^e LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

Author keywords

Biomarkers; Environmental assessment; Freshwater mussel; Metal; Oxidative stress; Urban River

Indexed keywords

CADMIUM; CALCIUM; CATALASE; COPPER; GLUTATHIONE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; LEAD; MAGNESIUM; NICKEL; POTASSIUM; REACTIVE OXYGEN METABOLITE; SODIUM; SUPEROXIDE DISMUTASE; THIOL DERIVATIVE; ZINC; BIOLOGICAL MARKER; METAL; WATER POLLUTANT;

BIOACCUMULATION; BIOMARKER; BIVALVE; ENVIRONMENTAL ASSESSMENT; ENZYME ACTIVITY; METABOLISM; METAL; POLLUTION EFFECT; POLLUTION EXPOSURE;

ADULT; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CANADA; CHEMICAL COMPOSITION; CHRONIC TOXICITY; CONTROLLED STUDY; DETOXIFICATION; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL IMPACT ASSESSMENT; FRESHWATER SPECIES; GILL; LASMIGONA COSTATA; LIPID PEROXIDATION; LONG TERM EXPOSURE; MUSSEL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN METABOLISM; RIVER; TISSUE LEVEL; URBAN AREA; WATER CONTAMINATION; WATER POLLUTION INDICATOR; WILD ANIMAL; ANIMAL; BIVALVE; CHEMISTRY; DRUG EFFECTS; ENVIRONMENTAL MONITORING; METABOLISM; TOXICITY; WATER POLLUTANT;

CANADA; GRAND RIVER [ONTARIO]; ONTARIO [CANADA];

LASMIGONA COSTATA;

ANIMALS; BIOLOGICAL MARKERS; BIVALVIA; ENVIRONMENTAL MONITORING; GILLS; METALS; ONTARIO; OXIDATIVE STRESS; RIVERS; WATER POLLUTANTS;

EID: 84925230765     PISSN: 09639292     EISSN: 15733017     Source Type: Journal    
DOI: 10.1007/s10646-014-1277-8     Document Type: Article

References (51)

1. Alsop D, Wood CM (2011) Metal uptake and acute toxicity in zebrafish: common mechanisms across multiple metals. Aquat Toxicol 105:385-393
2. Amado LL, Garcia ML, Ramos PB, Freitas RF, Zafalon B, Ferreira JLR, Yunes JS, Monserrat JM (2009) A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: Application to evaluate microcystins toxicity. Sci Tot Environ 407:2115-2123
3. Beutler E (1975) Red cell metabolism: a manual of biochemical methods. Grune & Straton, New York
4. Box A, Sureda A, Galgani F, Pons A, Deudero S (2007) Assessment of environmental pollution at Balearic Islands applying oxidative stress biomarkers in the mussel Mytilus galloprovincialis. Comp Biochem Physiol C 146:531-539 (Pubitemid 47500151)
5. Carlberg I, Mannervik B (1975) Purification and characterization of the flavoenzyme glutathione reductase from rat liver. J Biol Chem 250:5475-5480
6. Cooke S (2006) Water quality in the Grand River: a summary of current conditions (2000-2004) and long term trends. Grand River Conservation Authority. http://www.grandriver.ca/water/2006-WaterQuality-complete.pdf Accessed Jan 2014
7. Depledge MH, Aagaard A, Györkös P (1995) Assessment of trace metal toxicity using molecular, physiological and behavioural biomarkers. Mar Poll Bull 31:9-27
8. Farcy E, Gagné F, Martel L, Fortier M, Trépanier S, Brousseau P, Fournier M (2011) Short-term physiological effects of a xenobiotic mixture on the freshwater mussel Elliptio complanata exposed to municipal effluents. Environ Res 111:1096-1106
9. Frank R, Logan L (1988) Pesticide and industrial chemical residues at the mouth of the Grand, Saugeen and Thames rivers, Ontario, Canada, 1981-85. Arch Environ Contam Toxicol 17:741-754
10. Gagné F, André C, Cejka P, Hausler R, Fournier M (2011) Evidence of neuroendocrine disruption in freshwater mussels exposed to municipal wastewaters. Sci Tot Environ 409:3711-3718
11. Giacomin M, Gillis PL, Bianchini A, Wood CM (2013) Interactive effects of copper and dissolved organic matter on sodium uptake, copper bioaccumulation, and oxidative stress in juvenile freshwater mussels (Lampsilis siliquoidea). Aquat Toxicol 144-145:105-115
12. Géret F, Jouan A, Turpin V, Bebianno MJ, Cosson RP (2002) Influence of metal exposure on metallothionein synthesis and lipid peroxidation in two bivalve mollusks: the oyster (Crassostreagigas) and the mussel (Mytilus edulis). Aquat Living Resour 15:61-66 (Pubitemid 34281268)
13. Géret F, Serafim A, Bebianno MJ (2003) Antioxidant enzyme activities, metallothioneins and lipid peroxidation as biomarkers in Ruditapes decussatus? Ecotoxicology 12:417-426 (Pubitemid 37378249)
14. Gillis PL (2011) Assessing the toxicity of sodium chloride to the glochidia of freshwater mussel: implications for salinization of surface waters. Environ Pollut 159:1702-1708
15. Gillis PL (2012) Cumulative impacts of urban runoff and municipal wastewater effluents on wild freshwater mussels (Lasmigona costata). Sci Total Environ 431:348-356
16. Gillis PL, Gagné F, McInnis R, Hooey TM, Choy ES, André C, Hoque ME, Metcalfe CD (2014a) The impact of municipal wastewater effluents on field-deployed freshwater mussels on the Grand River (ON). Environ Toxicol Chem 33:131-143
17. Gillis PL, Higgins SK, Jorge MB (2014b) Evidence of oxidative stress in wild freshwater mussels (Lasmigona costata) chronically exposed to urban-derived contaminants. Ecotoxicol Environ Safety 102:62-69
18. Gonzalez-Rey M, Bebianno MJ (2011) Non-steroidal anti-inflammatory drug (NSAID) ibuprofen distresses antioxidant defense system in mussel Mytilus galloprovincialis gills. Aquat Toxicol 105:264-269
19. Grand River Conservation Authority (2013) http://www.grandriver.ca/. Accessed 10 Sept 2013
20. Grosell M, Nielsen C, Bianchini A (2002) Sodium turnover rate determines sensitivity to acute copper and silver exposure in freshwater animals. Comp Biochem Physiol C 133:287-303 (Pubitemid 35287073)
21. Jorge MB, Loro VL, Bianchini A, Wood CM, Gillis PL (2013) Mortality, bioaccumulation and physiological responses in juvenile freshwater mussels (Lampsilis siliquoidea) chronically exposed to copper. Aquat Toxicol 123:137-147
22. Keen JH,Habig H, Jakoby WB(1976)Mechanismfor several activities of the glutathione-S-transferase. J Biol Chem 20:6183-6188
23. Loomer HA, Cooke SE (2011) Water quality in the Grand River watershed: current conditions and trends (2003-2008). Grand River Conservation Authority/ http://www.grandriver.ca/water/2011-WaterQualityReport.pdf. Accessed Dec 2013
24. Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13-30
25. Lydeard C, Cowie RH, Ponder WF, Bogan AE, Bouchet P, Clark SA, Cummings KW, Frest TJ, Gargominy O, Herbert DG, Hershler R, Perez KE, Roth B, Seddon M, Strong EE, Thompson FG (2004) The global decline of nonmarine mussels. BioScience 54:321-330
26. Machado AAS, Hoff MLM, Klein RD, Cardozo JG, Giacomin MM, Pinho GLL, Bianchini A (2013) Biomarkers of waterborne copper exposure in the guppy Poecilia vivipara acclimated to salt water. Aquat Toxicol 138-139:60-69
27. Mackie GL (1996) Diversity and status of Unionidae (Bivalvia) in the Grand River, a tributary of Lake Erie, and its drainage basin. Ontario Ministry of Natural Resources, Peterborough
28. Martín-Díaz ML, Gagné F, Blaise C (2009) The use of biochemical responses to assess ecotoxicological effects of pharmaceutical and personal care products (PPCPs) after injection in the mussel Elliptio complanata. Environ Toxicol Pharmacol 28:237-242
29. Mazon AF, Monteiro EAS, Pinheiro GHD, Fernandes MN (2002) Hematological and physiological changes induced by short-term exposure to copper in the freshwater fish Prochilodus scrofa. Braz J Biol 62:621-631
30. McCord JM, Fridovich I (1969) Superoxide dismutase an enzymatic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049-6065
31. Metcalfe CM, Miao XS, Koenig BG, Struger J (2003) Distribution of acidic and neutral drugs in surface waters near sewage treatment plants in the lower Great Lakes, Canada. Environ Toxicol Chem 22:2881-2889 (Pubitemid 37485217)
32. Metcalfe CD, Chu S, Judt C, Li H, Oakes KD, Servos MR, Andrews DM (2010) Antidepressants and their metabolites in municipal waste water, and downstream exposure in an urban watershed. Environ Toxicol Chem 29:79-89
33. Metcalfe-Smith JL, Staton SK, Mackie GL, Lang NM (1998) Changes in the biodiversity of freshwater mussels in the Canadian water of lower Great Lakes drainage basin over the past 140 years. J Great Lakes Res 24:845-858 (Pubitemid 29112026)
34. Metcalfe-Smith JL, Mackie GL, Maio JD, Staton SK (2000) Changes over time in the diversity and distribution of freshwater mussels (Unionidae) in the Grand River, southwestern Ontario. J Great Lakes Res 26:445-459 (Pubitemid 32108979)
35. Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170-3175
36. Monserrat JM, Martínez PB, Geracitano LA, Amado LL, Martins CMG, Pinho GLL, Chaves IS, Ferreira-Cravo M, Ventura-Lima J, Bianchini A (2007) Pollution biomarkers in estuarine animals: Critical review and new perspectives. Comp Biochem Physiol C 146:221-234 (Pubitemid 47059054)
37. Nemerow NL (1991) Stream, lake, estuary, and ocean pollution, 2nd edn. Van Nostrand Reinhold, New York
38. Nenadic O, Greenacre M (2007) Correspondence analysis in R, with two- and three-dimensional graphics: the ca package. J Stat Softw 20(3). http://www.jstatsoft.org/v20/i03/.Accessed 19 Dec 2013
39. Neves RJ, Bogan AE, Williams JD, Ahlstedt SA, Hartfield PW (1997) Status of aquatic mollusks in the southeastern United States: a downward spiral of diversity. In: Benz GW, Collins DE (eds) Aquatic fauna in peril: the southeastern perspective special publication 1, Southeast Aquatic Research Institute, Lenz Design and Communications, Decatur, GA, pp 43-85
40. Nogueira LS, Wood CM, Gillis PL, Bianchini A (2013) Isolation and fractionation of gill cells from freshwater (Lasmigona costata) and seawater (Mesodesma mactroides) bivalves for use in toxicological studies with copper. Cytotechnology 65:773-783
41. Oliveira LF, Souza MM (2007) Aquatic invertebrates under water-borne lead exposure: Ionic and osmotic balance. Comp Biochem Physiol A 148:S66-S79
42. Ontario Provincial Water Quality Monitoring Network (2012) Website. http://www.ene.gov.on.ca/environment/en/monitoring-and-reporting/ provincial-water-quality-monitoring-net work/. Accessed 13 Jan 2012
43. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project. org/. Accessed 9 Nov 2013
44. Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound and non-protein sulfhydryl groups in tissue with Ellman's reagent. Anal Biochem 25:192-205
45. Serafim A, Lopes B, Company R, Cravo A, Gomes T, Sousa V, Bebianno MJ (2011) A multi-biomarker approach in crosstransplanted mussels Mytilus galloprovincialis. Ecotoxicology 20:1959-1974
46. Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radical Biol Med 18:321-336
47. Strayer DL, Downing JA, Haag WR, King TL, Layzer JB, Newton TJ, Nichols SJ (2004) Changing perspectives on pearly mussels, North America's most imperiled animals. Bioscience 54:429-439 (Pubitemid 38641535)
48. Tetreault GR, Bennett CJ, Shires K, Knight B, Servos MR, McMaster ME (2011) Intersex and reproductive impairment of wild fish exposed to multiple municipal wastewater discharges. Aquat Toxicol 104:278-290
49. Viarengo A, Lowe D, Bolognesi C, Fabbri E, Koehler A (2007) The use of biomarkers in biomonitoring: a 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Comp Biochem Physiol C 146:281-300 (Pubitemid 47127013)
50. Viarengo A, Nott JA (1993) Mechanisms of heavy metal cation homeostasis in marine invertebrates. Comp Physiol Chem C 104:355-372 (Pubitemid 23167306)
51. Wang S, Oakes KD, Bragg LM, Pawliszyn J, Dixon G, Servos MR (2011) Validation and use of in vivo solid phase microextraction (SPME) for the detection of emerging contaminants in fish. Chemosphere 85:1472-1480