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Consideration of the bioavailability of metal/metalloid species in freshwaters: experiences regarding the implementation of biotic ligand model-based approaches in risk assessment frameworks

Abstract

After the scientific development of biotic ligand models (BLMs) in recent decades, these models are now considered suitable for implementation in regulatory risk assessment of metals in freshwater bodies. The BLM approach has been described in many peer-reviewed publications, and the original complex BLMs have been applied in prospective risk assessment reports for metals and metal compounds. BLMs are now also recommended as suitable concepts for the site-specific evaluation of monitoring data in the context of the European Water Framework Directive. However, the use is hampered by the data requirements for the original BLMs (about 10 water parameters). Recently, several user-friendly BLM-based bioavailability software tools for assessing the aquatic toxicity of relevant metals (mainly copper, nickel, and zinc) became available. These tools only need a basic set of commonly determined water parameters as input (i.e., pH, hardness, dissolved organic matter, and dissolved metal concentration). Such tools seem appropriate to foster the implementation of routine site-specific water quality assessments. This work aims to review the existing bioavailability-based regulatory approaches and the application of available BLM-based bioavailability tools for this purpose. Advantages and possible drawbacks of these tools (e.g., feasibility, boundaries of validity) are discussed, and recommendations for further implementation are given.

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References

  • Arora S, Rajwade JM, Paknikar KM (2012) Nanotoxicology and in vitro studies: the need of the hour. Toxicol Appl Pharmacol 258:151–165

    Article  CAS  Google Scholar 

  • Bergman HL, Dorward-King EJ (1997) Pellston Workshop on Reassessment of Metals Criteria for Aquatic Life Protection, reassessment of metals criteria for aquatic life protection: priorities for research and implementation: Proceedings of the Pellston Workshop on Reassessment of Metals Criteria for Aquatic Life Protection, 10–14 February 1996, Pensacola, Florida. Pensacola, SETAC Press

  • Bianchini A, Playle RC, Wood CM, Walsh PJ (2005) Mechanism of acute silver toxicity in marine invertebrates. Aquat Toxicol 72:67–82

    Article  CAS  Google Scholar 

  • Bio-met (2011) Bio-met Bioavailability Tool (version 1.4, 24.11.2011). Available at http://www.bio-met.net/ (after registration)

  • Blanchard J, Grosell M (2005) Effects of salinity on copper accumulation in the common killifish (Fundulus heteroclitus). Environ Toxicol Chem 24:1403–1413

    Article  CAS  Google Scholar 

  • Campbell PGC (1995) Interactions between trace metals and aquatic organisms: a critique of the free-ion activity model. In: Tessier A, Turner DR (eds) Metal speciation and bioavailability in aquatic systems. John Wiley and Sons, New York, pp 45–102

    Google Scholar 

  • Campbell PGC, Fortin C (2013) Biotic ligand model. In: Férard J-F, Blaise C (eds) Encyclopedia of Aquatic Ecotoxicology, Springer. ISBN 978-94-007-5040-1, 1195p

  • Campbell PGC, Lewis AG, Chapman PM, Crowder AA, Fletcher WK, Imber B, Luoma SN, Stokes PM, Winfrey M (1988) Biologically available metals in sediments. NRCC publication no. 27694. National Research Council Canada (NRCC), Ottawa, Canada

  • Casares MV, de Cabo LI, Seoane RS, Natale OE, Castro Ríos M, Weigandt C, de Iorio AF (2012) Measured copper toxicity to Cnesterodon decemmaculatus (Pisces: Poeciliidae) and predicted by biotic ligand model in Pilcomayo river water: a step for a cross-fish-species extrapolation. J Toxicol 2012:849315

    Google Scholar 

  • Chappaz A, Curtis PJ (2013) Integrating empirically dissolved organic matter quality for WHAM VI using the DOM optical properties: a case study of Cu-Al-DOM interactions. Environ Sci Technol 47:2001–2007

    Article  CAS  Google Scholar 

  • Choi O, Clevenger TE, Deng B, Surampalli RY, Ross L Jr, Hu Z (2009) Role of sulfide and ligand strength in controlling nanosilver toxicity. Water Res 43:1879–1886

    Article  CAS  Google Scholar 

  • Copper RAR (2008) Voluntary risk assessment reports—copper and copper compounds. European Copper Institute, Brussels, Belgium. http://echa.europa.eu/web/guest/copper-voluntary-risk-assessment-reports

  • Crémazy A, Campbell PG, Fortin C (2013) The biotic ligand model can successfully predict the uptake of a trivalent ion by a unicellular alga below pH 6.50 but not above: possible role of hydroxo-species. Environ Sci Technol 47:2408–2415

    Article  Google Scholar 

  • David M, Perceval O, Batty J, Rodriguez Romero J, Niebeek G, Delbeke K, Van Assche F, Merrington G, Schlekat G (2011) Workshop on metal bioavailability under the water framework directive: policy, science and implementation of regulatory tools. Workshop Report, June 2011

  • de Polo A, Scrimshaw MD (2012) Challenges for the development of a biotic ligand model predicting copper toxicity in estuaries and seas. Environ Toxicol Chem 31:230–238

    Article  Google Scholar 

  • De Schamphelaere KA, Janssen CR (2004) Development and field validation of a biotic ligand model predicting chronic copper toxicity to Daphnia magna. Environ Toxicol Chem 23:1365–1375

    Article  Google Scholar 

  • De Schamphelaere KA, Stauber JL, Wilde KL, Markich SJ, Brown PL, Franklin NM, Creighton NM, Janssen CR (2005) Toward a biotic ligand model for freshwater green algae: surface-bound and internal copper are better predictors of toxicity than free Cu2+-ion activity when pH is varied. Environ Sci Technol 39:2067–2072

    Article  Google Scholar 

  • Di Toro DM, Allen HE, Bergman HL, Meyer JS, Paquin PR, Santore RC (2001) Biotic ligand model of the acute toxicity of metals. 1. Technical basis. Environ Toxicol Chem 20:2383–2396

    Article  Google Scholar 

  • EC (2000) Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for community action in the field of water policy. Off J Eur Union L327, 22 December 2000: 72 pp. http://eur-lex.europa.eu/resource.html?uri=cellar:5c835afb-2ec6-4577-bdf8-756d3d694eeb.0004.02/DOC_1&format=PDF

  • EC (2006) Regulation (EC) No 1907/2006 of the European Parliament and of the Council of 18 December 2006 concerning the registration, evaluation, authorisation and restriction of chemicals (REACH), establishing a European Chemicals Agency. Off J Eur Union L396, 30.12.2006, 849 pp. http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=CONSLEG:2006R1907:LATEST:EN:PDF

  • EC (2008) Directive 2008/105/EC of the European Parliament and of the Council of 16 December 2008 on environmental quality standards in the field of water policy, amending and subsequently repealing Council Directives 82/176/EEC, 83/513/EEC, 84/156/EEC, 84/491/EEC, 86/280/EEC and amending Directive 2000/60/EC of the European Parliament and of the Council. Official Journal of the European Union, L 348/84, 24.12.2008. http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2008:348:0084:0097:EN:PDF

  • EC (2011) Technical guidance for deriving environmental quality standards. Common implementation strategy for the Water Framework Directive (2000/60/EC). Guidance document no. 27. Prepared by EU, Member States and stakeholders. Technical Report - 2011–055. https://circabc.europa.eu/sd/d/0cc3581b-5f65-4b6f-91c6-433a1e947838/TGD-EQS%20CIS-WFD%2027%20EC%202011.pdf

  • ECHA (2008) Guidance on information requirements and chemical safety assessment Appendix R.7.13-2: environmental risk assessment for metals and metal compounds. European Chemicals Agency (ECHA). Helsinki, Finland. http://www.echa.europa.eu/documents/10162/13632/information_requirements_r7_13_2_en.pdf

  • Environment Agency (2009). Using biotic ligand models to help implement environmental quality standards for metals under the Water Framework Directive. Science Report SC080021/SR7b. Environment Agency, Bristol, UK. http://www.wfduk.org/sites/default/files/Media/Environmental standards/biotic ligand models implement EQS.pdf

  • Erickson RJ (2013) The biotic ligand model approach for addressing effects of exposure water chemistry on aquatic toxicity of metals: genesis and challenges. Environ Toxicol Chem 32:1212–1214

    Article  CAS  Google Scholar 

  • Erickson RJ, Benoit DA, Mattson VR, Leonard EN, Nelson HP Jr (1996) The effects of water chemistry on the toxicity of copper to fathead minnows. Environ Toxicol Chem 15:181–193

    Article  CAS  Google Scholar 

  • EU (2013) Directive 2013/39/EU of the European Parliament and of the Council of 12 August 2013 amending Directives 2000/60/EC and 2008/105/EC as regards priority substances in the field of water policy. OJ L226, 24.8.2013, 17 pp. http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2013:226:0001:0017:EN:PDF

  • Fabrega J, Luoma SN, Tyler CR, Galloway TS, Lead JR (2011) Silver nanoparticles: behaviour and effects in the aquatic environment. Environ Int 37:517–531

    Article  CAS  Google Scholar 

  • Hatano A, Shoji R (2010) A new model for predicting time course toxicity of heavy metals based on biotic ligand model (BLM). Comp Biochem Physiol C Toxicol Pharmacol 151:25–32

    Article  Google Scholar 

  • Hayashi TI (2013) Applying biotic ligand models and Bayesian techniques: ecological risk assessment of copper and nickel in Tokyo rivers. Integr Environ Assess Manag 9:63–69

    Article  CAS  Google Scholar 

  • Hommen U, Rüdel H (2012) Sensitivity analysis of existing concepts for application of biotic ligand models (BLM) for the derivation and application of environmental quality standards for metals and evaluation of the approaches with appropriate monitoring data sets from German waters. FKZ 363 01 352. Final report for Umweltbundesamt, Dessau-Rosslau, Germany, by Fraunhofer Institute for Molecular Biology and Applied Ecology (IME), Schmallenberg, Germany

  • HydroQual (2007) The biotic ligand model windows interface, version 2.2.1: user’s guide and reference manual. HydroQual, Inc., Mahwah, NJ, February 2007. www.hydroqual.com/wr_blm.html

  • Jahn TP, Bienert GP (2010) MIPs and their role in the exchange of metalloids. Springer, New York

    Book  Google Scholar 

  • Janssen CR, De Schamphelaere K, Heijerick D, Muyssen B, Lock K, Bossuyt B, Vangheluwe M, Van Sprang P (2000) Uncertainties in the environmental risk assessment of metals. Human Ecol Risk Assess 6:1003–1018

    Article  CAS  Google Scholar 

  • Kalis EJJ, Weng L, Temminghoff EJM, Van Riemsdijk WH (2006) Measuring free metal ion concentrations in situ in natural waters using the Donnan Membrane Technique. Environ Sci Technol 40:955–961

    Article  CAS  Google Scholar 

  • Kennedy AJ, Chappell MA, Bednar AJ, Ryan AC, Laird JG, Stanley JK, Steevens JA (2012) Impact of organic carbon on the stability and toxicity of fresh and stored silver nanoparticles. Environ Sci Technol 46:10772–10780

    Article  CAS  Google Scholar 

  • Khan FR, Keller WB, Yan ND, Welsh PG, Wood CM, McGeer JC (2012) Application of biotic ligand and toxic unit modeling approaches to predict improvements in zooplankton species richness in smelter-damaged lakes near Sudbury, Ontario. Environ Sci Technol 46:1641–1649

    Article  CAS  Google Scholar 

  • Kinraide TB (2003) The controlling influence of cell-surface electrical potential on the uptake and toxicity of selenate (SeO42−). Physiol Plant 117:64–71

    Article  CAS  Google Scholar 

  • Kinraide TB (2006) Plasma membrane surface potential (psiPM) as a determinant of ion bioavailability: a critical analysis of new and published toxicological studies and a simplified method for the computation of plant psiPM. Environ Toxicol Chem 25:3188–3198

    Article  CAS  Google Scholar 

  • Leaes Pinho GL, Bianchini A (2010) Acute copper toxicity in the euryhaline copepod Acartia tonsa: implications for the development of an estuarine and marine biotic ligand model. Environ Toxicol Chem 29:1834–1840

    CAS  Google Scholar 

  • Levy JL, Stauber JL, Adams MS, Maher WA, Kirby JK, Jolley DF (2005) Toxicity, biotransformation, and mode of action of arsenic in two freshwater microalgae (Chlorella sp. and Monoraphidium arcuatum). Environ Toxicol Chem 24:2630–2639

    Article  CAS  Google Scholar 

  • Liu G, Fernandez A, Cai Y (2011) Complexation of arsenite with humic acid in the presence of ferric iron. Environ Sci Technol 45:3210–3216

    Article  CAS  Google Scholar 

  • Lombi E, Holm PE (2010) Metalloids, soil chemistry and the environment. In: Jahn TP, Bienert GP (eds) MIPs and their role in the exchange of metalloids. Springer, New York

    Google Scholar 

  • Luoma SN, Rainbow PS (2005) Why is metal bioaccumulation so variable? Biodynamics as a unifying concept. Environ Sci Technol 39:1921–1931

    Article  CAS  Google Scholar 

  • Morel FMM (1983) Principles of aquatic chemistry. Wiley, New York

    Google Scholar 

  • Mytych J, Wnuk M (2013) Nanoparticle technology as a double-edged sword: cytotoxic, genotoxic and epigenetic effects on living cells. J Biomater Nanobiotechnol 4:53–63

    Article  Google Scholar 

  • Natale OE, Leis MV (2008) Biotic ligand model estimation of copper bioavailability and toxicity in the yacyreta reservoir on the Parana river. Lakes Reservoirs Res Manage 13:231–244

    Article  CAS  Google Scholar 

  • Newman MC, Jagoe CH (1994) Ligands and the bioavailability of metals in aquatic environments. In: Hamelink JL, Landrum PF, Bergman HL, Benson WH (eds) Bioavailability: physical, chemical, and biological interactions. Lewis Publications, Boca Raton, pp 39–62

    Google Scholar 

  • Nickel EU RAR (2008) European Union Risk Assessment Report—nickel and nickel compounds. Office for Official Publications of the European Communities, Luxembourg. http://echa.europa.eu/documents/10162/cefda8bc-2952-4c11-885f-342aacf769b3

  • Nielsen FH (1991) Nutritional requirements for boron, silicon, vanadium, nickel, and arsenic: current knowledge and speculation. FASEB 5:2661–2667

    CAS  Google Scholar 

  • Niyogi S, Wood CM (2004) Biotic ligand model, a flexible tool for developing site-specific water quality guidelines for metals. Environ Sci Technol 38:6177–6192

    Article  CAS  Google Scholar 

  • Paganini CL, Bianchini A (2009) Copper accumulation and toxicity in isolated cells from gills and hepatopancreas of the blue crab (Callinectes sapidus). Environ Toxicol Chem 28:1200–1205

    Article  CAS  Google Scholar 

  • Pagenkopf GK (1983) Gill surface interaction model for trace-metal toxicity to fishes: role of complexation, pH and water hardness. Environ Sci Technol 17:342–347

    Article  CAS  Google Scholar 

  • Paquin PR, Gorsuch JW, Apte S, Batley GE, Bowles KC, Campbell PG, Delos CG, Di Toro DM, Dwyer RL, Galvez F, Gensemer RW, Goss GG, Hostrand C, Janssen CR, McGeer JC, Naddy RB, Playle RC, Santore RC, Schneider U, Stubblefield WA, Wood CM, Wu KB (2002) The biotic ligand model: a historical overview. Comp Biochem Physiol C Toxicol Pharmacol 133:3–35

    Article  Google Scholar 

  • Peijnenburg W, Sneller E, Sijm D, Lijzen J, Traas T, Verbruggen E (2002) Implementation of bioavailability in standard setting and risk assessment? J Soils Sediments 2:169–173

    Article  Google Scholar 

  • Peters A, Merrington G, de Schamphelaere K, Delbeke K (2011) Regulatory consideration of bioavailability for metals: simplification of input parameters for the chronic copper biotic ligand model. Integr Environ Assess Manag 7:437–444

    Article  CAS  Google Scholar 

  • Plette ACC, Nederlof MM, Temminghoff EJM, Van Riemsdijk WH (1999) Bioavailability of heavy metals in terrestrial and aquatic systems: a quantitative approach. Environ Toxicol Chem 18:1882–1890

    Article  CAS  Google Scholar 

  • PNEC.pro (2013) PNEC.pro Bioavailability Tool (version 5, June 2013). Available at http://www.pnec-pro.com

  • Rainbow PS (2007) Trace metal bioaccumulation: models, metabolic availability and toxicity. Environ Int 33:576–582

    Article  CAS  Google Scholar 

  • RD 60 (2011) Royal Decree 60/2011, of 21 January, on the norms of environmental quality in the field of the politics of waters. Ministry of Environment and Half Rural and Marino, Madrid, Spain. BOE 19 of 22/01/2011

  • Reidy B, Haase A, Lunch A, Dawson KA, Lynch I (2013) Mechanisms of silver nanoparticle release, transformation and toxicity: a critical review of current knowledge and recommendations for future studies and applications. Materials 6:2295–2350

    Article  CAS  Google Scholar 

  • SCHER (2010) Opinion on the Chemicals and the Water Framework Directive: Technical guidance for deriving environmental quality standards; Scientific Committee on Health and Environmental Risks (SCHER). October 2010. http://ec.europa.eu/health/scientific_committees/environmental_risks/docs/scher_o_127.pdf

  • Schlekat CE, Van Genderen E, De Schamphelaere KA, Antunes PM, Rogevich EC, Stubblefield WA (2010) Cross-species extrapolation of chronic nickel biotic ligand models. Sci Total Environ 408:6148–6157

    Article  CAS  Google Scholar 

  • Sigg I (2014) Metals as water quality parameters—role of speciation and bioavailability. Reference Module in Earth Systems and Environmental Sciences, Comprehensive Water Quality and Purification, Volume 4: Water Quality and Sustainability, pp. 315–328 www.sciencedirect.com/science/article/pii/B9780123821829000906

  • Slaveykova VI, Wilkinson KJ (2005) Predicting the bioavailability of metals and metal complexes: critical review of the biotic ligand model. Environ Chem 2:9–24

    Article  CAS  Google Scholar 

  • Sposito G (2008) The chemistry of soils, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Sun H (2011) Biological chemistry of arsenic, antimony and bismuth. Wiley, West Sussex

    Google Scholar 

  • Tessier A, Turner DR (eds) (1995) Metal speciation and bioavailability in aquatic systems. Wiley, New York

    Google Scholar 

  • Tipping E (1994) WHAMC-A chemical equilibrium model and computer code for waters, sediments, and soils incorporating a discrete site/electrostatic model of ion-binding by humic substances. Comp Geosci 20, 973–1023

  • US EPA (1985a) Guidelines for deriving numerical national water quality criteria for the protection of aquatic organisms and their uses. National Technical Information Service PB85-227049

  • US EPA (1985b) Ambient Water Quality Criteria for Copper—1984. National Technical Information Service PB85-227023

  • US EPA (2000) An Science Advisory Board Report: review of an integrated approach to metals assessment in surface waters and sediments. United States Environmental Protection Agency (US EPA), Office of Research and Development

  • US EPA (2003) Notice of availability of draft aquatic life criteria document for copper and request for scientific views. United States Environmental Protection Agency (US EPA). 68 FR 75552

  • US EPA (2007a) Aquatic life ambient freshwater quality criteria—copper. EPA-822-R-07-001. United States Environmental Protection Agency (US EPA), Office of Science and Technology. Washington, D.C., USA, February 2007 http://water.epa.gov/scitech/swguidance/standards/criteria/aqlife/pollutants/copper/upload/2009_04_27_criteria_copper_2007_criteria-full.pdf

  • US EPA (2007b) Aquatic Life Criteria—copper 2007 update. 16-Oct-2012. http://water.epa.gov/scitech/swguidance/standards/criteria/aqlife/copper/

  • US EPA (2007c) Training materials on copper BLM: data requirements. United States Environmental Protection Agency (US EPA), Office of Science and Technology, Standards and Health Protection Division. Washington, D.C., USA http://water.epa.gov/scitech/swguidance/standards/criteria/aqlife/copper/upload/2007_04_11_criteria_copper_faq_data-requirements.pdf

  • Van Sprang PA, Verdonck FA, Van Assche F, Regoli L, De Schamphelaere KA (2009) Environmental risk assessment of zinc in European freshwaters: a critical appraisal. Sci Total Environ 407:5373–5391

    Article  Google Scholar 

  • Veltman K, Huijbregts MA, Hendriks AJ (2010) Integration of biotic ligand models (BLM) and bioaccumulation kinetics into a mechanistic framework for metal uptake in aquatic organisms. Environ Sci Technol 44:5022–5028

    Article  CAS  Google Scholar 

  • Verschoor AJ, Vink JPM, de Snoo GR, Vijver MG (2011) Spatial and temporal variation of watertype-specific no-effect concentrations and risks of Cu, Ni, and Zn. Environ Sci Technol 45:6049–6056

    Article  CAS  Google Scholar 

  • Verschoor AJ, Vink JPM, Vijver MG (2012) Simplification of biotic ligand models of Cu, Ni, and Zn by 1-, 2-, and 3-parameter transfer functions. Integr Environ Assess Manag 8:738–748

    Article  CAS  Google Scholar 

  • Vijver MG, De Koning A, Peijnenburg WJ (2008) Uncertainty of water type-specific hazardous copper concentrations derived with biotic ligand models. Environ Toxicol Chem 27:2311–2319

    Article  CAS  Google Scholar 

  • Villavicencio G, Urrestarazu P, Arbildua J, Rodriguez PH (2011) Application of an acute biotic ligand model to predict chronic copper toxicity to Daphnia magna in natural waters of Chile and reconstituted synthetic waters. Environ Toxicol Chem 30:2319–2325

    Article  CAS  Google Scholar 

  • Vink JPM (2002) Measurement of heavy metal speciation over redox gradients in natural water-sediment interfaces and implications for uptake by benthic organisms. Environ Sci Technol 23:5130–5138

  • Vink JPM (2009) The origin of speciation. Environ Poll 157:519–527

    Article  CAS  Google Scholar 

  • Vink JPM, Verschoor A (2010) Biotic ligand models: availability, performance and applicability for water quality assessment. Deltares report 1203842, Utrecht, The Netherlands

  • Vukosav P, Mlakar M, Cukrov N, Kwokal Z, Pižeta I, Pavlus N, Spoljarić I, Vurnek M, Brozinčević A, Omanović D (2014) Heavy metal contents in water, sediment and fish in a karst aquatic ecosystem of the Plitvice Lakes National Park (Croatia). Environ Sci Pollut Res 21:3826–3839

    Article  CAS  Google Scholar 

  • Wang P, Zhou D, Kinraide TB, Luo X, Li L, Li D, Zhang H (2008) Cell membrane surface potential (psi0) plays a dominant role in the phytotoxicity of copper and arsenate. Plant Physiol 148:2134–2143

    Article  CAS  Google Scholar 

  • Wang P, Kinraide TB, Zhou D, Kopittke PM, Peijnenburg WJ (2011) Plasma membrane surface potential: dual effects upon ion uptake and toxicity. Plant Physiol 155:808–820

    Article  CAS  Google Scholar 

  • WFD-UKTAG (2012) Development and use of the copper bioavailability assessment tool (draft). Report SC080021/8a-a. Water Framework Directive - United Kingdom Technical Advisory Group (WFD-UKTAG), SNIFFER, Edinburgh, Scotland, UK. http://www.wfduk.org/sites/default/files/Media/Copper M-BAT report - UKTAG.pdf

  • Worms IA, Wilkinson KJ (2007) Ni uptake by a green alga. 2. Validation of equilibrium models for competition effects. Environ Sci Technol 41:4264–4270

    Article  CAS  Google Scholar 

  • Xiu ZM, Ma J, Alvarez PJ (2011) Differential effect of common ligands and molecular oxygen on antimicrobial activity of silver nanoparticles versus silver ions. Environ Sci Technol 45:9003–9008

    Article  CAS  Google Scholar 

  • Zhou DM, Wang P (2011) A novel approach for predicting the uptake and toxicity of metallic and metalloid ions. Plant Signal Behav 6:461–465

    Article  CAS  Google Scholar 

  • Zhou B, Nichols J, Playle RC, Wood CM (2005) An in vitro biotic ligand model (BLM) for silver binding to cultured gill epithelia of freshwater rainbow trout (Oncorhynchus mykiss). Toxicol Appl Pharmacol 202:25–37

    Article  CAS  Google Scholar 

  • Zinc EU RAR (2010) European Union risk assessment report zinc metal. Office for Official Publications of the European Communities, Luxembourg. http://publications.jrc.ec.europa.eu/repository/handle/JRC61245

  • Zitko V, Carson WG (1976) A mechanism of the effects of water hardness on the lethality of heavy metals to fish. Chemosphere 5:299–303

    Article  CAS  Google Scholar 

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Rüdel, H., Díaz Muñiz, C., Garelick, H. et al. Consideration of the bioavailability of metal/metalloid species in freshwaters: experiences regarding the implementation of biotic ligand model-based approaches in risk assessment frameworks. Environ Sci Pollut Res 22, 7405–7421 (2015). https://doi.org/10.1007/s11356-015-4257-5

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Keywords

  • Bioavailability
  • Biotic ligand model
  • Metals
  • Quality standards
  • Surface water monitoring
  • Copper
  • Nickel
  • Zinc