Bioavailability and toxicity of zinc from contaminated freshwater sediments: Linking exposure-dose-response relationships of the freshwater bivalve Hyridella australis to zinc-spiked sediments

Aquatic Toxicology

Volumn 156, Issue , 2014, Pages 179-190

  Marasinghe Wadige, Chamani P M ^a   Taylor, Anne M ^a   Maher, William A ^a   Krikowa, Frank ^a  

^a UNIVERSITY OF CANBERRA   (Australia)

Author keywords

Biologically active zinc; Biologically detoxified zinc; Biomarkers; Freshwater bivalve; Oxidative stress; Sub cellular partitioning

Indexed keywords

CALCIUM; METALLOTHIONEIN; SURFACE WATER; ZINC; BIOLOGICAL MARKER; FRESH WATER; WATER POLLUTANT;

ANTIOXIDANT; BIOAVAILABILITY; BIOMARKER; BIOMONITORING; BIVALVE; DOSE-RESPONSE RELATIONSHIP; ECOTOXICOLOGY; FRESHWATER SEDIMENT; LIPID; PARTITIONING; SUBLETHAL EFFECT; TOXICITY; ZINC;

ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BIOACCUMULATION; BIOAVAILABILITY; BIOLOGICAL MONITORING; BIVALVE; CELLULAR DISTRIBUTION; CONCENTRATION RESPONSE; ENVIRONMENTAL EXPOSURE; FRESHWATER ENVIRONMENT; FRESHWATER SEDIMENT CONTAMINATION; HEPATOPANCREAS; HYRIDELLA AUSTRALIS; LIPID PEROXIDATION; LYSOSOME MEMBRANE; METAL TOLERANCE; MICROCOSM; MICROSOME; NONHUMAN; TISSUE LEVEL; TOXICITY TESTING; WATER CONTAMINATION; WATER POLLUTION INDICATOR; ANIMAL; CHEMISTRY; DRUG EFFECTS; GILL; METABOLISM; SEDIMENT; TOXICITY; WATER POLLUTANT;

BIVALVIA; HYRIDELLA AUSTRALIS;

ANIMALS; BIOLOGICAL AVAILABILITY; BIOLOGICAL MARKERS; BIVALVIA; ENVIRONMENTAL EXPOSURE; FRESH WATER; GEOLOGIC SEDIMENTS; GILLS; HEPATOPANCREAS; METALLOTHIONEIN; WATER POLLUTANTS, CHEMICAL; ZINC;

EID: 84908013087     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2014.08.012     Document Type: Article

References (92)

1. Adams S.M., Shorey C.D. Energy dispersive spectroscopy of granular concretions in the mantle of the freshwater mussel Hyridella depressa from Lake Burragorang as a technique to monitor metals in aquatic systems. Aquatic Toxicol. 1998, 44(1-2):93-102.
2. Adams S.M., Shorey C.D., Byrne M. An ultrastructural and microanalytical study of metal-ion content in granular concretions of the freshwater mussel Hyridella depressa. Micron 1997, 28(1):1-11.
3. Alves De Almeida E., Celso Dias Bainy A., Paula De Melo Loureiro A., Regina Martinez G., Miyamoto S., Onuki J., Fujita Barbosa L., Carrião Machado Garcia C., Manso Prado F., Eliza Ronsein G., Alexandre Sigolo C., Barbosa Brochini C., Maria Gracioso Martins A., Helena Gennari De Medeiros M., Di Mascio P. Oxidative stress in Perna perna and other bivalves as indicators of environmental stress in the Brazilian marine environment: antioxidants, lipid peroxidation and DNA damage. Comp. Biochem. Physiol. Part A: Mol. Integrat. Physiol. 2007, 146(4):588-600.
4. Amiard J.C., Geffard A., Amiard-Triquet C., Crouzet C. Relationship between the lability of sediment-bound metals (Cd, Cu, Zn) and their bioaccumulation in benthic invertebrates. Estuarine, Coastal Shelf Sci. 2007, 72(3):511-521.
5. AZZECC/ARMCANZ, 2000. Australian and New Zealand Guidelines for Fresh and Marine Water Quality. Australian and New Zealand Environment and Conservation Council/Agriculture and resource Management council of Australia and New Zealand, Canberra, ACT.
6. Arakel A.V. Towards developing sediment quality assessment guidelines for aquatic systems: an Australian perspective. Austral. J. Earth Sci. 1995, 42(4):335-369.
7. ASTM-E1688-10, 2010. Standard Guide for Determination of the Bioaccumulation of Sediment-Associated Contaminants by Benthic Invertebrates, E1688-10. American Society for Testing and Materials, West Conshohocken, PA, USA.
8. Azevedo M.-M., Carvalho A., Pascoal C., Rodrigues F., Cássio F. Responses of antioxidant defenses to Cu and Zn stress in two aquatic fungi. Sci. Total Environ. 2007, 377(2-3):233-243.
9. Baldwin S., Deaker M., Maher W. Low-volume microwave digestion of marine biological tissues for the measurement of trace elements. Analyst 1994, 119(8):1701-1704.
10. Batty L.C., Auladell M., Sadler J., Hallberg K. The impacts of metalliferous drainage on aquatic communities in streams and rivers. Ecol. Indust. Pollut. 2010, 70-100.
11. Baudrimont M., Andres S., Durrieu G., Boudou A. The key role of metallothioneins in the bivalve Corbicula fluminea during the depuration phase, after in situ exposure to Cd and Zn. Aquat. Toxicol. 2003, 63(2):89-102.
12. Besser J.M., Brumbaugh W.G., Kemble N.E., Ivey C.D., Kunz J.L., Ingersoll C.G., Rudel D. Toxicity of nickel-spiked freshwater sediments to benthic invertebrates-spiking methodology, species sensitivity, and nickel bioavailability. US Geological Survey, Scient. Investig. Rep. 2011, 5225.
13. Bollhöfer A. Stable lead isotope ratios and metals in freshwater mussels from a uranium mining environment in Australia's wet-dry tropics. Appl. Geochem. 2012, 27(1):171-185.
14. Bonneris E., Perceval O., Masson S., Hare L., Campbell P.G.C. Sub-cellular partitioning of Cd, Cu and Zn in tissues of indigenous unionid bivalves living along a metal exposure gradient and links to metal-induced effects. Environ. Pollut. 2005, 135(2):195-208.
15. Bray T.M., Bettger W.J. The physiological role of zinc as an antioxidant. Free Rad. Biol. Med. 1990, 8(3):281-291.
16. Byrne M., Vesk P.A. Microanalysis of elements in granules in Hyridella depressa (Bivalvia): multivariate analysis and biomonitoring potential. Austral. J. Ecotoxicol. 1997, 2(2):91-97.
17. Byrne M., Vesk P.A. Elemental composition of mantle tissue granules in Hyridella depressa (Unionida) from the Hawkesbury-Nepean River system, Australia: inferences from catchment chemistry. Marine Freshwater Res. 2000, 51(2):183-192.
18. Cameron J.N. Unusual aspects of calcium-metabolism in aquatic animals. Ann. Rev. Physiol. 1990, 52:77-95.
19. Campana O., Rodríguez A., Blasco J. Evaluating the suitability of Hydrobia ulvae as a test species for sediment metal toxicity testing applying a tissue residue approach to metal mixtures in laboratory and field exposures. Chemosphere 2013, 91(8):1136-1145.
20. Canli M. Elimination of essential (Cu, Zn) and non-essential (Cd, Pb) metals from tissues of a freshwater fish Tilapia zilli. Turk. J. Zool. 2000, 24:429-436.
21. Cayman, 2011. Antioxidant Assay Kit User Protocol 709001.
22. Chapman P.M., Wang F., Janssen C., Persoone G., Allen H.E. Ecotoxicology of metals in aquatic sediments: binding and release, bioavailability, risk assessment, and remediation. Can. J. Fisheries Aquatic Sci. 1998, 55(10):2221-2243.
23. Ciutat A., Anschutz P., Gerino M., Boudou A. Effects of bioturbation on cadmium transfer and distribution into freshwater sediments. Environ. Toxicol. Chem. 2005, 24(5):1048-1058.
24. Cooper S., Bonneris E., Michaud A., Pinel-Alloul B., Campbell P.G.C. Influence of a step-change in metal exposure (Cd, Cu, Zn) on metal accumulation and subcellular partitioning in a freshwater bivalve, Pyganodon grandis: a long-term transplantation experiment between lakes with contrasting ambient metal levels. Aquat. Toxicol. 2013, 132-133(0):73-83.
25. Cossu C., Doyotte A., Babut M., Exinger A., Vasseur P. Antioxidant biomarkers in freshwater bivalves, Unio tumidus, in response to different contamination profiles of aquatic sediments. Ecotoxicol. Environ. Saf. 2000, 45(2):106-121.
26. Dietz K.-J., Baier M., Krämer U. Free radicals and reactive oxygen species as mediators of heavy metal toxicity in plants. Heavy Metal Stress in Plants 1999, 73-97.
27. Diks D., Allen H. Correlation of copper distribution in a freshwater-sediment system to bioavailability. Bull. Environ. Contam. Toxicol. 1983, 30(1):37-43.
28. Doyen P., Vasseur P., Rodius F. Identification, sequencing and expression of selenium-dependent glutathione peroxidase transcript in the freshwater bivalve Unio tumidus exposed to Aroclor 1254. Comp. Biochem. Physiol. Part C: Toxicol. Pharmacol. 2006, 144(2):122-129.
29. Doyotte A., Cossu C., Jacquin M.-C., Babut M., Vasseur P. Antioxidant enzymes, glutathione and lipid peroxidation as relevant biomarkers of experimental or field exposure in the gills and the digestive gland of the freshwater bivalve Unio tumidus. Aquat. Toxicol. 1997, 39(2):93-110.
30. Falfushynska H.I., Gnatyshyna L.L., Stoliar O.B. Effect of in situ exposure history on the molecular responses of freshwater bivalve Anodonta anatina (Unionidae) to trace metals. Ecotoxicol. Environ. Saf. 2013, 89(0):73-83.
31. Formigari A., Irato P., Santon A. Zinc, antioxidant systems and metallothionein in metal mediated-apoptosis: biochemical and cytochemical aspects. Comp. Biochem. Physiol. Part C: Toxicol. Pharmacol. 2007, 146(4):443-459.
32. Franco J.L., Trivella D.B.B., Trevisan R., Dinslaken D.F., Marques M.R.F., Bainy A.C.D., Dafre A.L. Antioxidant status and stress proteins in the gills of the brown mussel Perna perna exposed to zinc. Chemico-Biological Interact. 2006, 160(3):232-240.
33. Fraysse B., Baudin J.P., Garnier-Laplace J., Adam C., Boudou A. Effects of Cd and Zn waterborne exposure on the uptake and depuration of Co-57, Ag-110m and Cs-134 by the Asiatic clam (Corbicula fluminea) and the zebra mussel (Dreissena polymorpha)-whole organism study. Environ. Pollut. 2002, 118(3):297-306.
34. Gazaryan I.G., Krasinskaya I.P., Kristal B.S., Brown A.M. Zinc irreversibly damages major enzymes of energy production and antioxidant defense prior to mitochondrial permeability transition. J. Biol. Chem. 2007, 282(33):24373-24380.
35. Giguère A., Couillard Y., Campbell P.G.C., Perceval O., Hare L., Pinel-Alloul B., Pellerin J. Steady-state distribution of metals among metallothionein and other cytosolic ligands and links to cytotoxicity in bivalves living along a polymetallic gradient. Aquat. Toxicol. 2003, 64(2):185-200.
36. Graham, J.M., 1997. Homogenization of tissues and cells. In: Graham, J.M., Rickwood, D., (Eds.), Subcellular Fractionation-A Practical Approach. Oxford University Press, Oxford, England, UK, pp. 1-29.
37. Griscom S.B., Fisher N.S. Bioavailability of sediment-bound metals to marine bivalve molluscs: an overview. Estuaries 2004, 27(5):826-838.
38. Guidi P., Frenzilli G., Benedetti M., Bernardeschi M., Falleni A., Fattorini D., Regoli F., Scarcelli V., Nigro M. Antioxidant, genotoxic and lysosomal biomarkers in the freshwater bivalve (Unio pictorum) transplanted in a metal polluted river basin. Aquat. Toxicol. 2010, 100(1):75-83.
39. Gundacker C. Comparison of heavy metal bioaccumulation in freshwater molluscs of urban river habitats in Vienna. Environ. Pollut. 2000, 110(1):61-71.
40. Hare L., Tessier A., Borgmann U. Metal sources for freshwater invertebrates: pertinence for risk assessment. Human Ecol. Risk Assessment 2003, 9(4):779.
41. Hemelraad J., Kleinveld H., De Roos A., Holwerda D., Zandee D. Cadmium kinetics in freshwater clams III. Effects of zinc on uptake and distribution of cadmium in Anodonta cygnea. Arch. Environ. Contam. Toxicol. 1987, 16(1):95-101.
42. Hickey C.W., Roper D.S., Buckland S.J. Metal concentrations of resident and transplanted freshwater mussels Hyridella menziesi (Unionacea: Hyriidae) and sediments in the Waikato River, New Zealand. Sci. Total Environ. 1995, 175(3):163-177.
43. Hogstrand, C., 2011. 3-Zinc. In: Chris, A.P.F., Wood, M., Colin, J.B. (Eds.), Fish Physiology. Vol. Volume 31, Part A. Academic Press, pp. 135-200.
44. Jomova K., Valko M. Advances in metal-induced oxidative stress and human disease. Toxicology 2011, 283(2-3):65-87.
45. Jones W., Walker K. Accumulation of iron, manganese, zinc and cadmium by the australian freshwater mussel Velesunio ambiguus (Phillipi) and its potential as a biological monitor. Marine Freshwater Res. 1979, 30(6):741-751.
46. Lamoureux E.M., Brownawell B.J. Chemical and biological availability of sediment-sorbed hydrophobic organic contaminants. Environ. Toxicol. Chem. 1999, 18(8):1733-1741.
47. Lowe D., Fossato V., Depledge M. Contaminant-induced lysosomal membrane damage in blood cells of mussels Mytilus galloprovincialis from the Venice Lagoon: an in vitro study. Marine Ecol. Prog. Ser. 1995, 129(1):189-196.
48. Luoma S., Rainbow P.S. Trace metal bioaccumulation. Metal Contamination in Aquatic Environments: Science and Lateral Management 2008, 126-168. Cambridge University Press, Cambridge, UK.
49. Luoma S.N. Can we determine the biological availability of sediment-bound trace elements?. Hydrobiologia 1989, 176(1):379-396.
50. Macklin M.G., Hudson-Edwards K.A., Dawson E.J. The significance of pollution from historic metal mining in the Pennine orefields on river sediment contaminant fluxes to the North Sea. Sci. Total Environ. 1997, 194-195(0):391-397.
51. Maher W., Forster S., Krikowa F., Snitch P., Chapple G., Craig P. Measurement of trace elements and phosphorus in marine animal and plant tissues by low-volume microwave digestion and ICP-MS. Atom. Spectroc.-Norwalk Connecticut 2001, 22(5):361-370.
52. Marasinghe Wadige C.P.M., Maher W.A., Taylor A.M., Krikowa F. Exposure-dose-response relationships of the freshwater bivalve Hyridella australis to cadmium spiked sediments. Aquat. Toxicol. 2014, 152(0):361-371.
53. Marasinghe Wadige C.P.M., Taylor A.M., Maher W.A., Ubrihien R.P., Krikowa F. Effects of lead-spiked sediments on freshwater bivalve, Hyridella australis: linking organism metal exposure-dose-response. Aquat. Toxicol. 2014, 149(0):83-93.
54. Marchese M., Gagneten A., Parma M., Pavé P. Accumulation and elimination of chromium by freshwater species exposed to spiked sediments. Arch. Environ. Contam. Toxicol. 2008, 55(4):603-609.
55. Marie V., Baudrimont M., Boudou A. Cadmium and zinc bioaccumulation and metallothionein response in two freshwater bivalves (Corbicula fluminea and Dreissena polymorpha) transplanted along a polymetallic gradient. Chemosphere 2006, 65(4):609-617.
56. Marigomez I., Soto M., Cajaraville M.P., Angulo E., Giamberini L. Cellular and subcellular distribution of metals in molluscs. Microsc. Res. Techniq. 2002, 56(5):358-392.
57. Markich S.J. Element Concentrations in the Soft Tissues of a Freshwater Bivalve Species from the Mammy-Johnson River, NSW, Sydney 1996, 29. Australian Nuclear Science and Technology Organisation, ANSTO Report C485.
58. Markich S.J., Brown P.L., Jeffree R.A. Divalent metal accumulation in freshwater bivalves: an inverse relationship with metal phosphate solubility. Sci. Total Environ. 2001, 275(1-3):27-41.
59. Markich S.J., Jeffree R.A. Absorption of divalent trace metals as analogues of calcium by Australian freshwater bivalves: an explanation of how water hardness reduces metal toxicity. Aquat. Toxicol. 1994, 29(3):257-290.
60. Mason A.Z., Jenkins K.D. Metal detoxification in aquatic organisms. Metal Speciation and Bioavailability in Aquatic Systems 1995, John Wiley & Sons Ltd., New York, NY. A. Tessier, D.R. Turner (Eds.).
61. Millington P., Walker K. Australian freashwater mussel Velesunio ambiguus (Philippi) as a biological monitor for zinc, iron and manganese. Marine Freshwater Res. 1983, 34(6):873-892.
62. Naito W., Kamo M., Tsushima K., Iwasaki Y. Exposure and risk assessment of zinc in Japanese surface waters. Sci. Total Environ. 2010, 408(20):4271-4284.
63. Nicholas W.L., Thomas M. Biological release and recycling of toxic metals from lake and river sediments. Austral. Water Resour. Council Technical Paper No. 1978, 33.
64. Pasteris A., Vecchi M., Reynoldson T.B., Bonomi G. Toxicity of copper-spiked sediments to Tubifex tubifex (Oligochaeta, Tubificidae): a comparison of the 28-day reproductive bioassay with a 6-month cohort experiment. Aquat. Toxicol. 2003, 65(3):253-265.
65. Péry A.R.R., Béthune A., Gahou J., Mons R., Garric J. Body residues: a key variable to analyze toxicity tests with Chironomus riparius exposed to copper-spiked sediments. Ecotoxicol. Environ. Saf. 2005, 61(2):160-167.
66. Phillips D.J.H. The chemistries and environmental fates of trace metals and organochlorines in aquatic ecosystems. Marine Pollut. Bull. 1995, 31(4-12):193-200.
67. Qiu J.W., Xie Z.C., Wang W.X. Effects of calcium on the uptake and elimination of cadmium and zinc in asiatic clams. Arch. Environ. Contamin. Toxicol. 2005, 48(2):278-287.
68. Rainbow P.S. Trace metal concentrations in aquatic invertebrates: why and so what?. Environ. Pollut. 2002, 120(3):497-507.
69. Regoli F. Chemical pollutants and the mechanisms of reactive oxygen species generation in aquatic organisms. Oxidative Stress in Aquatic Ecosystems 2011, 308-310. John Wiley & Sons, Ltd. Doris Abele, Jose Pablo Vazquez-Medina, Zenteno-Savin T. (Eds.).
70. Regoli F., Nigro M., Orlando E. Lysosomal and antioxidant responses to metals in the Antarctic scallop Adamussium colbecki. Aquatic Toxicol. 1998, 40(4):375-392.
71. Ridgway J., Shimmield G. Estuaries as repositories of historical contamination and their impact on shelf seas. Estuarine, Coastal Shelf Sci. 2002, 55(6):903-928.
72. Ringwood A., Hoguet J., Keppler C., Gielazyn M., Ward B., Rourk A. 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.
73. Rosabal M., Hare L., Campbell P.G.C. Subcellular metal partitioning in larvae of the insect Chaoborus collected along an environmental metal exposure gradient (Cd, Cu, Ni and Zn). Aquatic Toxicol. 2012, 120-121(0):67-78.
74. Simpson S.L., Angel B.M., Jolley D.F. Metal equilibration in laboratory-contaminated (spiked) sediments used for the development of whole-sediment toxicity tests. Chemosphere 2004, 54(5):597-609.
75. Sloane P., Norris R. Relationship of AUSRIVAS-based macroinvertebrate predictive model outputs to a metal pollution gradient. J. North Am. Benthol. Soc. 2003, 22(3):457-471.
76. Stewart A.R. Accumulation of Cd by a freshwater mussel (Pyganodon grandis) is reduced in the presence of Cu, Zn, Pb, and Ni. Can. J. Fish. Aquat. Sci. 1999, 56(3):467-478.
77. Taylor, A.M., Maher, W.A., 2010. Establishing metal exposure-dose-response relationships in marine organisms: illustrated with a case study of cadmium toxicity in Tellina deltoidalis. New Oceanography Research Developments: Marine Chemistry, Ocean Floor Analyses and Marine Phytoplankton. Nova Science, New York, pp. 1-57.
78. Taylor A.M., Maher W.A. Exposure-dose-response of Anadara trapezia to metal contaminated estuarine sediments. 1. Cadmium spiked sediments. Aquatic Toxicol. 2012, 109(0):234-242.
79. Taylor A.M., Maher W.A. Exposure-dose-response of Anadara trapezia to metal contaminated estuarine sediments. 2. Lead spiked sediments. Aquatic Toxicol. 2012, 116-117(0):79-89.
80. Taylor A.M., Maher W.A. Exposure-dose-response of Tellina deltoidalis to metal-contaminated estuarine sediments: 1. Cadmium spiked sediments. Comp. Biochem. Physiol. Part C: Toxicol. Pharmacol. 2013, 158(1):44-55.
81. Telford K., Maher W., Krikowa F., Foster S. Measurement of total antimony and antimony species in mine contaminated soils by ICPMS and HPLC-ICPMS. J. Environ. Monit. 2008, 10(1):136-140.
82. Tessier A., Campbell P., Auclair J., Bisson M. Relationships between the partitioning of trace metals in sediments and their accumulation in the tissues of the freshwater mollusc Elliptio complanata in a mining area. Can. J. Fish. Aquatic Sci. 1984, 41(10):1463-1472.
83. Tessier A., Couillard Y., Campbell P., Auclair J. Modeling Cd partitioning in oxic lake sediments and Cd concentrations in the freshwater bivalve Anodonta grandis. Limnol. Oceanogr. 1993, 1-17.
84. Tran A. Metal Concentrations in the Freshwater Bivalve, Hyridella drapeta, From Minimally Polluted Sites in the Middle Shoalhaven River, NSW, Wollongong, Australia 1998, 117. University of Wollongong, BEnvSc (Hons) Thesis.
85. USEPA, 2000. Methods for Measuring the Toxicity and Bioaccumulation of Sediment-associated Contaminants with Freshwater Invertebrates. Second edition book-99/064 2000 Duluth, MN, USA.
86. 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(2):57-149.
87. Vesk P.A., Byrne M. Metal levels in tissue granules of the freshwater bivalve Hyridella depressa (Unionida) for biomonitoring: the importance of cryopreparation. Sci. Total Environ. 1999, 225(3):219-229.
88. Voets J., Redeker E.S., Blust R., Bervoets L. Differences in metal sequestration between zebra mussels from clean and polluted field locations. Aquat. Toxicol. 2009, 93(1):53-60.
89. Wallace W.G., Lee B.-G., Luoma S.N. Subcellular compartmentalization of Cd and Zn in two bivalves I. Significance of metal-sensitive fractions (MSF) and biologically detoxified metal (BDM). Marine Ecol. Prog. Ser. 2003, 249:183-197.
90. Warren L.J. Contamination of sediments by lead, zinc and cadmium: a review. Environ. Pollut. Ser. B Chem. Phys. 1981, 2(6):401-436.
91. Weatherley A.H., Beevers J.R., Lake P.S. The ecology of a zinc polluted river. Australian Inland Waters and their Fauna: Eleven Studies 1967, ANU Press, Canberra.
92. Winston G.W., Moore M.N., Kirchin M.A., Soverchia C. Production of reactive oxygen species by Hemocytes from the marine mussel, Mytilus edulis: lysosomal localization and effect of xenobiotics. Comp. Biochem. Physiol. Part C: Pharmacol. Toxicol. Endocrinol. 1996, 113(2):221-229.