Hexachlorobenzene (HCB), listed on the Stockholm Convention on persistent organic pollutants and regulated as a hazardous priority pollutant by the Water Framework Directive (WFD), is ubiquitously distributed in the environment and assumed to mildly biomagnify in aquatic foodwebs. The proposal to include trophic magnification factors (TMFs) in the procedure for comparing contaminant levels in biota at different trophic levels (TLs) with WFD environmental quality standards requires adequate selection of TMFs. In the first step of our study, we compared two independently obtained datasets of pentachlorobenzene (PeCB) and HCB concentration ratios from passive sampling (PS) in water and in fish through routine monitoring programs in Norway to evaluate possible biomagnification. In this procedure, PeCB is used for benchmarking the bioconcentration in fish, and the observed HCB/PeCB ratios in fish are compared with ratios expected in the case of (i) HCB bioconcentration or (ii) biomagnification using published TMF values. Results demonstrate that it is not possible to confirm that HCB biomagnifies in fish species that would be used for WFD monitoring in Norway and challenges the proposed monitoring procedures for such compounds in Norwegian or European waters. In the second step, fish-water chemical activity ratios for HCB and PeCB as well as for polychlorinated biphenyls where biota and PS were conducted alongside were calculated and found to rarely exceed unity for cod (Gadus morhua), a fish species with a TL of approximately 4.

Norwegian Institute for Water Research Økernveien 94 Oslo NO 0579 Norway

RECETOX Faculty of Science Masaryk University Kotlarska 2 Brno 61137 Czech Republic

Zobrazit více v PubMed

Fliedner A.; Rüdel H.; Lohmann N.; Buchmeier G.; Koschorreck J. Biota monitoring under the Water Framework Directive: on tissue choice and fish species selection. Environ. Pollut. 2018, 235, 129–140. 10.1016/j.envpol.2017.12.052. PubMed DOI

Fliedner A.; Rüdel H.; Teubner D.; Buchmeier G.; Lowis J.; Heiss C.; Wellmitz J.; Koschorreck J. Biota monitoring and the Water Framework Directive-can normalization overcome shortcomings in sampling strategies?. Environ. Sci. Pollut. Res. 2016, 23, 21927–21939. 10.1007/s11356-016-7442-2. PubMed DOI PMC

Moermond C. T.; Verbruggen E. M. An evaluation of bioaccumulation data for hexachlorobenzene to derive water quality standards according to the EU-WFD methodology. Integr. Environ. Assess. Manage. 2013, 9, 87–97. 10.1002/ieam.1351. PubMed DOI

Carere M.; Dulio V.; Hanke G.; Polesello S. Guidance for sediment and biota monitoring under the Common Implementation Strategy for the Water Framework Directive. TrAC, Trends Anal. Chem. 2012, 36, 15–24. 10.1016/j.trac.2012.03.005. DOI

Deutsch K.; Leroy D.; Belpaire C.; Den Haan K.; Vrana B.; Clayton H.; Hanke G.; Ricci M.; Held A.; Gawlik B.. COMMON IMPLEMENTATION STRATEGY FOR THE WATER FRAMEWORK DIRECTIVE (2000/60/EC). Guidance Document No. 32 on Biota Monitoring (The Implementation of EQSBIOTA) under the Water Framework Directive; European Commission, 2013.

Kidd K. A.; Burkhard L. P.; Babut M.; Borgå K.; Muir D. C.; Perceval O.; Ruedel H.; Woodburn K.; Embry M. R. Practical advice for selecting or determining trophic magnification factors for application under the European Union Water Framework Directive. Integr. Environ. Assess. Manage. 2019, 15, 266–277. 10.1002/ieam.4102. PubMed DOI PMC

Booij K.; Robinson C. D.; Burgess R. M.; Mayer P.; Roberts C. A.; Ahrens L.; Allan I. J.; Brant J.; Jones L.; Kraus U. R.; Larsen M. M.; Lepom P.; Petersen J.; Pröfrock D.; Roose P.; Schäfer S.; Smedes F.; Tixier C.; Vorkamp K.; Whitehouse P. Passive sampling in regulatory chemical monitoring of nonpolar organic compounds in the aquatic environment. Environ. Sci. Technol. 2015, 50, 3–17. 10.1021/acs.est.5b04050. PubMed DOI

Gilbert D.; Witt G.; Smedes F.; Mayer P. Polymers as reference partitioning phase: polymer calibration for an analytically operational approach to quantify multimedia phase partitioning. Anal. Chem. 2016, 88, 5818–5826. 10.1021/acs.analchem.6b00393. PubMed DOI

Smedes F.; Sobotka J.; Rusina T. P.; Fialová P.; Carlsson P.; Kopp R.; Vrana B. Unraveling the Relationship between the Concentrations of Hydrophobic Organic Contaminants in Freshwater Fish of Different Trophic Levels and Water Using Passive Sampling. Environ. Sci. Technol. 2020, 54, 7942–7951. 10.1021/acs.est.9b07821. PubMed DOI

Mayer P.; Toräng L.; Glæsner N.; Jönsson J. Å. Silicone Membrane Equilibrator: Measuring Chemical Activity of Nonpolar Chemicals with Poly(dimethylsiloxane) Microtubes Immersed Directly in Tissue and Lipids. Anal. Chem. 2009, 81, 1536–1542. 10.1021/ac802261z. PubMed DOI

Allan I. J.; Bæk K.; Haugen T. O.; Hawley K. L.; Høgfeldt A. S.; Lillicrap A. D. In vivo passive sampling of nonpolar contaminants in brown trout (Salmo trutta). Environ. Sci. Technol. 2013, 47, 11660–11667. 10.1021/es401810r. PubMed DOI

Pintado-Herrera M. G.; Allan I. J.; González-Mazo E.; Lara-Martín P. A. Passive Samplers vs Sentinel Organisms: One-Year Monitoring of Priority and Emerging Contaminants in Coastal Waters. Environ. Sci. Technol. 2020, 54, 6693–6702. 10.1021/acs.est.0c00522. PubMed DOI

Jahnke A.; McLachlan M. S.; Mayer P. Equilibrium sampling: Partitioning of organochlorine compounds from lipids into polydimethylsiloxane. Chemosphere 2008, 73, 1575–1581. 10.1016/j.chemosphere.2008.09.017. PubMed DOI

Ruus A.; Allan I. J.; Bæk K.; Borgå K. Partitioning of persistent hydrophobic contaminants to different storage lipid classes. Chemosphere 2021, 263, 127890.10.1016/j.chemosphere.2020.127890. PubMed DOI

Smedes F.; Rusina T. P.; Beeltje H.; Mayer P. Partitioning of hydrophobic organic contaminants between polymer and lipids for two silicones and low density polyethylene. Chemosphere 2017, 186, 948–957. 10.1016/j.chemosphere.2017.08.044. PubMed DOI

Jahnke A.; MacLeod M.; Wickström H.; Mayer P. Equilibrium sampling to determine the thermodynamic potential for bioaccumulation of persistent organic pollutants from sediment. Environ. Sci. Technol. 2014, 48, 11352–11359. 10.1021/es503336w. PubMed DOI

Jahnke A.; Mayer P.; McLachlan M. S. Sensitive equilibrium sampling to study polychlorinated biphenyl disposition in Baltic Sea sediment. Environ. Sci. Technol. 2012, 46, 10114–10122. 10.1021/es302330v. PubMed DOI

Jahnke A.; Mayer P.; McLachlan M. S.; Wickström H.; Gilbert D.; MacLeod M. Silicone passive equilibrium samplers as ’chemometers’ in eels and sediments of a Swedish lake. Environmental Science: Processes & Impacts 2014, 16, 464–472. 10.1039/c3em00589e. PubMed DOI

Allan I. J.; Vrana B.; de Weert J.; Kringstad A.; Ruus A.; Christensen G.; Terentjev P.; Green N. W. Passive sampling and benchmarking to rank HOC levels in the aquatic environment. Sci. Rep. 2021, 11, 11231.10.1038/s41598-021-90457-3. PubMed DOI PMC

Allan I.; Jenssen M. T. S.; Braaten H. F. V.. Priority Substances and Emerging Contaminants in Selected Norwegian Rivers–The River Monitoring Programme 2017; NIVA-rapport, 2018.

Jartun M.; Økelsrud A.; Rundberget T.; Enge E. K.; Rostkowski P.; Warner N. A.; Harju M.; Johansen I.. Monitoring of Environmental Contaminants in Freshwater Ecosystems 2018–Occurrence and Biomagnification; NIVA-rapport, 2019.

Lyche J. L.; Nøstbakken O. J.; Berg V.. EU Water Framework-Directive Priority Contaminants in Norwegian Freshwater Fish; EU, 2019.

Green N.; Molvær J.; Kaste Ø.; Schrum C.; Yakushev E.; Sørensen K.; Allan I.; Høgåsen T.; Bjørkenes-Chr A.. Tilførselsprogrammet 2009. Overvåkning av tilførsel og miljøtilstand i Barentshavet og Lofotenområdet; NIVA report, 2010; p 5980.

Green N. W.; Heldal H. E.; Måge A.; Aas W.; Gäfvert T.; Schrum C.; Boitsov S.; Breivik K.; Iosjpe M.; Yakushev E.. Tilførselsprogrammet 2010. Overvåking Av Tilførsler Og Miljøtilstand I Nordsjøen; NIVA, 2011.

Green N. W.; Heldal H. E.; Måge A.; Aas W.; Gäfvert T.; Schrum C.; Boitsov S.; Breivik K.; Iosjpe M.; Yakushev E.. Tilførselsprogrammet 2011. Overvåking Av Tilførsler Og Miljøtilstand I Norskehavet; NIVA, 2012.

Green N.; Schøyen M.; Øxnevad S.; Ruus A.; Allan I.; Hjermann D.; Høgåsen T.; Beylich B.; Håvardstun J.; Lund E.. Contaminants in coastal waters of Norway-2014. Miljøgifter I kystområdene 2014. Norwegian Environment Agency Miljødirektoratet, Monitoring report M-433| 2015; Norwegian Institute for Water Research project, 2015; Vol. 15330; p 6917.

Green N.; Schøyen M.; Øxnevad S.; Ruus A.; Hjermann D.; Severinsen G.; Høgåsen T.; Beylich B.; Håvardstun J.; Lund E.. Contaminants in coastal waters of Norway-2016. Miljøgifter I kystområdene 2015. Norwegian Environment Agency Miljødirektoratet, Monitoring report M-656| 2017; Norwegian Institute for Water Research project, 2017; Vol. 17330; p 7200.

Green N. W.; Schøyen M.; Øxnevad S.; Ruus A.; Allan I.; Hjermann D. Ø.; Høgåsen T.; Beylich B.; Håvardstun J.; Lund E.. Contaminants in Coastal Waters of Norway 2014; NIVA, 2015.

Ruus A.; Bæk K.; Petersen K.; Allan I.; Beylich B.; Schlabach M.; Warner N.; Helberg M.. Miljøgifter I en urban fjord, 2014. Environmental Contaminants In an Urban Fjord 2014; NIVA, 2015; p 6884.

Schøyen M.; Allan I. J.; Ruus A.; Håvardstun J.; Hjermann D. Ø.; Beyer J. Comparison of caged and native blue mussels (Mytilus edulis spp.) for environmental monitoring of PAH, PCB and trace metals. Mar. Environ. Res. 2017, 130, 221–232. 10.1016/j.marenvres.2017.07.025. PubMed DOI

Green N. W.; Schøyen M.; Øxnevad S.; Ruus A.; Allan I.; Hjermann D.; Severinsen G.; Høgåsen T.; Beylich B.; Håvardstun J.. Contaminants in Coastal Waters of Norway 2015. Miljøgifter I Norske Kystområder 2015; NIVA-rapport, 2016.

Booij K.; Smedes F.; Crum S. Laboratory performance study for passive sampling of nonpolar chemicals in water. Environ. Toxicol. Chem. 2017, 36, 1156–1161. 10.1002/etc.3657. PubMed DOI

Kelly B. C.; Ikonomou M. G.; Blair J. D.; Morin A. E.; Gobas F. A. P. C. Food Web–Specific Biomagnification of Persistent Organic Pollutants. science 2007, 317, 236–239. 10.1126/science.1138275. PubMed DOI

Adolfsson-Erici M.; Åkerman G.; McLachlan M. S. Measuring bioconcentration factors in fish using exposure to multiple chemicals and internal benchmarking to correct for growth dilution. Environ. Toxicol. Chem. 2012, 31, 1853–1860. 10.1002/etc.1897. PubMed DOI

Smedes F. Silicone-water partition coefficients determined by cosolvent method for chlorinated pesticides, musks, organo phosphates, phthalates and more. Chemosphere 2018, 210, 662–671. 10.1016/j.chemosphere.2018.07.054. PubMed DOI

Inoue Y.; Hashizume N.; Yoshida T.; Murakami H.; Suzuki Y.; Koga Y.; Takeshige R.; Kikushima E.; Yakata N.; Otsuka M. Comparison of bioconcentration and biomagnification factors for poorly water-soluble chemicals using common carp (Cyprinus carpio L.). Arch. Environ. Contam. Toxicol. 2012, 63, 241–248. 10.1007/s00244-012-9761-8. PubMed DOI

Arnot J. A.; Gobas F. A. A review of bioconcentration factor (BCF) and bioaccumulation factor (BAF) assessments for organic chemicals in aquatic organisms. Environ. Rev. 2006, 14, 257–297. 10.1139/a06-005. DOI

Houde M.; Muir D. C. G.; Kidd K. A.; Guildford S.; Drouillard K.; Evans M. S.; Wang X.; Whittle D. M.; Haffner D.; Kling H. Influence of lake characteristics on the biomagnification of persistent organic pollutants in lake trout food webs. Environ. Toxicol. Chem. 2008, 27, 2169–2178. 10.1897/08-071.1. PubMed DOI

Ruus A.; Ugland K. I.; Skaare J. U. Influence of trophic position on organochlorine concentrations and compositional patterns in a marine food web. Environ. Toxicol. Chem. 2002, 21, 2356–2364. 10.1002/etc.5620211114. PubMed DOI

Burkhard L. P.; Borgå K.; Powell D. E.; Leonards P.; Muir D. C.; Parkerton T. F.; Woodburn K. B.. Improving the Quality and Scientific Understanding of Trophic Magnification Factors (TMFs); ACS Publications, 2013. PubMed

Økelsrud A.; Lydersen E.; Fjeld E. Biomagnification of mercury and selenium in two lakes in southern Norway. Sci. Total Environ. 2016, 566–567, 596–607. 10.1016/j.scitotenv.2016.05.109. PubMed DOI

Kim S.-K.; Kang C.-K. Temporal and spatial variations in hydrophobicity dependence of field-derived metrics to assess the biomagnification potential of hydrophobic organochlorine compounds. Sci. Total Environ. 2019, 690, 300–312. 10.1016/j.scitotenv.2019.06.221. PubMed DOI

Ruus A.; Daae I. A.; Hylland K. Accumulation of polychlorinated biphenyls from contaminated sediment by Atlantic cod (Gadus morhua): Direct accumulation from resuspended sediment and dietary accumulation via the polychaeteNereis virens. Environ. Toxicol. Chem. 2012, 31, 2472–2481. 10.1002/etc.1973. PubMed DOI

Kim J.; Gobas F. A. P. C.; Arnot J. A.; Powell D. E.; Seston R. M.; Woodburn K. B. Evaluating the roles of biotransformation, spatial concentration differences, organism home range, and field sampling design on trophic magnification factors. Sci. Total Environ. 2016, 551–552, 438–451. 10.1016/j.scitotenv.2016.02.013. PubMed DOI

Walters D. M.; Jardine T. D.; Cade B. S.; Kidd K. A.; Muir D. C. G.; Leipzig-Scott P. Trophic Magnification of Organic Chemicals: A Global Synthesis. Environ. Sci. Technol. 2016, 50, 4650–4658. 10.1021/acs.est.6b00201. PubMed DOI

Hallanger I. G.; Warner N. A.; Ruus A.; Evenset A.; Christensen G.; Herzke D.; Gabrielsen G. W.; Borgå K. Seasonality in contaminant accumulation in Arctic marine pelagic food webs using trophic magnification factor as a measure of bioaccumulation. Environ. Toxicol. Chem. 2011, 30, 1026–1035. 10.1002/etc.488. PubMed DOI

Kelly B. C.; Ikonomou M. G.; Blair J. D.; Gobas F. A. Bioaccumulation behaviour of polybrominated diphenyl ethers (PBDEs) in a Canadian Arctic marine food web. Sci. Total Environ. 2008, 401, 60–72. 10.1016/j.scitotenv.2008.03.045. PubMed DOI

Fliedner A.; Lohmann N.; Rüdel H.; Teubner D.; Wellmitz J.; Koschorreck J. Current levels and trends of selected EU Water Framework Directive priority substances in freshwater fish from the German environmental specimen bank. Environ. Pollut. 2016, 216, 866–876. 10.1016/j.envpol.2016.06.060. PubMed DOI

Miège C.; Mazzella N.; Allan I.; Dulio V.; Smedes F.; Tixier C.; Vermeirssen E.; Brant J.; O’Toole S.; Budzinski H.; Ghestem J.-P.; Staub P.-F.; Lardy-Fontan S.; Gonzalez J.-L.; Coquery M.; Vrana B. Position paper on passive sampling techniques for the monitoring of contaminants in the aquatic environment - Achievements to date and perspectives. Trends Environ. Anal. Chem. 2015, 8, 20–26. 10.1016/j.teac.2015.07.001. DOI

Lohmann R.; Muir D.; Zeng E. Y.; Bao L.-J.; Allan I. J.; Arinaitwe K.; Booij K.; Helm P.; Kaserzon S.; Mueller J. F.. Aquatic Global Passive Sampling (AQUA-GAPS) Revisited: First Steps toward a Network of Networks for Monitoring Organic Contaminants in the Aquatic Environment; ACS Publications, 2017. PubMed

Booij K.; Smedes F.; Allan I. J.. Guidelines for Determining Polymer-Water and Polymer-Polymer Partition Coefficients of Organic Compounds; ICES, 2017.

Verhagen R.; O’Malley E.; Smedes F.; Mueller J. F.; Kaserzon S. Calibration parameters for the passive sampling of organic UV filters by silicone; diffusion coefficients and silicone-water partition coefficients. Chemosphere 2019, 223, 731–737. 10.1016/j.chemosphere.2019.02.077. PubMed DOI

Pintado-Herrera M. G.; Lara-Martín P. A.; González-Mazo E.; Allan I. J. Determination of silicone rubber and low-density polyethylene diffusion and polymer/water partition coefficients for emerging contaminants. Environ. Toxicol. Chem. 2016, 35, 2162–2172. 10.1002/etc.3390. PubMed DOI

Huber S.; Warner N. A.; Nygård T.; Remberger M.; Harju M.; Uggerud H. T.; Kaj L.; Hanssen L. A broad cocktail of environmental pollutants found in eggs of three seabird species from remote colonies in Norway. Environ. Toxicol. Chem. 2015, 34, 1296–1308. 10.1002/etc.2956. PubMed DOI

Hoydal K. S.; Letcher R. J.; Blair D. A. D.; Dam M.; Lockyer C.; Jenssen B. M. Legacy and emerging organic pollutants in liver and plasma of long-finned pilot whales (Globicephala melas) from waters surrounding the Faroe Islands. Sci. Total Environ. 2015, 520, 270–285. 10.1016/j.scitotenv.2015.03.056. PubMed DOI

Allan I. J.; Bæk K.; Kringstad A.; Roald H. E.; Thomas K. V. Should silicone prostheses be considered for specimen banking? A pilot study into their use for human biomonitoring. Environ. Int. 2013, 59, 462–468. 10.1016/j.envint.2013.06.021. PubMed DOI