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Accumulation of Aqueous and Nanoparticulate Silver by the Marine Gastropod Littorina littorea

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Abstract

The accumulation of Ag by the marine herbivorous gastropod, Littorina littorea, has been studied in a series of exposures in which the metal was added in aqueous form and as nanoparticles, both in the presence and absence of contaminated algal food (Ulva lactuca). Significant accumulation occurred in the gill, kidney, stomach and visceral mass when the snail was exposed to aqueous Ag in the absence of food. Despite the consumption of U. lactuca that had been previously contaminated by Ag, no accumulation was observed from the dietary route. When added as nanoparticles, accumulation of Ag was only measured in the head and gill and only in the absence of contaminated food. These observations suggest that Ag is most bioavailable to L. littorina when in true solution and that Ag measured in external tissues of the snail following exposure to nanoparticles arises from some physical association that does not result in significant transfer of the metal to internal organs.

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References

  • Abbe, G. R., & Sanders, J. G. (1990). Pathways of silver uptake and accumulation by the American oyster (Crassostrea virginica) in Chesapeake Bay. Estuarine, Coastal and Shelf Science, 31, 113–123.

    Article  CAS  Google Scholar 

  • Asharani, P. V., Wu, Y. L., Gong, Z. Y. & Valiyaveettil, S. (2008). Toxicity of silver nanoparticles in zebra fish models. Nanotechnology, 19, article 255102

    Google Scholar 

  • Bilberg, K., Malte, H., Wang, T., & Baatrup, E. (2010). Silver nanoparticles and silver nitrate cause respiratory stress in Eurasian perch (Perca fluviatilis). Aquatic Toxicology, 96, 159–165.

    Article  CAS  Google Scholar 

  • Blackmore, G., & Wang, W.-X. (2004). The transfer of cadmium, mercury, methylmercury and zinc in an intertidal rocky shore food chain. Journal of Experimental Marine Biology and Ecology, 307, 91–110.

    Article  CAS  Google Scholar 

  • Blaser, S. A., Scheringer, M., Macleod, M., & Hungerbühler, K. (2008). Estimation of cumulative aquatic exposure and risk due to silver: contribution to nano-functionalized plastics and textiles. Science of the Total Environment, 390, 396–409.

    Article  CAS  Google Scholar 

  • Blinova, I., Ivask, A., Heinlaan, M., Mortimer, M., & Kahru, A. (2010). Ecotoxicity of nanoparticles of CuO and ZnO in natural water. Environmental Pollution, 158, 41–47.

    Article  CAS  Google Scholar 

  • Bradford, A., Handy, R. D., Readman, J. W., Atfield, A., & Mühling, M. (2009). Impact of silver nanoparticle contamination on the genetic diversity of natural bacterial assemblages in estuarine waters. Environmental Science and Technology, 43, 4530–4536.

    Article  CAS  Google Scholar 

  • Carlson, C., Hussain, S. M., Schrand, A. M., Braydich-Stolle, L. K., Hess, K. L., Jones, R. L., et al. (2008). Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. Journal of Physical Chemistry, 112, 13608–13619.

    Article  CAS  Google Scholar 

  • Chan, S. M., Wang, W.-X., & Ni, I. H. (2003). The uptake of Cd, Cr, and Zn by the macroalga Enteromorpha crinita and subsequent transfer to the marine herbivorous rabbitfish, Siganus canaliculatus. Archives of Environmental Contamination and Toxicology, 44, 298–306.

    Article  CAS  Google Scholar 

  • Connell, D. B., Sanders, J. G., Riedel, G. F., & Abbe, G. R. (1991). Pathways of silver uptake and trophic transfer in estuarine organisms. Environmental Science and Technology, 25, 921–924.

    Article  CAS  Google Scholar 

  • Crouteau, M. N., Dybowska, A. D., Luoma, S. N., & Valsami-Jones, E. (2011a). A novel approach reveals that zinc oxide nanoparticles are bioavailable and toxic after dietary exposure. Nanotoxicology, 5, 79–90.

    Article  Google Scholar 

  • Crouteau, M. N., Misra, S. K., Luoma, S. N., & Valsami-Jones, E. (2011b). Silver bioaccumulation dynamics in a freshwater invertebrate after aqueous and dietary exposures to nanosized and ionic Ag. Environmental Science and Technology, 45, 660–6607.

    Google Scholar 

  • Fabrega, J., Luoma, S. N., Tyler, C. R., Galloway, T. S., & Lead, J. R. (2011). Silver nanoparticles: behaviour and effects in the aquatic environment. Environment International, 37, 517–531.

    Article  CAS  Google Scholar 

  • Ferry, J. L., Craig, P., Hexel, C., Sisco, P., Frey, R., Pennington, P. L., et al. (2009). Transfer of gold nanoparticles from the water column to the estuarine food web. Nature Nanotechnology, 4, 441–444.

    Article  CAS  Google Scholar 

  • Fisher, N. S., & Wang, W. X. (1998). Trophic transfer of silver to marine herbivores: a review of recent studies. Environmental Toxicology and Chemistry, 17, 562–571.

    Article  CAS  Google Scholar 

  • Gottschalk, F., Sonderer, T., Scholz, R. W., & Nowack, B. (2009). Modeled environmental concentrations of engineered nanoparticles (TiO2, ZnO, Ag, CNT, fullerenes) for different regions. Environmental Science and Technology, 43, 8113–8118.

    Article  Google Scholar 

  • Hao, L. H., Wang, Z. Y., & Xing, B. S. (2009). Effect of sub-acute exposure to TiO2 nanoparticles on oxidative stress and histopathological changes in juvenile carp (Cyprinus carpio). Journal of Environmental Sciences, 21, 1459–1466.

    Article  CAS  Google Scholar 

  • Jin, X., Li, M., Wang, J., Marambio-Jones, C., Peng, F. B., Huang, X. F., et al. (2010). High-throughput screening of silver nanoparticle stability and bacterial inactivation in aquatic media: influence of specific ions. Environmental Science and Technology, 44, 7321–7328.

    Article  CAS  Google Scholar 

  • Kashiwada, S. (2006). Distribution of nanoparticles in the see-through medaka (Oryzias latipes). Environmental Health Perspectives, 114, 1697–1702.

    CAS  Google Scholar 

  • Köhler, A. R., Som, C., Helland, A., & Gottschalk, F. (2008). Studying the potential release of carbon nanotubes throughout the application life cycle. Journal of Cleaner Production, 16, 927–937.

    Article  Google Scholar 

  • Langston, W. J., Bebianno, M. J., & Burt, G. R. (1998). Metal handling strategies in molluscs. In W. J. Langston & M. J. Bebianno (Eds.), Metal metabolism in aquatic environments (pp. 219–283). London: Chapman and Hall.

    Google Scholar 

  • Lee, K. J., Nallathamby, P. D., Browning, L. M., Osgood, C. J., & Xu, X. H. N. (2007). In vivo imaging of transport and biocompatibility of single silver nanoparticles in early development of zebrafish embryos. ACS Nano, 1, 133–143.

    Article  CAS  Google Scholar 

  • Liu, J., & Hurt, R. H. (2010). Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environmental Science and Technology, 44, 2169–2175.

    Article  CAS  Google Scholar 

  • Luoma, S. N., Ho, Y. B., & Bryan, G. W. (1995). Fate, bioavailability and toxicity of silver in estuarine environments. Marine Pollution Bulletin, 31, 44–54.

    Article  CAS  Google Scholar 

  • MacKay, C. E., Johns, M., Salatas, J. H., Bessinger, B., & Perri, M. (2006). Stochastic probability modeling to predict the environmental stability of nanoparticles in aqueous suspension. Integrated Environmental Assessment and Management, 2, 293–298.

    Article  Google Scholar 

  • Miao, A. J., Schwehr, K. A., Xu, C., Zhang, S. J., Luo, Z., Quigg, A., et al. (2009). The algal toxicity of silver engineered nanoparticles and detoxification by exopolymeric substances. Environmental Pollution, 157, 3034–3041.

    Article  CAS  Google Scholar 

  • Moore, M. N. (2006). Do nanoparticles present ecotoxicological risks for the health of the aquatic environment? Environment International, 32, 967–976.

    Article  CAS  Google Scholar 

  • Mulholland, R., & Turner, A. (2011). Accumulation of platinum group elements by the marine gastropod Littorina littorea. Environmental Pollution, 159, 977–982.

    Article  CAS  Google Scholar 

  • Nowack, B., & Bucheli, T. D. (2007). Occurrence, behavior and effects of nanoparticles in the environment. Environmental Pollution, 150, 5–22.

    Article  CAS  Google Scholar 

  • Park, S. J., Park, Y. C., Lee, S. W., Jeong, M. S., Yu, K. N., Jung, H., et al. (2011). Comparing the toxic mechanism of synthesized zinc oxide nanomaterials by physicochemical characterization and reactive oxygen species properties. Toxicology Letters, 207, 197–203.

    Article  CAS  Google Scholar 

  • Reinfelder, J. R., & Chang, S. I. (1999). Speciation and microalgal bioavailability of inorganic silver. Environmental Science and Technology, 33, 1860–1863.

    Article  CAS  Google Scholar 

  • Ringwood, A. H., McCarthy, M., Bates, T. C., & Carroll, D. L. (2010). The effects of silver nanoparticles on oyster embryos. Marine Environmental Research, 69, S49–S51.

    Article  CAS  Google Scholar 

  • Tao, X., Fortner, J. D., Zhang, B., He, Y. H., Chen, Y. S., & Hughes, J. B. (2009). Effects of aqueous stable fullerene nanocrystals (nC(60)) on Daphnia magna: evaluation of sub-lethal reproductive responses and accumulation. Chemosphere, 77, 1482–1487.

    Article  CAS  Google Scholar 

  • Turner, A., Brice, D., & Brown, M. T. (2012). Interactions of silver nanoparticles with the marine macroalga, Ulva lactuca. Ecotoxicology, 21, 148–154.

    Article  CAS  Google Scholar 

  • Ward, J. E., & Kach, D. J. (2009). Marine aggregates facilitate ingestion of nanoparticles by suspension-feeding bivalves. Marine Environmental Research, 68, 137–142.

    Article  CAS  Google Scholar 

  • Wood, C. M., Grosell, M., McDonald, M. D., Playle, R. C., & Walsh, P. J. (2010). Effects of waterborne silver in a marine teleost, the gulf toadfish (Opsanus beta): effects of feeding and chronic exposure on bioaccumulation. Aquatic Toxicology, 99, 138–148.

    Article  CAS  Google Scholar 

  • Zhao, C. M., & Wang, W. X. (2010). Biokinetic uptake and efflux of silver nanoparticles in Daphnia magna. Environmental Science and Technology, 44, 7699–7704.

    Article  CAS  Google Scholar 

  • Zhu, X. S., Zhu, L., Lang, Y. P., & Chen, Y. S. (2008). Oxidative stress and growth inhibition in the freshwater fish Carassius autatus induced by chronic exposure to sublethal fullerene aggregates. Environmental Toxicology and Chemistry, 27, 1979–1985.

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Andrew Atfield, Angela Harrop and Andy Fisher (UoP) for technical advice and assistance throughout this study. HL was funded by an Erasmus Mundus Joint European Masters scholarship.

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Authors and Affiliations

  1. School of Geography, Earth and Environmental Sciences, University of Plymouth, Drake Circus, Plymouth, PL4 8AA, UK

    Haiying Li & Andrew Turner

  2. School of Marine Science and Engineering, University of Plymouth, Drake Circus, Plymouth, PL4 8AA, UK

    Murray T. Brown

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  1. Haiying Li
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  2. Andrew Turner
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  3. Murray T. Brown
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Correspondence to Andrew Turner.

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Li, H., Turner, A. & Brown, M.T. Accumulation of Aqueous and Nanoparticulate Silver by the Marine Gastropod Littorina littorea . Water Air Soil Pollut 224, 1354 (2013). https://doi.org/10.1007/s11270-012-1354-7

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  • DOI: https://doi.org/10.1007/s11270-012-1354-7

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