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Environmental problems - Chemical approaches
RESEARCH ARTICLE

Developing a sentinel mollusc species for toxicity assessment: metal exposure, dose and response – laboratory v. field exposures and resident organisms

Anne Taylor A B and William Maher A
+ Author Affiliations
- Author Affiliations

A Ecochemistry Laboratory, Institute for Applied Ecology, University of Canberra, Canberra, ACT 2601, Australia.

B Corresponding author: anne.taylor@canberra.edu.au

Environmental Chemistry 13(3) 434-446 https://doi.org/10.1071/EN15104
Submitted: 21 May 2015  Accepted: 31 July 2015   Published: 6 October 2015

Environmental context. Metal contamination in estuarine sediments can affect ecosystem health. Molluscs are commonly used as environmental indicators because they accumulate contaminants that cause adverse health effects. We investigated metal uptake and effects in the Sydney cockle, comparing exposure to contaminated lake sediments in situ and in laboratory aquariums. Although differences were observed between the different exposure types, all approaches were found to be valid for investigating metal health effects in this organism.

Abstract. Relationships between exposure, tissue dose and biological responses of the benthic marine bivalve Anadara trapezia to an estuarine sediment zinc, copper, lead, cadmium and selenium contamination gradient in Lake Macquarie, NSW, were evaluated using three approaches. Organisms were exposed to sediments in laboratory aquaria, caged in situ in the lake and lake resident organisms collected. Dose included total metal tissue burden and subcellular metal distribution to determine metabolically available metal. Response indices were total antioxidant capacity, lipid peroxidation, lysosomal stability and condition index. Bioaccumulation of total metals was higher in the laboratory and resident organisms than in those transplanted in the field but the contribution of individual metals to the total differed. Laboratory-exposed organisms had increased concentrations of cadmium and lead in their biologically active and detoxified metal fractions but not of the essential elements zinc and copper. Subcellular metal distribution patterns were the same in resident organisms but cadmium and lead burdens were higher in both fractions. Biomarker responses were similar in laboratory, transplanted and resident organisms. Total antioxidant capacity was significantly reduced and lipid peroxidation and lysosomal destabilisation significantly increased in all metal-exposed organisms compared with the reference A. trapezia. Condition index of laboratory-exposed organisms was significantly lower than in situ, resident and reference organisms. Clear metal exposure–dose–response relationships have been demonstrated for A. trapezia in laboratory and in situ experiments. Non-resident organisms, in both exposure scenarios, gave similar responses to resident metal-exposed organisms, showing all approaches are valid when investigating effects in this species.


References

[1]  W. J. Adams, R. Blust, U. Borgmann, K. V. Brix, D. K. DeForest, A. S. Green, J. S. Meyer, J. C. McGeer, P. R. Paquin, P. S. Rainbow, C. M. Wood, Utility of tissue residues for predicting effects of metals on aquatic organisms. Integr. Environ. Assess. Manag. 2011, 7, 75.
Utility of tissue residues for predicting effects of metals on aquatic organisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvFOjsLk%3D&md5=d5c736878fdb70407c4e8b2ac55bee3aCAS | 21184570PubMed |

[2]  ASTM E1688-10. Standard Guide for Determination of the Bioaccumulation of Sediment-Associated Contaminants by Benthic Invertebrates 2010 (ASTM International, West Conshohocken, PA).

[3]  S. N. Luoma, P. S. Rainbow, Metal Contamination in Aquatic Environments: Science and Lateral Management 2008 (Cambridge University Press: Cambridge, UK).

[4]  A. Burt, W. Maher, A. Roach, F. Krikowa, P. Honkoop, B. L. Bayne, The accumulation of Zn, Se, Cd and Pb and physiological condition of Anadara trapezia transplanted to a contamination gradient in Lake Macquarie, New South Wales, Australia. Mar. Environ. Res. 2007, 64, 54.
The accumulation of Zn, Se, Cd and Pb and physiological condition of Anadara trapezia transplanted to a contamination gradient in Lake Macquarie, New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvFOmurg%3D&md5=40663e34586657bf5ccbcc6cc2514afcCAS | 17306363PubMed |

[5]  H. A. Schmitz, W. A. Maher, A. M. Taylor, F. Krikowa, Effects of cadmium accumulation from suspended sediments and phytoplankton on the oyster Saccostrea glomerata. Aquat. Toxicol. 2015, 160, 22.
Effects of cadmium accumulation from suspended sediments and phytoplankton on the oyster Saccostrea glomerata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhs1Sgur8%3D&md5=769143094c1383e64fb6051bf868f3bfCAS | 25577692PubMed |

[6]  A. M. Taylor, W. A. Maher, Exposure–dose–response of Anadara trapezia to metal-contaminated estuarine sediments 1. Cadmium-spiked sediments. Aquat. Toxicol. 2012, 109, 234.
Exposure–dose–response of Anadara trapezia to metal-contaminated estuarine sediments 1. Cadmium-spiked sediments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XitFCgsLs%3D&md5=d08fd5d381d285f1dccb0c8a26cd38f9CAS | 22014600PubMed |

[7]  A. M. Taylor, W. A. Maher, Exposure–dose–response of Anadara trapezia to metal-contaminated estuarine sediments 2. Lead-spiked sediments. Aquat. Toxicol. 2012, 116–117, 79.
Exposure–dose–response of Anadara trapezia to metal-contaminated estuarine sediments 2. Lead-spiked sediments.Crossref | GoogleScholarGoogle Scholar | 22466358PubMed |

[8]  A. M. Taylor, W. A. Maher, Exposure–dose–response of Anadara trapezia to metal-contaminated estuarine sediments 3. Selenium-spiked sediments. Aquat. Toxicol. 2012, 124–125, 152.
Exposure–dose–response of Anadara trapezia to metal-contaminated estuarine sediments 3. Selenium-spiked sediments.Crossref | GoogleScholarGoogle Scholar | 22963858PubMed |

[9]  A. M. Taylor, W. A. Maher, Exposure–dose–response of Tellina deltoidalis to metal-contaminated estuarine sediments: 1. Cadmium-spiked sediments. Comp Biochem Physiol. C: Toxicol Pharmacol. 2013, 158, 44.
| 1:CAS:528:DC%2BC3sXhtVOrurvL&md5=e187c9108f12c40b16b2fc9d2eca1f9cCAS |

[10]  A. M. Taylor, W. A. Maher, Exposure–dose–response of Tellina deltoidalis to metal-contaminated estuarine sediments 2. Lead-spiked sediments. Comp Biochem Physiol. C: Toxicol Pharmacol. 2014, 159, 52.
| 1:CAS:528:DC%2BC3sXhvFSjsr%2FN&md5=e2ccfc3c8a6891de27c6b056711e4deaCAS |

[11]  A. M. Taylor, W. A. Maher, Exposure–dose–response of Tellina deltoidalis to metal-contaminated estuarine sediments 3. Selenium-spiked sediments. Comp Biochem Physiol. C: Toxicol Pharmacol. 2014, 166, 34.
| 1:CAS:528:DC%2BC2cXht1Cks73P&md5=6644ffe3d930cb3381bab0bd1066b77dCAS |

[12]  A. M. Taylor, W. A. Maher, Establishing metal exposure–dose–response relationships in marine organisms: illustrated with a case study of cadmium toxicity in Tellina deltoidalis, in New Oceanography Research Developments: Marine Chemistry, Ocean Floor Analyses and Marine Phytoplankton (Eds K. Puopolo, L. Martorino) 2010. p. 1–57 (Nova Science: New York).

[13]  Methods for Measuring the Toxicity and Bioaccumulation of Sediment-Associated Contaminants with Freshwater Invertebrates. USEPA 600/R-99/064March 2000, 2nd edn 2000 (US EPA: Duluth, MN).

[14]  M. N. Moore, J. P. Shaw, D. R. Ferrar Adams, A. Viarengo, Anti-oxidative cellular protection effect of fasting-induced autophagy as a mechanism for hormesis. Mar. Environ. Res. 2015, 107, 35.
Anti-oxidative cellular protection effect of fasting-induced autophagy as a mechanism for hormesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXmt1Wluro%3D&md5=df4edcba49610ae24b2d5ee07eed352aCAS | 25881010PubMed |

[15]  A. Roach, Assessment of metals in sediments from Lake Macquarie, New South Wales, Australia, using normalisation models and sediment quality guidelines. Mar. Environ. Res. 2005, 59, 453.
Assessment of metals in sediments from Lake Macquarie, New South Wales, Australia, using normalisation models and sediment quality guidelines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVyrsbnN&md5=2171f20fd50879352f6fb229d495bab7CAS | 15603769PubMed |

[16]  AWACS, Lake Macquarie Estuary Process Study, Australian Water and Coastal Studies Report 94/25 Vol 1 1995 (JH & ES Laxton Pty Ltd: Newcastle City Council, NSW, Australia).

[17]  D. J. H. Phillips, Use of macroalgae and invertebrates as monitors of metal levels in estuaries and coastal waters, in Heavy Metals in the Marine Environment (Ed. R.W. Furness. P.S. Rainbow) 1990, Ch. 6, pp. 81–99. (CRC Press: Boca Raton, FL).

[18]  D. J. H. Phillips, P. S. Rainbow, Biomonitoring of Trace Aquatic Contaminants 1994, pp. 51–78 (Chapman & Hall: London Oxford).

[19]  R. Rai, The use of Anadara trapezia as a bioindicator of cadmium, copper, and zinc pollutants in estuarine environments 1998, M.Ap.Sc.(Research) thesis, University of Canberra, ACT.

[20]  G. E. Sullivan, Functional morphology, micro-anatomy and histology of the ‘Sydney cockle’ Anadara trapezia (Deshayes) (Lamellibranchia: Arcidae). Aust. J. Zool. 1961, 9, 219.
Functional morphology, micro-anatomy and histology of the ‘Sydney cockle’ Anadara trapezia (Deshayes) (Lamellibranchia: Arcidae).Crossref | GoogleScholarGoogle Scholar |

[21]  G. E. Batley, Heavy metal speciation in waters, sediments and biota from Lake Macquarie, New South Wales. Aust. J. Mar. Freshwater Res. 1987, 38, 591.
Heavy metal speciation in waters, sediments and biota from Lake Macquarie, New South Wales.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXotFGktw%3D%3D&md5=a9e8b110e611a48af6c545a354e3e996CAS |

[22]  D. J. Cain, S. N. Luoma, Copper and silver accumulation in transplanted and resident clams (Macoma balthica) in south San Francisco Bay. Mar. Environ. Res. 1985, 15, 115.
Copper and silver accumulation in transplanted and resident clams (Macoma balthica) in south San Francisco Bay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXksVaitb0%3D&md5=9338e461b63fff943f80940768c4b860CAS |

[23]  Y. Couillard, P. G. C. Campbell, A. Tessier, J. Pellerin-Massicotte, J. G. Auclair, Field transplantation of a freshwater bivalve, Pyganodon grandis, across a metal contamination gradient. I. Temporal changes in metallothionein and metal (Cd, Cu, and Zn) concentrations in soft tissues. Can. J. Fish. Aquat. Sci. 1995, 52, 690.
Field transplantation of a freshwater bivalve, Pyganodon grandis, across a metal contamination gradient. I. Temporal changes in metallothionein and metal (Cd, Cu, and Zn) concentrations in soft tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXovFersrg%3D&md5=13083e2ac3e3d580e36f3dcf1c8624d6CAS |

[24]  Y. Couillard, P. G. C. Campbell, A. Tessier, J. Pellerin-Massicotte, J. G. Auclair, Field transplantation of a freshwater bivalve, Pyganodon grandis, across a metal contamination gradient. II. Metallothionein response to Cd and Zn exposure, evidence for cytotoxicity, and links to effects at higher levels of biological organization. Can. J. Fish. Aquat. Sci. 1995, 52, 703.
Field transplantation of a freshwater bivalve, Pyganodon grandis, across a metal contamination gradient. II. Metallothionein response to Cd and Zn exposure, evidence for cytotoxicity, and links to effects at higher levels of biological organization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXovFersrk%3D&md5=dbd040624be1c52e85a93f7a2a1ef609CAS |

[25]  T. H. Dewitt, C. W. Hickey, D. J. Morrisey, M. G. Nipper, D. S. Roper, R. B. Williamson, L. V. Dam, E. K. Williams, Do amphipods have the same concentration-response to contaminated sediment in situ as in vitro? Environ. Toxicol. Chem. 1999, 18, 1026.
Do amphipods have the same concentration-response to contaminated sediment in situ as in vitro?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXislSltr4%3D&md5=3e613cdcf0e04b928fd9901dbe21881bCAS |

[26]  D. Martinčić, Ž. Kwokal, Ž. Peharec, D. Marguš, M. Branica, Distribution of Zn, Pb, Cd and Cu between seawater and transplanted mussels (Mytilus galloprovincialis). Sci. Total Environ. 1992, 119, 211.
Distribution of Zn, Pb, Cd and Cu between seawater and transplanted mussels (Mytilus galloprovincialis).Crossref | GoogleScholarGoogle Scholar |

[27]  G. P. Quinn, M. J. Keough, Multifactor Analysis of Variance. Experimental Design and Data Analysis for Biologists 2002, pp. 208–261 (Cambridge University Press; Cambridge, UK).

[28]  A. J. de Groot, Metals and sediments: a global perspective, in Metal-Contaminated Aquatic Sediments (Ed. H. E. Allen) 1995, pp. 1–16 (Ann Arbor Press Inc.: Ann Arbor, MI, USA).

[29]  S. Baldwin, M. Deaker, W. Maher, Low-volume microwave digestion of marine biological tissues for the measurement of trace elements. Analyst 1994, 119, 1701.
Low-volume microwave digestion of marine biological tissues for the measurement of trace elements.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmtVSgtLo%3D&md5=47a2c8a26192561fbe0f24c1ae456ab4CAS | 7978323PubMed |

[30]  I. M. Sokolova, A. H. Ringwood, C. Johnson, Tissue-specific accumulation of cadmium in subcellular compartments of eastern oysters Crassostrea virginica Gmelin (Bivalvia: Ostreidae). Aquat. Toxicol. 2005, 74, 218.
Tissue-specific accumulation of cadmium in subcellular compartments of eastern oysters Crassostrea virginica Gmelin (Bivalvia: Ostreidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXns1WjsbY%3D&md5=a48996151766d5b5083ffb537c272a1dCAS | 15993495PubMed |

[31]  W. G. Wallace, B. G. Lee, S. N. Luoma, Subcellular compartmentalization of Cd and Zn in two bivalves. I. Significance of metal-sensitive fractions (MSF) and biologically detoxified metal (BDM). Mar. Ecol. Prog. Ser. 2003, 249, 183.
Subcellular compartmentalization of Cd and Zn in two bivalves. I. Significance of metal-sensitive fractions (MSF) and biologically detoxified metal (BDM).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkt1Shsbs%3D&md5=6c6eb89abcf5959203b089a45a8a248bCAS |

[32]  J. M. Graham, Homogenization of tissues and cells, in Subcellular Fractionation: A Practical Approach (Eds J. M. Graham, D. Rickwood) 1997, pp. 1–29 (Oxford University Press: Oxford, UK).

[33]  Antioxidant Assay Kit User Protocol Catalog number 709001 2011 (Cayman Chemical Company: Ann Arbor, MI, USA).

[34]  Oxitek TBARS Assay Kit User Protocol ZMC Catalog number 0801192 2011 (ZepoMetrix Corporation: Buffalo, NY, USA).

[35]  A. H. Ringwood, J. Hoguet, C. J. Keppler, M. L. Gielazyn, C. H. Ward, A. R. Rourk, Cellular Biomarkers (Lysosomal Destabilization, Glutathione & Lipid Peroxidation) in Three Common Estuarine Species: A Methods Handbook 2003 (Marine Resources Research Institute, South Carolina Department of Natural Resources: Charleston, SC).

[36]  S. Duquesne, M. Liess, D. J. Bird, Sublethal effects of metal exposure: physiological and behavioural responses of the estuarine bivalve Macoma balthica. Mar. Environ. Res. 2004, 58, 245.
Sublethal effects of metal exposure: physiological and behavioural responses of the estuarine bivalve Macoma balthica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkslSisb8%3D&md5=329b4d7117ef05c0c6dcb8e298dc1f42CAS | 15178039PubMed |

[37]  J. Kirby, W. Maher, F. Krikowa, Selenium, cadmium, copper, and zinc concentrations in sediments and mullet (Mugil cephalus) from the southern basin of Lake Macquarie, NSW, Australia. Arch. Environ. Contam. Toxicol. 2001, 40, 246.
Selenium, cadmium, copper, and zinc concentrations in sediments and mullet (Mugil cephalus) from the southern basin of Lake Macquarie, NSW, Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtV2ks70%3D&md5=9c250d0c82ca46bc52f644510e1683dbCAS | 11243327PubMed |

[38]  G. M. Peters, W. A. Maher, F. Krikowa, A. C. Roach, H. K. Jeswani, J. P. Barford, V. G. Gomes, D. D. Reible, Selenium in sediments, pore waters and benthic in fauna of Lake Macquarie, New South Wales, Australia. Mar. Environ. Res. 1999, 47, 491.
Selenium in sediments, pore waters and benthic in fauna of Lake Macquarie, New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitlehtb8%3D&md5=7a87bdaa7ffd9480d20e235d46fd5a44CAS |

[39]  P. S. Roy, E. A. Crawford, Heavy metals in a contaminated Australian estuary – dispersion and accumulation trend. Estuar. Coast. Shelf Sci. 1984, 19, 341.
Heavy metals in a contaminated Australian estuary – dispersion and accumulation trend.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXosVSksw%3D%3D&md5=36c02990d16401da8af41f090225682eCAS |

[40]  Australian Guidelines for Water-Quality Monitoring and Reporting. National Water Quality Management Strategy Paper number 4 2000 (Australian and New Zealand Environment and Conservation Council and Agriculture and Resource Management Council of Australia and New Zealand: Canberra, ACT).

[41]  B. Carroll, A review of selenium and heavy metal contamination of Lake Macquarie, New South Wales due to power generation and lead–zinc smelting. 1996 (Australian Minerals & Energy Environment Foundation; Melbourne).

[42]  K. Simkiss, A. Z. Mason, Cellular responses of molluscan tissues to environmental metals. Mar. Environ. Res. 1984, 14, 103.
Cellular responses of molluscan tissues to environmental metals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXmtVGgsLY%3D&md5=54ec120bf6895d4c29c19d40ee8f2ed2CAS |

[43]  P. B. Lobel, C. D. Bajdik, S. P. Belkhode, S. E. Jackson, H. P. Longerich, Improved protocol for collecting mussel watch specimens taking into account sex, size, condition, shell shape, and chronological age. Arch. Environ. Contam. Toxicol. 1991, 21, 409.
Improved protocol for collecting mussel watch specimens taking into account sex, size, condition, shell shape, and chronological age.Crossref | GoogleScholarGoogle Scholar |

[44]  I. M. Sokolova, S. Evans, F. M. Hughes, Cadmium-induced apoptosis in oyster hemocytes involves disturbance of cellular energy balance but no mitochondrial permeability transition. J. Exp. Biol. 2004, 207, 3369.
Cadmium-induced apoptosis in oyster hemocytes involves disturbance of cellular energy balance but no mitochondrial permeability transition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpslOlu78%3D&md5=26cc8aa7fdaadda1da3dab1a695be13cCAS | 15326213PubMed |

[45]  A. H. Ringwood, D. E. Connors, A. DiNovo, The effects of copper exposures on cellular responses in oysters. Mar. Environ. Res. 1998, 46, 591.
The effects of copper exposures on cellular responses in oysters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmtVOhtr4%3D&md5=eac06a0f9f15028ee598f34f9837b795CAS |

[46]  A. H. Ringwood, J. Hoguet, C. Keppler, M. Gielazyn, Linkages between cellular biomarker responses and reproductive success in oysters – Crassostrea virginica. Mar. Environ. Res. 2004, 58, 151.
Linkages between cellular biomarker responses and reproductive success in oysters – Crassostrea virginica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkslSis7k%3D&md5=1494758dd4d3f489e03d6c4fbd006eb0CAS | 15178027PubMed |

[47]  G. Frenzilli, R. Bocchetti, M. Pagliarecci, M. Nigro, F. Annarumma, V. Scarcelli, D. Fattorini, F. Regoli, Time-course evaluation of ROS-mediated toxicity in mussels, Mytilus galloprovincialis, during a field translocation experiment. Mar. Environ. Res. 2004, 58, 609.
Time-course evaluation of ROS-mediated toxicity in mussels, Mytilus galloprovincialis, during a field translocation experiment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkslSiurs%3D&md5=c0328b6f895ba446d93471a73e02a195CAS | 15178087PubMed |

[48]  F. Regoli, G. Frenzilli, R. Bocchetti, F. Annarumma, V. Scarcelli, D. Fattorini, M. Nigro, Time-course variations of oxyradical metabolism, DNA integrity and lysosomal stability in mussels, Mytilus galloprovincialis, during a field translocation experiment. Aquat. Toxicol. 2004, 68, 167.
Time-course variations of oxyradical metabolism, DNA integrity and lysosomal stability in mussels, Mytilus galloprovincialis, during a field translocation experiment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktVCnt7o%3D&md5=45f412da0148a2201469e4bc19eac825CAS | 15145226PubMed |

[49]  S. Moncheva, S. Trakhtenberg, E. Katrich, M. Zemser, I. Goshev, F. Toledo, P. Arancibia-Avila, V. Doncheva, S. Gorinstein, Total antioxidant capacity in the black mussel (Mytilus galloprovincialis) from Black Sea coasts. Estuar. Coast. Shelf Sci. 2004, 59, 475.
Total antioxidant capacity in the black mussel (Mytilus galloprovincialis) from Black Sea coasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvFCisbo%3D&md5=3f33a0b69f0afd64e26a38eb6325e578CAS |

[50]  F. Regoli, Total oxyradical scavenging capacity (TOSC) in polluted and translocated mussels: a predictive biomarker of oxidative stress. Aquat. Toxicol. 2000, 50, 351.
Total oxyradical scavenging capacity (TOSC) in polluted and translocated mussels: a predictive biomarker of oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtVCksr4%3D&md5=6a98068255c828c825edfe30960f71a4CAS | 10967397PubMed |

[51]  F. Regoli, G. Principato, Glutathione, glutathione-dependent and antioxidant enzymes in mussel, Mytilus galloprovincialis, exposed to metals under field and laboratory conditions: implications for the use of biochemical biomarkers. Aquat. Toxicol. 1995, 31, 143.
Glutathione, glutathione-dependent and antioxidant enzymes in mussel, Mytilus galloprovincialis, exposed to metals under field and laboratory conditions: implications for the use of biochemical biomarkers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjvVensL8%3D&md5=145a0310a9d24973546cfef36bacff32CAS |

[52]  L. Camus, D. M. Pampanin, E. Volpato, E. Delaney, S. Sanni, C. Nasci, 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, 801.
Total oxyradical scavenging capacity responses in Mytilus galloprovincialis transplanted into the Venice Lagoon (Italy) to measure the biological impact of anthropogenic activities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpsVKjt70%3D&md5=50db50f90a372846c8c81506d802daeaCAS | 15530524PubMed |

[53]  M. Aloísio Torres, C. Pires Testa, C. Gáspari, M. Beatriz Masutti, C. Maria Neves Panitz, R. Curi-Pedrosa, E. Alves de Almeida, P. Di Mascio, D. Wilhelm Filho, Oxidative stress in the mussel Mytella guyanensis from polluted mangroves on Santa Catarina Island, Brazil. Mar. Pollut. Bull. 2002, 44, 923.
Oxidative stress in the mussel Mytella guyanensis from polluted mangroves on Santa Catarina Island, Brazil.Crossref | GoogleScholarGoogle Scholar |

[54]  R. Company, A. Serafim, M. J. Bebianno, R. Cosson, B. Shillito, A. Fiala-Medioni, Effect of cadmium, copper and mercury on antioxidant enzyme activities and lipid peroxidation in the gills of the hydrothermal vent mussel Bathymodiolus azoricus. Mar. Environ. Res. 2004, 58, 377.
Effect of cadmium, copper and mercury on antioxidant enzyme activities and lipid peroxidation in the gills of the hydrothermal vent mussel Bathymodiolus azoricus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkslSit74%3D&md5=c42ebd3ea6275e7fbc31a6732a780ff8CAS | 15178056PubMed |

[55]  S. Gorinstein, R. E. Jung, S. Moncheva, P. Arancibia-Avila, Y.-S. Park, S.-G. Kang, I. Goshev, S. Trakhtenberg, J. Namiesnik, Partial characterization of proteins from mussels Mytilus galloprovincialis as a biomarker of contamination. Arch. Environ. Contam. Toxicol. 2005, 49, 504.
Partial characterization of proteins from mussels Mytilus galloprovincialis as a biomarker of contamination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFCqsrzL&md5=863a1d94b5419d02220d4968e3d7abdeCAS | 16170449PubMed |

[56]  G. W. Winston, R. T. Di Giulio, Prooxidant and antioxidant mechanisms in aquatic organisms. Aquat. Toxicol. 1991, 19, 137.
Prooxidant and antioxidant mechanisms in aquatic organisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXks1Kgsrc%3D&md5=e1fc6b37f7d148829e1aa932cab4197bCAS |

[57]  N. Ercal, H. Gurer-Orhan, N. Aykin-Burns, Toxic metals and oxidative stress part 1: mechanisms involved in metal-induced oxidative damage. Curr. Top. Med. Chem. 2001, 1, 529.
Toxic metals and oxidative stress part 1: mechanisms involved in metal-induced oxidative damage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXos1ait7s%3D&md5=707133a839c79f30ab2e151e300aa2c3CAS | 11895129PubMed |

[58]  E. A. de Almeida, S. Miyamoto, A. C. D. Bainy, M. H. G. Medeiros, P. Di Mascio, Protective effect of phospholipid hydroperoxide glutathione peroxidase (PHGPx) against lipid peroxidation in mussels Perna perna exposed to different metals. Mar. Pollut. Bull. 2004, 49, 386.
Protective effect of phospholipid hydroperoxide glutathione peroxidase (PHGPx) against lipid peroxidation in mussels Perna perna exposed to different metals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvFSiurY%3D&md5=860d7462430279448e81c24c8e22549aCAS | 15325206PubMed |

[59]  L. R. Bacanskas, J. Whitaker, R. T. Di Giulio, Oxidative stress in two populations of killifish (Fundulus heteroclitus) with differing contaminant exposure histories. Mar. Environ. Res. 2004, 58, 597.
Oxidative stress in two populations of killifish (Fundulus heteroclitus) with differing contaminant exposure histories.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkslSiur0%3D&md5=6c4a4b47c5864e9da03bdce72aa2d581CAS | 15178085PubMed |

[60]  S. M. Bard, Multixenobiotic resistance as a cellular defense mechanism in aquatic organisms. Aquat. Toxicol. 2000, 48, 357.
Multixenobiotic resistance as a cellular defense mechanism in aquatic organisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXislWhsrk%3D&md5=18ef16b6c752f4a0d08e0bc9814b75b4CAS | 10794825PubMed |

[61]  C. Bolognesi, G. Frenzilli, C. Lasagna, E. Perrone, P. Roggieri, Genotoxicity biomarkers in Mytilus galloprovincialis: wild versus caged mussels. Mutat. Res. Fundam. Mol. Mech. Mutagen. 2004, 552, 153.
Genotoxicity biomarkers in Mytilus galloprovincialis: wild versus caged mussels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmt1Kntrw%3D&md5=30ddd7ec638d0497af1dc23004f05f5dCAS |

[62]  M. Ferreira, M. Caetano, J. Costa, P. Pousão-Ferreira, C. Vale, M. A. Reis-Henriques, Metal accumulation and oxidative stress responses in, cultured and wild, white seabream from north-west Atlantic. Sci. Total Environ. 2008, 407, 638.
Metal accumulation and oxidative stress responses in, cultured and wild, white seabream from north-west Atlantic.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVWhsr%2FJ&md5=bff98ca6a76bfd513fd13ca7a4623c0fCAS | 18783819PubMed |

[63]  V. K. Mubiana, K. Vercauteren, R. Blust, The influence of body size, condition index and tidal exposure on the variability in metal bioaccumulation in Mytilus edulis. Environ. Pollut. 2006, 144, 272.
The influence of body size, condition index and tidal exposure on the variability in metal bioaccumulation in Mytilus edulis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptVGltL8%3D&md5=8483b95a3350f77d3dcbe3602dddd1b9CAS | 16513234PubMed |

[64]  W. M. De Coen, C. R. Janssen, The missing biomarker link: relationships between effects on the cellular energy allocation biomarker of toxicant-stressed Daphnia magna and corresponding population characteristics. Environ. Toxicol. Chem. 2003, 22, 1632.
The missing biomarker link: relationships between effects on the cellular energy allocation biomarker of toxicant-stressed Daphnia magna and corresponding population characteristics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXot1Wrurg%3D&md5=d6d96a3cb925ee60861e245efa228d4dCAS | 12836990PubMed |

[65]  M. Erk, D. Ivankovic, Z. Strizak, Selection of target mussel tissue for application of cellular energy allocation as a physiological biomarker in native mussels Mytilus galloprovincialis (Lamarck, 1819). J. Shellfish Res. 2012, 31, 61.
Selection of target mussel tissue for application of cellular energy allocation as a physiological biomarker in native mussels Mytilus galloprovincialis (Lamarck, 1819).Crossref | GoogleScholarGoogle Scholar |

[66]  L. Moolman, J. H. J. Van Vuren, V. Wepener, Comparative studies on the uptake and effects of cadmium and zinc on the cellular energy allocation of two freshwater gastropods. Ecotoxicol. Environ. Saf. 2007, 68, 443.
Comparative studies on the uptake and effects of cadmium and zinc on the cellular energy allocation of two freshwater gastropods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFers73O&md5=59054291b1d3c3db95bd5f749f0c2a4bCAS | 17303241PubMed |

[67]  R. Smolders, L. Bervoets, W. De Coen, R. Blust, Cellular energy allocation in zebra mussels exposed along a pollution gradient: linking cellular effects to higher levels of biological organization. Environ. Pollut. 2004, 129, 99.
Cellular energy allocation in zebra mussels exposed along a pollution gradient: linking cellular effects to higher levels of biological organization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvFOrsA%3D%3D&md5=15514a93992252ca023a95068d89d227CAS | 14749074PubMed |

[68]  T. Jager, A. Barsi, N. T. Hamda, B. T. Martin, E. I. Zimmer, V. Ducrot, Dynamic energy budgets in population ecotoxicology: applications and outlook. Ecol. Modell. 2014, 280, 140.
Dynamic energy budgets in population ecotoxicology: applications and outlook.Crossref | GoogleScholarGoogle Scholar |

[69]  I. M. Sokolova, Energy-limited tolerance to stress as a conceptual framework to integrate the effects of multiple stressors. Integr. Comp. Biol. 2013, 53, 597.
Energy-limited tolerance to stress as a conceptual framework to integrate the effects of multiple stressors.Crossref | GoogleScholarGoogle Scholar | 23615362PubMed |

[70]  I. M. Sokolova, M. Frederich, R. Bagwe, G. Lannig, A. A. Sukhotin, Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar. Environ. Res. 2012, 79, 1.
Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVeqtL7L&md5=d18b9c2863a4b8226d04d4ee16ee510fCAS | 22622075PubMed |