Chronic exposure to copper and zinc induces DNA damage in the polychaete Alitta virens and the implications for future toxicity of coastal sites

Watson, G. J.; Pini, J. M.; Richir, Jonathan

doi:10.1016/j.envpol.2018.09.091

Article (Scientific journals)

Chronic exposure to copper and zinc induces DNA damage in the polychaete Alitta virens and the implications for future toxicity of coastal sites

Watson, G. J.; Pini, J. M.; Richir, Jonathan

2018 • In Environmental Pollution, p. 1498-1508

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/236319

DOI
10.1016/j.envpol.2018.09.091

PubMed
30293035

Files (3)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Watson et al. (accepted mn) - Environmental Pollution.pdf

Author preprint (2.91 MB)

Download

Full Text Parts

Watson et al. (2018) - Environmental Pollution.pdf

Publisher postprint (1.07 MB)

Request a copy

mmc1.docx

Publisher postprint (43.84 kB)

Request a copy

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Antifouling; Bioavailability; Genotoxic; Nanoparticles; Nereis virens; Porewater

Abstract :

[en] Copper and zinc are metals that have been traditionally thought of as past contamination legacies. However, their industrial use is still extensive and current applications (e.g. nanoparticles and antifouling paints) have become additional marine environment delivery routes. Determining a pollutant's genotoxicity is an ecotoxicological priority, but in marine benthic systems putative substances responsible for sediment genotoxicity have rarely been identified. Studies that use sediment as the delivery matrix combined with exposures over life-history relevant timescales are also missing for metals. Here we assess copper and zinc's genotoxicity by exposing the ecologically important polychaete Alitta virens to sediment spiked with environmentally relevant concentrations for 9 months. Target bioavailable sediment and subsequent porewater concentrations reflect the global contamination range for coasts, whilst tissue concentrations, although elevated, were comparable with other polychaetes. Survival generally reduced as concentrations increased, but monthly analyses show that growth was not significantly different between treatments. The differential treatment mortality may have enabled the surviving worms in the high concentration treatments to capture more food thus removing any concentration treatment effects for biomass. Using the alkaline comet assay we confirm that both metals via the sediment are genotoxic at concentrations routinely found in coastal regions and this is supported by elevated DNA damage in worms from field sites. However, combined with the growth data it also highlights the tolerance of A. virens to DNA damage. Finally, using long term (decadal) monitoring data we show stable or increasing sediment concentrations of these metals for many areas. This will potentially mean coastal sediment is a significant mutagenic hazard to the benthic community for decades to come. An urgent reappraisal of the current input sources for these ‘old pollutants’ is, therefore, required. Chronic exposure of zinc and copper via sediment at environmentally relevant concentrations induces DNA damage in a marine polychaete. © 2018 Elsevier Ltd

Research center :

Institute of Marine Sciences, School of Biological Sciences, University of Portsmouth

Disciplines :

Environmental sciences & ecology

Author, co-author :

Watson, G. J.; Institute of Marine Sciences, School of Biological Sciences, University of Portsmouth, Ferry Road, Portsmouth, United Kingdom

Pini, J. M.; Institute of Marine Sciences, School of Biological Sciences, University of Portsmouth, Ferry Road, Portsmouth, United Kingdom

Richir, Jonathan ; Université de Liège - ULiège > Département d'astrophys., géophysique et océanographie (AGO) > Chemical Oceanography Unit (AGO)

Language :

English

Title :

Chronic exposure to copper and zinc induces DNA damage in the polychaete Alitta virens and the implications for future toxicity of coastal sites

Publication date :

2018

Journal title :

Environmental Pollution

ISSN :

0269-7491

eISSN :

1873-6424

Publisher :

Elsevier Ltd

Pages :

1498-1508

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

part-funded by the European RDF, INTER-REG IVA under part of the CHRONEXPO and 3C projects.

Available on ORBi :

since 04 June 2019

Statistics

Number of views

104 (4 by ULiège)

Number of downloads

90 (6 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

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. Estuar. Coast Shelf Sci. 72 (2007), 511–521.
Amiard, J.C., Amiard-Triquet, C., Berthet, B., Metayer, C., Comparative study of the patterns of bioaccumulation of essential (Cu, Zn) and non-essential (Cd, Pb) trace metals in various estuarine and coastal organisms. J. Exp. Mar. Biol. Ecol. 106 (1987), 73–89.
Anjos, V.A., da Silva-Júnior, F.M.R., Souza, M.M., Cell damage induced by copper: an explant model to study anemone cells. Toxicol. Vitro 28 (2014), 365–372.
Baker, T.J., Tyler, C.R., Galloway, T.S., Impacts of metal and metal oxide nanoparticles on marine organisms. Environ. Pollut. 186 (2014), 257–271.
Batley, G.E., Stahl, R.G., Babut, M.P., Bott, T.L., Clark, J.R., Field, L.J., Ho, K.T., Mount, D.R., Swartz, R.C., Tessier, A., Scientific underpinnings of sediment quality guidelines. Wenning, R., Batley, G., Ingersoll, C., Moore, D., (eds.) Use of Sediment Quality Guidelines and Related Tools for the Assessment of Contaminated Sediments, 2005, SETAC Press, Pensacola, USA, 39–120.
Berthet, B., Mouneyrac, C., Amiard, J.C., Amiard-Triquet, C., Berthelot, Y., Le Hen, A., Mastain, O., Rainbow, P.S., Smith, B.D., Accumulation and soluble binding of cadmium, copper and zinc in the polychaete Hediste diversicolor from coastal sites with different trace metal bioavailabilities. Arch. Environ. Toxicol. 45 (2003), 468–478.
Bonnard, M., Romeo, M., Amiard-Triquet, C., Effects of copper on the burrowing behavior of estuarine and coastal invertebrates, the polychaete Nereis diversicolor and the bivalve Scrobicularia plana. Hum. Ecol. Risk Assess. 15 (2009), 11–26.
Briant, N., Bancon-Montigny, C., Elbaz-Poulichet, F., Freydier, R., Delpoux, S., Cossa, D., Trace elements in the sediments of a large Mediterranean marina (port Camargue, France): levels and contamination history. Mar. Pollut. Bull. 73 (2013), 78–85.
Bryan, G.W., Hummerstone, L.G., Adaptation of the polychaete Nereis diversicolor to estuarine sediments containing high concentrations of zinc and cadmium. J. Mar. Biol. Ass. UK 53 (1973), 839–857.
Bryan, G.W., Gibbs, P.E., Zinc - major inorganic component of nereid polychaete jaws. J. Mar. Biol. Assoc. U. K. 59 (1979), 969–973.
Bryan, G.W., Langston, W.J., Bioavailability, accumulation and effects of heavy-metals in sediments with special reference to United Kingdom Estuaries - a review. Environ. Pollut. 76 (1992), 89–131.
Cade, B.S., Noon, B.R., A gentle introduction to quantile regression for ecologists. Front. Ecol. Environ. 1 (2003), 412–420.
Cadet, J., Douki, T., Ravanat, J.L., Oxidatively generated base damage to cellular DNA. Free Radical Biol. Med. 49 (2010), 9–21.
Caldwell, G.S., Lewis, C., Pickavance, G., Taylor, R.L., Bentley, M.G., Exposure to copper and cytotoxic polyunsaturated aldehyde induces reproductive failure in the marine polychaete Nereis virens (Sars). Aquat. Toxicol. 104 (2011), 126–134.
Caplat, C., Texier, H., Barillier, D., Lelievre, C., Heavy metal mobility in harbour contaminated sediments: the case of Port-en-Bessin. Mar. Pollut. Bull. 50 (2005), 504–511.
Casado-Martinez, M.C., Smith, B.D., Luoma, S., Rainbow, P.S., Metal toxicity in a sediment-dwelling polychaete: threshold body concentrations or overwhelming accumulation rates?. Environ. Pol. 158 (2010), 3071–3076.
Chapman, P.M., Wang, F.Y., Germano, J.D., Batley, G., Pore water testing and analysis: the good, the bad and the ugly. Mar. Pollut. Bull. 44 (2002), 359–366.
Chen, G., White, P.A., The mutagenic hazards of aquatic sediments: a review. Mutat. Res. 567 (2004), 151–225.
Clark, M., Thorne, M., King, M., Hipperson, H., Hoffman, J.I., Peck, L., Life in the intertidal: cellular responses, methylation and epigenetics. Funct. Ecol. 32 (2018), 1982–1994.
Cong, Y., Banta, G.T., Selck, H., Berhanu, D., Valsami-Jones, E., Forbes, V.E., Toxic effects and bioaccumulation of nano-, micron-and ionic-Ag in the polychaete. Nereis diversicolor. Aquat. Toxicol. 105 (2011), 403–411.
Cong, Y., Banta, G.T., Selck, H., Berhanu, D., Valsami-Jones, E., Forbes, V.E., Toxicity and bioaccumulation of sediment-associated silver nanoparticles in the estuarine polychaete, Nereis (Hediste) diversicolor. Aquat. Toxicol. 156 (2014), 106–115.
Cook, J.M., Gardner, M.J., Griffiths, A.H., Jessep, M.A., Ravenscroft, J.E., Yates, R., The comparability of sample digestion techniques for the determination of metals in sediments. Mar. Pollut. Bull. 34 (1997), 6 7–644.
Dean, H.K., The use of polychaetes (Annelida) as indicator species of marine pollution: a review. Rev. Biol. Trop. 158 (2008), 11–38.
Fernandes, H., Heavy metal distribution in sediments and ecological risk assessment: the role of diagenetic processes in reducing metal toxicity in bottom sediments. Environ. Pollut. 97 (1997), 317–325.
Fukunaga, A., Anderson, M.J., Webster-Brown, J.G., Assessing the nature of the combined effects of copper and zinc on estuarine infaunal communities. Environ. Pollut. 159 (2011), 116–124.
Gao, Y., Luo, Z., He, N., Wang, M.K., Metallic nanoparticle production and consumption in China between 2000 and 2010 and associative aquatic environmental risk assessment. J. Nanoparticle Res., 15, 2013, 1681.
Garcês, J., Costa, M.H., Trace metals in populations of Marphysa sanguinea (Montagu, 1813) from Sado estuary: effect of body size on accumulation. Sci. Mar. 73 (2009), 605–616.
Giangrande, A., Licciano, M., del Pasqua, M., Fanizzi, F.P., Migoni, D., Stabili, L., Heavy metals in five Sabellidae species (Annelida, Polychaeta): ecological implications. Environ. Sci. Pollut. Res. 24 (2017), 3759–3768.
Gomes, T., Araújo, O., Pereira, R., Almeida, A.C., Cravo, A., Bebianno, M.J., Genotoxicity of copper oxide and silver nanoparticles in the mussel Mytilus galloprovincialis. Mar. Environ. Res. 84 (2013), 51–59.
Hagger, J.A., Fisher, A.S., Hill, S.J., Depledge, M.H., Jha, A.N., Genotoxic, cytotoxic and ontogenetic effects of tri-n-butyltin on the marine worm, Platynereis dumerilii (Polychaeta: Nereidae). Aquat. Toxicol. 57 (2002), 243–255.
Harris, S.L., Levine, A.J., The p53 pathway: positive and negative feedback loops. Oncogene 24 (2005), 2899–2908.
Hartwig, A., Asmuss, M., Ehleben, I., Herzer, U., Kostelac, D., Pelzer, A., Schwerdtle, T., Burkle, A., Interference by toxic metal ions with DNA repair processes and cell cycle control: molecular mechanisms. Environ. Health Perspect. 110 (2002), 797–799.
Haynes, D., Toohey, D., Clarke, D., Marney, D., Temporal and spatial variation in concentrations of trace metals in coastal sediments from the Ninety Mile Beach, Victoria, Australia. Mar. Pollut. Bull. 30 (1995), 414–418.
Hose, J.E., Brown, E.D., Field applications of the piscine anaphase aberration test: lessons from the Exxon Valdez oil spill. Mutat. Res. 399 (1998), 167–178.
Hutchins, C.M., Teasdale, P.R., Lee, S.Y., Simpson, S.L., The effect of sediment type and pH-adjustment on the porewater chemistry of copper- and zinc-spiked sediments. Soil Sediment Contam. 18 (2009), 55–73.
Jha, A.N., Ecotoxicological applications and significance of the comet assay. Mutagenesis 23 (2008), 207–221.
Jha, A.N., Cheung, V.V., Foulkes, M.E., Hill, S.J., Depledge, M.H., Detection of genotoxins in the marine environment: adoption and evaluation of an integrated approach using the embryo-larval stages of the marine mussel. Mytilus edulis. Mutat. Res. 359 (2000), 141–150.
Johnson, A.C., Donnachie, R.L., Sumpter, J.P., Jürgens, M.D., Moeckel, C., Pereira, M.G., An alternative approach to risk rank chemicals on the threat they pose to the aquatic environment. Sci. Total Environ. 599 (2017), 1372–1381.
Kille, P., Andre, J., Anderson, C., Ang, H.N., Bruford, M.W., Bundy, J.G., Donnelly, R., Hodson, M.E., Juma, G., Lahive, E., Morgan, A.J., DNA sequence variation and methylation in an arsenic tolerant earthworm population. Soil Biol. Biochem. 57 (2013), 524–532.
King, C.K., Dowse, M.C., Simpson, S.L., Jolley, D.F., An assessment of five Australian polychaetes and bivalves for use in whole-sediment toxicity tests: toxicity and accumulation of copper and zinc from water and sediment. Arch. Environ. Contam. Toxicol. 47 (2004), 314–323.
Koenker, R., Bassett, G., Regression quantiles. Econometrica 46 (1978), 33–50.
Kristensen, E., Life-cycle, growth and production in estuarine populations of the polychaetes Nereis virens and N. diversicolor. Holarctic Ecol. 7 (1984), 249–256.
Kristensen, E., Kostka, J., Macrofaunal burrows and irrigation in marine sediment: microbiological and biogeochemical interactions. Interactions between Macro- and Microorganisms in Marine Sediments, 2005, AGU, Washington, DC, 125–157.
Langston, W.J., Pope, N.D., Davey, M., Langston, K.M., O'Hara, S.C.M., Gibbs, P.E., Pascoe, P.L., Recovery from TBT pollution in English Channel environments: a problem solved?. Mar. Pollut. Bull. 95 (2005), 551–564.
Larner, B.L., Seen, A.J., Palmer, A.S., Snape, I., A study of metal and metalloid contaminant availability in Antarctic marine sediments. Chemosphere 67 (2007), 1967–1974.
Lee, R.F., Steinert, S., Use of the single cell gel electrophoresis/comet assay for detecting DNA damage in aquatic (marine and freshwater) animals. Mutat. Res. 544 (2003), 43–64.
Lewis, C., Galloway, T., Genotoxic damage in polychaetes: a study of species and cell-type sensitivities. Mutat. Res. 654 (2008), 69–75.
Lewis, C., Watson, G.J., Expanding the ecotoxicological toolbox: the inclusion of polychaete reproductive endpoints. Mar. Environ. Res. 75 (2012), 10–22.
Li, J., Schiavo, S., Xiangli, D., Rametta, G., Miglietta, M.L., Oliviero, M., Changwen, W., Manzo, S., Early ecotoxic effects of ZnO nanoparticle chronic exposure in Mytilus galloprovincialis revealed by transcription of apoptosis and antioxidant-related genes. Ecotoxicology 27 (2018), 369–384.
Luoma, S.N., Rainbow, P.S., Metal Contamination in Aquatic Environments: Science and Lateral Management. 2008, Cambridge University Press, New York, 537.
Lushchak, V.I., Environmentally induced oxidative stress in aquatic animals. Aquat. Toxicol. 101 (2011), 13–30.
Mai, H., Cachot, J., Brune, J., Geffard, O., Belles, A., Budzinski, H., Morin, B., Embryotoxic and genotoxic effects of heavy metals and pesticides on early life stages of Pacific oyster (Crassostrea gigas). Mar. Pollut. Bull. 64 (2012), 2663–2670.
Martins, M., Costa, P.M., The comet assay in environmental risk assessment of marine pollutants: applications, assets and handicaps of surveying genotoxicity in non-model organisms. Mutagenesis 30 (2015), 89–106.
Matthiessen, P., Reed, J., Johnson, M., Sources and potential effects of copper and zinc concentrations in the estuarine waters of Essex and Suffolk, United Kingdom. Mar. Pollut. Bull. 38 (1999), 908–920.
McQuillan, J.S., Killie, P., Powell, K., Galloway, T., The regulation of copper stress response genes in the polychaete Nereis diversicolor during prolonged extreme copper contamination. Environ. Sci. Technol. 48 (2014), 13085–13092.
Miller, B.S., Pirie, D.J., Redshaw, C.J., An assessment of the contamination and toxicity of marine sediments in the Holy Loch. Scotland. Mar. Pollut. Bull. 40 (2000), 22–35.
Millero, F.J., Woolsley, R., Ditrolio, B., Waters, J., Effect of ocean acidification on the speciation of metals in seawater. Ocean 22 (2009), 72–85.
Miron, G., Desrosiers, G., Retière, C., Lambert, R., Dispersion and prospecting behaviour of the polychaete Nereis virens (Sars) as a function of density. J. Exp. Mar. Biol. Ecol. 145 (1991), 65–77.
Mouneyrac, C., Mastain, O., Amiard, J.C., Amiard-Triquet, C., Beaunier, P., Jeantet, A.Y., Smith, B.D., Rainbow, P.S., Trace-metal detoxification and tolerance of the estuarine worm Hediste diversicolor chronically exposed in their environment. Mar. Biol. 143 (2003), 731–744.
Naidu, A.S., Blanchard, A.L., Misra, D., Trefry, J.H., Dsaher, D.H., Kelley, J.J., Venkatesan, M.I., Historical changes in trace metals and hydrocarbons in nearshore sediments, Alaskan Beaufort Sea, prior and subsequent to petroleum-related industrial development: Part 1. trace metals. Mar. Pollut. Bull. 64 (2012), 2177–2189.
Nayar, S., Miller, D., Bryars, S., Cheshire, A.C., A simple, inexpensive and large volume porewater sampler for sandy and muddy substrates. Estuar. Coast Shelf Sci. 66 (2006), 298–302.
Pan, K., Wang, W.-X., Trace metal contamination in estuarine and coastal environments in China. Sci. Total Environ. 421–422 (2012), 3–16.
Pini, J.M., An Environmental and Ecotoxicological Assessment of the Impacts of Chronic Exposure of Copper and Zinc on the Polychaete Nereis (Alitta) Virens (M. Sars, 1835): Behavioural, Biochemical, Cellular and Genotoxic Responses. Ph.D. Dissertation, 2014, University of Portsmouth, UK.
Pini, J.M., Richir, J., Watson, G.J., Metal bioavailability and bioaccumulation in the polychaete Nereis (Alitta) virens (Sars): the effects of site-specific sediment characteristics. Mar. Pollut. Bull. 95 (2015), 565–575.
Poirier, L., Berthet, B., Amiard, J.C., Jeantet, A.Y., Amiard-Triquet, C., A suitable model for the biomonitoring of trace metal bioavailabilities in estuarine sediments: the annelid polychaete Nereis diversicolor. J. Mar. Biol. Assoc. U. K. 86 (2006), 71–82.
Pook, C., Lewis, C., Galloway, T., The metabolic and fitness costs associated with metal resistance in Nereis diversicolor. Mar. Pollut. Bull. 58 (2009), 1063–1071 2009.
Pueyo, M., Rauret, G., Lűck, D., Yli-Halla, M., Muntau, H., Quevauviller, Ph, López-Sánchez, J.F., Certification of the extractable contents of Cd, Cr, Cu, Ni, Pb and Zn in a freshwater sediment following a collaboratively tested and optimised three-step sequential extraction procedure. J. Environ. Monit. 3 (2001), 243–250.
Rainbow, P.S., Kriefman, S., Smith, B.D., Luoma, S.N., Have the bioavailabilities of trace metals to a suite of biomonitors changed over three decades in SW England estuaries historically affected by mining?. Sci. Total Environ. 409 (2011), 1589–1602.
Rainbow, P.S., Luoma, S.N., Metal toxicity, uptake and bioaccumulation in aquatic invertebrates – modelling zinc in crustaceans. Aquqt. Toxicol. 105 (2011), 455–465.
Rainbow, P.S., Smith, B.D., Luoma, S.N., Differences in trace metal bioaccumulation kinetics among populations of the polychaete Nereis diversicolor from metal-contaminated estuaries. Mar. Ecol. Prog. Ser. 376 (2009), 173–184.
Reichert, W.L., Myers, M.S., Peck-Miller, K., French, B., Anulacion, B.F., Collier, T.K., Stein, J.E., Varanasi, U., Molecular epizootiology of genotoxic events in marine fish: linking contaminant exposure, DNA damage, and tissue-level alterations. Mutat. Res. 411 (1998), 215–225.
Reish, D.J., Gerlinger, T.V., A review of the toxicological studies with polychaetous annelids. Bull. Mar. Sci. 60 (1997), 584–607.
Remaili, T.M., Simpson, S.L., Amato, E.D., Spadaro, D.A., Jarolimek, C.V., Jolley, D.F., The impact of sediment bioturbation by secondary organisms on metal bioavailability, bioaccumulation, and toxicity to target organisms in benthic bioassays: implications for sediment quality assessment. Environ. Pol. 208 (2016), 590–599.
Ruiz, P., Katsumiti, A., Nieto, J.A., Bori, J., Jimeno-Romero, A., Reip, P., Arostegui, I., Orbea, A., Cajaraville, M.P., Short-term effects on antioxidant enzymes and long-term genotoxic and carcinogenic potential of CuO nanoparticles compared to bulk CuO and ionic copper in mussels Mytilus galloprovincialis. Mar. Environ. Res. 111 (2015), 107–120.
Schwarz, J., Mitchelmore, C., Jones, R., O'Dea, A., Seymour, S., Exposure to copper induces oxidative and stress responses and DNA damage in the coral Montastraea franksi. Comp. Biochem. Physiol. C 157 (2013), 272–279.
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 54 (2004), 597–609.
Simpson, S.L., Batley, G.B., Chariton, a. A., Revision of the ANZECC/ARMCANZ Sediment Quality Guidelines. CSIRO Land and Water Science Report 08/07, 2013, CSIRO Land and Water, Australia, 121.
Simpson, S.L., Rochford, L., Birch, G.F., Geochemical influences on metal partitioning in contaminated estuarine sediments. Mar. Freshw. Res. 53 (2002), 9–17.
Song, M.O., Li, J., Freedman, J.H., Physiological and toxicological transcriptome changes in HepG2 cells exposed to coper. Physiol. Genom. 38 (2009), 386–401.
Speit, G., Kojima, H., Burlinson, B., Collins, A.R., Kasper, P., Plappert-Helbig, U., Uno, Y., Vasquez, M., Beevers, C., De Boeck, M., Escobar, P.A., Kitamoto, S., Pant, K., Pfuhler, S., Tanaka, J., Levy, D.D., Critical issues with the in vivo comet assay: a report of the comet assay working group in the 6th International Workshop on Genotoxicity testing (IWGT). Mutat. Res. 783 (2015), 6–12.
Stohs, S.J., Bagchi, D., Oxidative mechanisms in the toxicity of metal-ions. Free Radic. Biol. Med. 18 (1995), 321–336.
Sutherland, R.A., BCR R-701: a review of 10-years of sequential extraction analyses. Anal. Chim. Acta 680 (2010), 10–20.
Thit, A., Dybowska, A., Købler, C., Kennaway, G., Selck, H., Influence of copper oxide nanoparticle shape on bioaccumulation, cellular internalization and effects in the estuarine sediment-dwelling polychaete. Nereis diversicolor. Mar. Environ. Res. 111 (2015), 89–98.
U.S.EPA, Procedures for the Derivation of Equilibrium Partitioning Sediment Benchmarks (ESBs) for the Protection of Benthic Organisms: Metal Mixtures (Cadmium, Copper, Lead, Nickel, Silver and Zinc)’. EPA-600-R-02-011, 2005, Office of Research and Development, Washington, DC 20460.
Vandegehuchte, M.B., Janssen, C.R., Epigenetics in an ecotoxicological context. Mutat. Res. Genet. Toxicol. Environ. Mutagen 764 (2014), 36–45.
Walker, C.H., Hopkins, S.P., Sibley, R.M., Peakall, D.B., Principles of Ecotoxicology. 2006, CRC Press, Taylor and Francis, U.K., 2296.
Wang, W.X., Interactions of trace metals and different marine food chains. Mar. Ecol. Prog. Ser. 243 (2002), 295–309.
Watson, G.J., Leach, A., Fones, G., Effects of copper and other metals on fertilization, embryo development, larval survival and settlement of the polychaete Nereis (Neanthes) virens. Invertebr. Reprod. Dev. 52 (2008), 101–112 2008.
Watson, G.J., Murray, J.M., Schaefer, M., Bonner, A., Bait worms: a valuable and important fishery with implications for fisheries and conservation management. Fish Fish. 18 (2017), 374–388.
Watson, G.J., Pini, J.M., Leach, A., Fones, G., Long term incubation of adult Nereis virens (Annelida: polychaeta) in copper spiked sediment: the effects on adult mortality, gametogenesis, spawning and embryo development. Aquat. Toxicol. 128–129 (2013), 1–12.
Zimmerman, A.J., Weindorf, D.C., Heavy metal and trace metal analysis in soil by sequential extraction: a review of procedures. Int. J. Anal. Chem., 2010, 387803, 10.1155/2010/387803.