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Mercury uptake by halophytes in response to a long-term contamination in coastal wetland salt marshes (northern Adriatic Sea)

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Abstract

Mercury (Hg) distribution in saltmarsh sediments and in three selected halophytes (Limonium narbonense, Sarcocornia fruticosa and Atriplex portulacoides) of a wetland system (Marano and Grado Lagoon, Italy) following a contamination gradient in sediments was investigated. The Hg uptake was evaluated at the root system level by calculating the enrichment factor (EF) and in the aboveground tissues by means of the translocation factor (TF). The related methylmercury (MeHg) concentrations in the halophytes were also investigated with regard to the location of the sites and their degree of contamination. Hg concentration in halophytes seemed poorly correlated both with the total Hg in rhizo-sediments and with the specific plant considered, supporting the evidence that the chemico-physical parameters of sediments could significantly affect metal availability for plants. Hg concentrations in roots increased with depth and were 20-fold higher than content measured in related rhizo-sediments (high EF). A low content of Hg is translocated in aboveground tissues (very low TF values), thus highlighting a kind of avoidance strategy of these halophytes against Hg toxicity. MeHg values were comparable between the two sites and among species, but the translocation from below- to aboveground plant tissues was more active.

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References

  • Acquavita, A., Aleffi, I. F., Benci, C., Bettoso, N., Crevatin, E., Milani, L., et al. (2015). Annual characterization of nutrients pattern and trophic state in a Mediterranean coastal lagoon: The Marano and Grado Lagoon, northern Adriatic Sea. Regional Studies in Marine Science, 2, 132–144.

    Article  Google Scholar 

  • Acquavita, A., Covelli, S., Emili, A., Berto, D., Faganeli, J., Giani, M., et al. (2012). Mercury in the sediments of the Marano and Grado Lagoon (northern Adriatic Sea): Sources, distribution and speciation. Estuarine, Coastal and Shelf Science, 113, 20–31.

    Article  CAS  Google Scholar 

  • Anjum, N. A., Ahmad, I., Válega, M., Pacheco, M., Figueira, E., Duarte, A. C., et al. (2011). Impact of seasonal fluctuations on the sediment-mercury, its accumulation and partitioning in Halimione portulacoides and Juncus maritimus collected from Ria de Aveiro Coastal Lagoon (Portugal). Water, Air, and Soil pollution, 222(1–4), 1–15.

    Article  CAS  Google Scholar 

  • Anjum, N. A., Ahmad, I., Válega, M., Pacheco, M., Figueira, E., Duarte, A. C., et al. (2012). Salt marsh macrophyte Phragmites australis strategies assessment for its dominance in mercury-contaminated coastal lagoon (Ria de Aveiro, Portugal). Environmental Science and Pollution Research, 19, 2879–2888.

    Article  CAS  Google Scholar 

  • Anjum, N. A., Israr, M., Duarte, A. C., Pereira, M. E., & Ahmad, I. (2014). Halimione portulacoides (L.) physiological/biochemical characterization for its adaptive responses to environmental mercury exposure. Environmental Research, 131, 39–49.

    Article  CAS  Google Scholar 

  • Antisari, L. V., De Nobili, M., Ferronato, C., Natale, M., Pellegrini, E., & Vianello, G. (2016). Hydromorphic to subaqueous soils transitions in the central Grado lagoon (northern Adriatic Sea, Italy). Estuarine, Coastal and Shelf Science, 173, 39–48.

    Article  Google Scholar 

  • Best, E. P., Hintelmann, H., Dimock, B., & Bednar, A. J. (2008). Natural cycles and transfer of mercury through Pacific coastal marsh vegetation dominated by Spartina foliosa and Salicornia virginica. Estuaries and Coasts, 31, 1072–1088.

    Article  CAS  Google Scholar 

  • Biester, H., Gosar, M., & Covelli, S. (2000). Mercury speciation in sediments affected by dumped mining residues in the drainage area of the Idrija mercury mine, Slovenia. Environmental Science and Technology, 34, 3330–3336.

    Article  CAS  Google Scholar 

  • Bloom, N. S., Moretto, L. M., Scopece, P., & Ugo, P. (2004). Seasonal cycling of mercury and monomethyl mercury in the Venice Lagoon (Italy). Marine Chemistry, 91(1), 85–99.

    Article  CAS  Google Scholar 

  • Bonometto, L. (2005). Functional characteristics of salt marshes in the Venice Lagoon and environmental restoration scenarios. In: C. A. Fletcher & T. Spencer (Eds.), Flooding and environmental challenges for venice and its Lagoon: State of knowledge (pp. 473–486). Cambridge: Cambridge University Press.

  • Brambati, A. (1997). Metalli pesanti nelle lagune di Marano e Grado. Piano di studi finalizzato all’accertamento di sostanze persistenti nelle Lagune di Marano e Grado ed al loro risanamento. Regione Autonoma Friuli Venezia Giulia (p. 175). Trieste: Direzione Regionale dell’Ambiente, Servizio dell’Idraulica. (in Italian).

    Google Scholar 

  • Brambati, A. (2001). Coastal sediments and biota as indicators of Hg contamination in the Marano and Grado Lagoons. RMZ: Materials and Geoenvironment, 48, 165–171.

    CAS  Google Scholar 

  • Breteler, R. J., Valiela, I., & Teal, J. M. (1981). Bioavailability of mercury in several north-eastern US Spartina ecosystems. Estuarine, Coastal and Shelf Science, 12, 155–166.

    Article  CAS  Google Scholar 

  • Burke, D. J., Weis, J. S., & Weis, P. (2000). Release of metals by the leaves of the salt marsh grasses Spartina alterniflora and Phragmites australis. Estuarine, Coastal and Shelf Science, 51, 153–159.

    Article  CAS  Google Scholar 

  • Caçador, I., Caetano, M., Duarte, B., & Vale, C. (2009). Stock and losses of trace metals from salt marsh plants. Marine Environmental Research, 67(2), 75–82.

    Article  Google Scholar 

  • Caetano, M., Vale, C., Cesário, R., & Fonseca, N. (2008). Evidence for preferential depths of metal retention in roots of salt marsh plants. The Science of the Total Environment, 390, 466–474.

    Article  CAS  Google Scholar 

  • Canário, J., Caetano, M., & Vale, C. (2006). Validation and application of an analytical method for monomethylmercury quantification in aquatic plant tissues. Analytica Chimica Acta, 580, 258–262.

    Article  Google Scholar 

  • Canário, J., Caetano, M., Vale, C., & Cesário, R. (2007). Evidence for elevated production of methylmercury in salt marshes. Environmental Science and Technology, 41, 7376–7382.

    Article  Google Scholar 

  • Canário, J., Poissant, L., Pilote, M., Caetano, M., Hintelmann, H., & O’Driscoll, N. J. (2017). Salt-marsh plants as potential sources of Hg0 into the atmosphere. Atmospheric Environment. doi:10.1016/j.atmosenv.2017.01.011.

    Google Scholar 

  • Canário, J., Vale, C., Poissant, L., Nogueira, M., Pilote, M., & Branco, V. (2010). Mercury in sediments and vegetation in a moderately contaminated salt marsh (Tagus Estuary, Portugal). Journal of Environmental Sciences, 22, 1151–1157.

    Article  Google Scholar 

  • Castro, R., Pereira, S., Lima, A., Corticeiro, S., Válega, M., Pereira, E., et al. (2009). Accumulation, distribution and cellular partitioning of mercury in several halophytes of a contaminated salt marsh. Chemosphere, 76, 1348–1355.

    Article  CAS  Google Scholar 

  • Cazzin, M., Ghirelli, L., Mion, D., & Scarton, F. (2009). Completamento della cartografia della vegetazione e degli habitat della laguna di Venezia: Anni 2005–2007. Lavori Società Veneta di Scienze Naturali, 34, 81–89.

    Google Scholar 

  • Cortinhas, A., Erben, M., Paes, A. P., Espirito Santo, D., Guara-Requena, M., & Caperta, A. D. (2015). Taxonomic complexity in the halophyte Limonium vulgare and related taxa (Plumbaginaceae): Insight from analysis of morphological, reproductive and karyological data. Annals of Botany, 115, 369–383.

    Article  Google Scholar 

  • Covelli, S. (2012). The MIRACLE Project: An integrated approach to understanding biogeochemical cycling of mercury and its relationship with lagoon clam farming. Estuarine, Coastal and Shelf Science, 13, 1–6.

    Article  Google Scholar 

  • Covelli, S., Emili, A., Acquavita, S., Koron, N., & Faganeli, J. (2011). Benthic biogeochemical cycling of mercury in two contaminated northern Adriatic coastal lagoons. Continental Shelf Research, 31, 1777–1789.

    Article  Google Scholar 

  • Covelli, S., Faganeli, J., Horvat, M., & Brambati, A. (2001). Mercury contamination in sediments of coastal sediments as the result of long-term cinnabar activity (Gulf of Trieste, northern Adriatic Sea). Applied Geochemistry, 16, 541–558.

    Article  CAS  Google Scholar 

  • Covelli, S., Langone, L., Acquavita, A., Piani, R., & Emili, A. (2012). Historical flux of mercury associated with mining and industrial sources in the Marano and Grado Lagoon (northern Adriatic Sea). Estuarine, Coastal and Shelf Science, 113, 7–19.

    Article  CAS  Google Scholar 

  • Covelli, S., Piani, R., Acquavita, A., Predonzani, S., & Faganeli, J. (2007). Transport and dispersion of particulate Hg associated with a river plume in coastal Northern Adriatic environments. Marine Pollution Bullettin, 55, 436–450.

    Article  CAS  Google Scholar 

  • De Sousa, M. P., Huang, C. P. A., & Terry, N. C. (1999). Rhizosphere bacteria enhance the accumulation of selenium and mercury in wetland plants. Planta, 209, 259–263.

    Article  Google Scholar 

  • Devai I., Patrick W. H., Neue H. -U., DeLaune R. D., Kongchum M., Rinklebe J. (2005). Methylmercury and heavy metal content in soils of rivers Saale and Elbe (Germany). Analytical Letters, 38, 1037-1048.

  • Drake, K., Halifax, H., Adamowicz, S. C., & Craft, C. (2015). Carbon Sequestration in tidal salt marshes of the northeast United States. Environmental Management, 56(4), 998–1008.

    Article  Google Scholar 

  • Flowers, T. J., & Colmer, T. D. (2008). Salinity tolerance in halophytes. New Phytologist, 179(4), 945–963.

    Article  CAS  Google Scholar 

  • Fontolan, G., Pillon, S., Bezzi, A., Villalta, R., Lipizer, M., Triches, A., et al. (2012). Human impact and the historical transformation of saltmarshes in the Marano and Grado Lagoon, northern Adriatic Sea. Estuarine, Coastal and Shelf Science, 113, 41–56.

    Article  Google Scholar 

  • Foster, N. M., Hudson, M. D., Bray, S., & Nicholls, R. J. (2013). Intertidal mudflat and saltmarsh conservation and sustainable use in the UK. A review. Journal of Environmental Management, 126(96), 104.

    Google Scholar 

  • Frohne T., Rinklebe, J. (2013). Biogeochemical fractions of mercury in soil profiles of two different floodplain ecosystems in Germany. Water, Air, and Soil Pollution, 224, 1591–1608.

    Article  Google Scholar 

  • Frohne T., Rinklebe J., Langer U., Du Laing G., Mothes S., Wennrich R. (2012). Biogeochemical factors affecting mercury methylation rate in two contaminated floodplain soils. Biogeosciences, 9, 493–507.

    Article  CAS  Google Scholar 

  • Gagnon, C., Pelletier, E., & Mucci, A. (1997). Behaviour of anthropogenic mercury in coastal marine sediments. Marine Chemistry, 59, 159–176.

    Article  CAS  Google Scholar 

  • Gardner, W. S., Kendall, D. R., Odom, R. R., Windom, H. L., & Stephens, J. A. (1978). The distribution of methylmercury in a salt marsh ecosystem. Environmental Pollution, 15, 243–251.

    Article  CAS  Google Scholar 

  • Giani, M., Rampazzo, F., Berto, D., Maggi, C., Mao, A., Horvat, M., et al. (2012). Bioaccumulation of mercury in reared and wild Ruditapes philippinarum of a Mediterranean lagoon. Estuarine, Coastal and Shelf Science, 113, 116–125.

    Article  CAS  Google Scholar 

  • Goñi, M. A., Teixeira, M. J., & Perkey, D. W. (2003). Sources and distribution of organic matter in a river-dominated estuary (Winyah Bay, SC, USA). Estuarine, Coastal and Shelf Science, 57, 1023–1048.

    Article  Google Scholar 

  • Hedges, J. I., & Stern, J. H. (1984). Carbon and nitrogen determinations of carbonate-containing solids. Limnology and Oceanography, 29, 657–663.

    Article  CAS  Google Scholar 

  • Horvat, M., Covelli, S., Faganeli, J., Logar, M., Mandić, V., Rajar, R., et al. (1999). Mercury in contaminated coastal environments; a case study: The Gulf of Trieste. The Science of the Total Environment, 237, 43–56.

    Article  Google Scholar 

  • Jackson, L. J. (1998). Paradigms of metal accumulation in rooted aquatic vascular plants. The Science of the Total Environment, 219(2), 223–231.

    Article  CAS  Google Scholar 

  • Kraus, M. L., Weis, P., & Crow, J. H. (1986). The excretion of heavy metals by the salt marsh cord grass, Spartina alterniflora, and Spartina’s role in mercury cycling. Marine Environmental Research, 20, 307–316.

    Article  CAS  Google Scholar 

  • Leady, B. S., & Gottgens, J. F. (2001). Mercury accumulation in sediment cores and along food chains in two regions of the Brazilian Pantanal. Wetland Ecology Management, 9, 349–361.

    Article  CAS  Google Scholar 

  • Lucena, J. J., Hernández, L. E., & Carpena-Ruíz, R. O. (1993). Micronutrient content in leguminous plants contaminated with mercury. In M. A. C. Fragoso & M. L. Van Beusichen (Eds.), Optimization of plant nutrition (pp. 531–537). Dordretch: Kluwer Academic Publishers.

    Chapter  Google Scholar 

  • Marques, B., Lillebø, A. I., Pereira, E., & Duarte, A. C. (2011). Mercury cycling and sequestration in salt marshes sediments: An ecosystem service provided by Juncus maritimus and Scirpus maritimus. Environmental Pollution, 159, 1869–1876.

    Article  CAS  Google Scholar 

  • Mergler, D., Anderson, H. A., Chan, L. H. M., Mahaffey, K. R., Murray, M., et al. (2007). Methylmercury exposure and health effects in humans: A worldwide concern. Ambio: A Journal of the Human Environment, 36, 3–11.

    Article  CAS  Google Scholar 

  • O’Driscoll, N. J., Canário, J., Crowell, N., & Webster, T. (2011). Mercury speciation and distribution in coastal wetlands and tidal mudflats: Relationships with sulphur speciation and organic carbon. Water, Air, and Soil pollution, 220, 313–326.

    Article  Google Scholar 

  • Pereira, M. E., Lillebø, A. I., Pato, P., Válega, M., Coelho, J. P., Lopes, C. B., et al. (2009). Mercury pollution in Ria de Aveiro (Portugal): A review of the system assessment. Environmental Monitoring and Assessment, 155, 39–49.

    Article  CAS  Google Scholar 

  • Petranich, E., Acquavita, A., Covelli, S., & Emili, A. (2016). Potential bioaccumulation of trace metals in halophytes from salt marshes of a northern Adriatic coastal lagoon. Journal of Soils and Sediments. doi:10.1007/s11368-016-1545.

    Google Scholar 

  • Piani, R., & Covelli, S. (2001). Contributo antropico di metalli pesanti e 137Cs nei sedimenti del bacino di Buso (Laguna di Marano e Grado, Italia settentrionale). Studi Trentini di Scienze Naturali-Acta Geologica, 77, 169–177.

    Google Scholar 

  • Piani, R., Covelli, S., & Biester, H. (2005). Mercury contamination in Marano Lagoon (northern Adriatic sea, Italy): Source identification by analyses of Hg phases. Applied Geochemistry, 20, 1546–1559.

    Article  CAS  Google Scholar 

  • Poldini, L., Oriolo, G., Vidali, M., Tomasella, M., Stoch, F., & Orel, G. (2006). Manuale degli habitat del Friuli Venezia Giulia. Strumento a supporto della valutazione d’impatto ambientale (VIA), ambientale strategica (VAS) e d’incidenza ecologica (VIEc). Regione Autonoma Friuli Venezia Giulia-Direz. Trieste: Centrale ambiente e lavori pubblici-Servizio valutazione impatto ambientale, Univ. Studi Trieste-Dipart. Biologia. (in Italian).

    Google Scholar 

  • R Core Team. (2013). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

    Google Scholar 

  • Reboreda, R., & Caçador, I. (2007). Halophyte vegetation influences in salt marsh retention capacity for heavy metals. Environmental Pollution, 146, 147–154.

    Article  CAS  Google Scholar 

  • Rodrigues, M. J., Gangadhar, K. N., Vizetto-Duarte, C., Wubshet, S. G., Nyberg, N. T., Barreira, L., et al. (2014). Maritime halophyte species from southern Portugal as sources of bioactive molecules. Marine Drugs, 100, 2228–2244.

    Article  Google Scholar 

  • Rozema, J., Gude, H., & Pollak, G. (1981). An ecophysiological study of the salt secretion of four halophytes. New Phytology, 89, 201–217.

    Article  CAS  Google Scholar 

  • Shepard, F. P. (1954). Nomenclature based on sand-silt-clay ratios. Journal of Sedimentary Petrology, 24, 151–158.

    Article  Google Scholar 

  • Skinner, K., Wright, N., & Porter-Goff, E. (2007). Mercury uptake and accumulation by four species of aquatic plants. Environmental Pollution, 14, 234–237.

    Article  Google Scholar 

  • Sladonja, B., Bettoso, N., Zentilin, A., Tamberlich, F., & Acquavita, A. (2011). Manila Clam (Tapes philippinarum Adams & Reeve, 1852) in the Lagoon of Marano and Grado (northern Adriatic Sea, Italy): Socio-economic and environmental pathway of a shell farm. In: B. Sladonja (Ed.), Aquaculture and the environment—A shared destiny, Published: December 22, 2011 under CC BY 3.0 license. InTech d.o.o., Rijeka, Croatia.

  • Sousa, A. I., Caçador, I., Lillebø, A. I., & Pardal, A. (2008). Heavy metal accumulation in Halimione portulacoides: Intra- and extra-cellular metal binding sites. Chemosphere, 70, 850–857.

    Article  CAS  Google Scholar 

  • St-Cyr, L., & Campbell, P. G. C. (1996). Metals (Fe, Mn, Zn) in the root plaque of submerged aquatic plants collected in situ: Relations with metal concentrations in the adjacent sediments and in the root tissue. Biogeochemistry, 33, 45–76.

    Article  CAS  Google Scholar 

  • Ulrich, S. M., Tanton, T. W., & Abdrashitova, S. A. (2001). Mercury in the aquatic environment: A review of factors affecting methylation. Critical Review in Environmental Science and Technology, 31, 241–293.

    Article  Google Scholar 

  • Válega, M., Lillebø, A. I., Caçador, I., Pereira, M. E., Duarte, A. C., & Pardal, M. A. (2008a). Mercury mobility in a salt marsh colonised by Halimione portulacoides. Chemosphere, 72, 1607–1613.

    Article  Google Scholar 

  • Válega, M., Lillebø, A. I., Pereira, M. E., Caçador, I., Duarte, A. C., & Pardal, M. A. (2008b). Mercury in salt marshes ecosystems: Halimione portulacoides as biomonitor. Chemosphere, 73, 1224–1229.

    Article  Google Scholar 

  • Válega, M., Lillebø, A. I., Pereira, M. E., Corns, W. T., Stockwell, P. B., Duarte, A. C., et al. (2008c). Assessment of methylmercury production in a temperate salt marsh (Ria de Aveiro Lagoon, Portugal). Marine Pollution Bulletin, 56, 136–162.

    Article  Google Scholar 

  • Válega, M., Lillebø, A. I., Pereira, M. E., Duarte, A. C., & Pardal, M. A. (2008d). Long-term effects of mercury in a salt marsh: Hysteresis in the distribution of vegetation following recovery from contamination. Chemosphere, 71, 765–772.

    Article  Google Scholar 

  • Válega, M., Lima, A. I. G., Figueira, E. M. A. P., Pereira, E., Pardal, M. A., & Duarte, A. C. (2009). Mercury intracellular partitioning and chelation in a salt marsh plant, Halimione portulacoides (L.) Aellen: Strategies underlying tolerance in environmental exposure. Chemosphere, 74, 530–536.

    Article  Google Scholar 

  • Vilela, C., Santos, S. A. O., Coelho, D., Silva, A. M. S., Freire, C. S. R., Neto, C. P., et al. (2014). Screening of lipophilic and phenolic extractives from different morphological parts of Halimione portulacoides. Industrial Crops and Products, 52, 373–379.

    Article  CAS  Google Scholar 

  • Weis, J. S., & Weis, P. (2004). Metal uptake, transport and release by wetland plants: Implications for phytoremediation and restoration. Environment International, 30, 685–700.

    Article  CAS  Google Scholar 

  • Weis, P., Windham, L., Burke, D. J., & Weis, J. S. (2002). Release into the environment of metals by two vascular salt marsh plants. Marine Environmental Research, 54, 325–329.

    Article  CAS  Google Scholar 

  • Windham, L., Weis, J. S., & Weis, P. (2003). Uptake and distribution of metals in two dominant salt marsh macrophytes, Spartina alterniflora (cordgrass) and Phragmites australis (common reed). Estuarine, Coastal and Shelf Science, 56, 63–72.

    Article  CAS  Google Scholar 

  • Windom, H., Gardner, W., Stephens, J., & Taylor, F. (1976). The role of methylmercury production in the transfer of mercury in a salt marsh ecosystem. Estuarine, Coastal Marine Science, 4, 579–583.

    Article  CAS  Google Scholar 

  • Yoon, J., Cao, X., Zhou, Q., & Ma, L. Q. (2006). Accumulation of Pb, Cu and Zn in native plants growing on a contaminated Florida site. The Science of the Total Environment, 368, 456–464.

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the University of Trieste and by the Environmental Protection Agency of Friuli Venezia Giulia (ARPA-FVG), and was carried out in the framework of the Project entitled Studio SedimentologicoGeochimico delle aree barenicole della Laguna di Marano & Grado (scientific coordinators Stefano Covelli and Giorgio Fontolan). The authors wish to thank the ARPA-FVG for logistic support during the sampling campaign in the Marano and Grado Lagoon. Special thanks to Karry Close for proofreading.

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Pellegrini, E., Petranich, E., Acquavita, A. et al. Mercury uptake by halophytes in response to a long-term contamination in coastal wetland salt marshes (northern Adriatic Sea). Environ Geochem Health 39, 1273–1289 (2017). https://doi.org/10.1007/s10653-017-9981-y

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