Advertisement

Mercury accumulation and biotransportation in wetland biota affected by gold mining

  • Odwa Mbanga
  • Somandla Ncube
  • Hlanganani Tutu
  • Luke Chimuka
  • Ewa CukrowskaEmail author
Article
  • 105 Downloads

Abstract

Phytoremediation is a cost-effective, eco-friendly technology for the removal of metals from polluted areas. In this study, six different plant species (Datura stramonium, Phragmites australis, Persicaria lapathifolia, Melilotus alba, Panicum coloratum, and Cyperus eragrostis) growing in a gold mine contaminated wetland were investigated as potential phytoremediators of mercury. The accumulation of total mercury and methylmercury in plant tissues was determined during the wet and dry seasons to establish the plants’ variability in accumulation. The highest accumulation of total mercury was in the tissues of Phragmites australis with recorded concentrations of 806, 495, and 833 μg kg−1 in the roots, stem, and leaves, respectively, during the dry season. The lowest accumulation levels were recorded for Melilotus alba during both seasons. The highest amount of the methylmercury was found in Phragmites australis during the dry season with a value of 618 μg kg−1. The accumulation and biotransportation were not significantly different between the seasons for some plants. The results of this study indicated that plants growing in wetlands can be used for phytoremediation of mercury and suggest the choice of species for constructed wetlands.

Keywords

Bioaccumulation Mercury Methylation Phytoremediation Seasonality Wetlands 

Notes

Funding information

The authors thank the Water Research Commission of South Africa (Grant number K5/2394//3) for funding this project.

References

  1. Akcil, A., Erust, C., Ozdemiroglu, S., Fonti, V., & Beolchini, F. (2015). A review of approaches and techniques used in aquatic contaminated sediments: metal removal and stabilization by chemical and biotechnological processes. Journal of Cleaner Production, 86, 24–26.  https://doi.org/10.1016/j.jclepro.2014.08.009.CrossRefGoogle Scholar
  2. Azevedo, R., & Rodriguez, E. (2012). Phytotoxicity of mercury in plants: a review. Journal of Botany, 2012, 1–6.  https://doi.org/10.1155/2012/848614.CrossRefGoogle Scholar
  3. Boening, D. (2000). Ecological effects, transport, and fate of mercury: a general review. Chemosphere, 40(12), 1335–1351.CrossRefGoogle Scholar
  4. Březinová, T., & Vymazal, J. (2015). Evaluation of heavy metals seasonal accumulation in Phalaris arundinacea in a constructed treatment wetland. Ecological Engineering, 79, 94–99.  https://doi.org/10.1016/j.ecoleng.2015.04.008.CrossRefGoogle Scholar
  5. Calderón, J., Gonçalves, S., Cordeiro, F., & de la Calle, B. (2013). Determination of methylmercury in seafood by direct mercury analysis: standard operating procedure (p. 80259). JRC.Google Scholar
  6. Chen, J., & Yang, Z. M. (2012). Mercury toxicity, molecular response and tolerance in higher plants. BioMetals, 25(5), 847–857.  https://doi.org/10.1007/s10534-012-9560-8.CrossRefGoogle Scholar
  7. Chen, G. Q., Li, J. S., Chen, B., Wen, C., Yang, Q., Alsaedi, A., & Hayat, T. (2016). An overview of mercury emissions by global fuel combustion: the impact of international trade. Renewable and Sustainable Energy Reviews, 65, 345–355.  https://doi.org/10.1016/j.rser.2016.06.049.CrossRefGoogle Scholar
  8. Chibuike, G. U., & Obiora, S. C. (2014). Heavy metal polluted soils: effect on plants and bioremediation methods. Applied and Environmental Soil Science, 2014, 1–12.  https://doi.org/10.1155/2014/752708.CrossRefGoogle Scholar
  9. Choppala, G., Saifullah, Bolan, N., Bibi, S., Iqbal, M., Rengel, Z., et al. (2014). Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Critical Reviews in Plant Sciences, 33(5), 374–391.  https://doi.org/10.1080/07352689.2014.903747.CrossRefGoogle Scholar
  10. Dabrowski, J. M., Ashton, P. J., Murray, K., Leaner, J. J., & Mason, R. P. (2008). Anthropogenic mercury emissions in South Africa: coal combustion in power plants. Atmospheric Environment, 42(27), 6620–6626.  https://doi.org/10.1016/j.atmosenv.2008.04.032.CrossRefGoogle Scholar
  11. De Simone, F., Gencarelli, C. N., Hedgecock, I. M., & Pirrone, N. (2016). A modeling comparison of mercury deposition from current anthropogenic mercury emission inventories. Environmental Science and Technology, 50(10), 5154–5162.  https://doi.org/10.1021/acs.est.6b00691.CrossRefGoogle Scholar
  12. Deng, H., Ye, Z. H., & Wong, M. H. (2004). Accumulation of lead, zinc, copper and cadmium by 12 wetland plant species thriving in metal-contaminated sites in China. Environmental Pollution, 132(1), 29–40.  https://doi.org/10.1016/j.envpol.2004.03.030.CrossRefGoogle Scholar
  13. Dombaiová, R. (2005). Mercury and methylmercury in plants from differently contaminated sites in Slovakia. Plant, Soil and Environment, 51(10), 456–463.  https://doi.org/10.1002/jpln.200421635.CrossRefGoogle Scholar
  14. Dye, P. J., Jarmain, C., Oageng, B., Xaba, J., & Weiersbye, I. M. (2008). The potential of woodlands and reed-beds for control of acid mine drainage in the Witwatersrand gold fields, South Africa. Mine Closure, 2, 487–497.Google Scholar
  15. Edraki, M., Baumgartl, T., Manlapig, E., Bradshaw, D., Franks, D. M., & Moran, C. J. (2014). Designing mine tailings for better environmental, social and economic outcomes: a review of alternative approaches. Journal of Cleaner Production, 84(1), 411–420.  https://doi.org/10.1016/j.jclepro.2014.04.079.CrossRefGoogle Scholar
  16. Fagerström, T., & Jernelöv, A. (1971). Formation of methyl mercury from pure mercuric sulphide in aerobic organic sediment. Water Research, 5(3), 121–122.  https://doi.org/10.1016/0043-1354(71)90127-8.CrossRefGoogle Scholar
  17. Fashola, M. O., Ngole-Jeme, V. M., & Babalola, O. O. (2016). Heavy metal pollution from gold mines: environmental effects and bacterial strategies for resistance. International Journal of Environmental Research and Public Health, 13(11), 1–20.  https://doi.org/10.3390/ijerph13111047.CrossRefGoogle Scholar
  18. Forstner, U., & Wittman, G. T. W. (1976). Metal accumulation in acidic waters from gold mines in South Africa. Geoforum, 7(1), 41–49.CrossRefGoogle Scholar
  19. Gabriel, M. C., & Williamson, D. G. (2004). Principal biogeochemical factors affecting the speciation and transport of mercury through the terrestrial environment. Environmental Geochemistry and Health, 26(3–4), 421–434.  https://doi.org/10.1007/s10653-004-1308-0.CrossRefGoogle Scholar
  20. Galal, T. M., & Shehata, H. S. (2015). Bioaccumulation and translocation of heavy metals by Plantago major L. grown in contaminated soils under the effect of traffic pollution. Ecological Indicators, 48, 244–251.  https://doi.org/10.1016/j.ecolind.2014.08.013.CrossRefGoogle Scholar
  21. García-Mercadoa, H. D., Fernándezb, G., Garzón-Zúñigac, M. A., & Durán-Domínguez-de-Bazúaa, M. d. C. (2017). Remediation of mercury-polluted soils using artificial wetlands. International Journal of Phytoremediation, 19(1), 3–13.  https://doi.org/10.1080/15226514.2016.1216074.CrossRefGoogle Scholar
  22. Jiang, B., Xing, Y., Zhang, B., Cai, R., Zhang, D., & Sun, G. (2018). Effective phytoremediation of low-level heavy metals by native macrophytes in a vanadium mining area, China. Environmental Science and Pollution Research, 25(31), 31272–31282.  https://doi.org/10.1007/s11356-018-3069-9.CrossRefGoogle Scholar
  23. Keller, B. E. M., Lajtha, K., & Cristofor, S. (1998). Trace metal concentrations in the sediments and plants of the Danube Delta, Romani. The society of wetland scientists, 18(1), 42–50.CrossRefGoogle Scholar
  24. Leguizamo, M. A., Fernandez Gomez, W. D., & Sarmiento, M. C. G. (2017). Native herbaceous plant species with potential use in phytoremediation of heavy metals, spotlight on wetlands: a review. Chemosphere, 168, 1230–1247.  https://doi.org/10.1016/j.chemosphere.2016.10.075.CrossRefGoogle Scholar
  25. Li, Z., Ma, Z., Van der Kuijp, T. J., Yuan, Z., & Huang, L. (2014). A review of soil heavy metal pollution from mines in China: pollution and health risk assessment. Science of the Total Environment, 468–469, 843–853.  https://doi.org/10.1016/j.scitotenv.2013.08.090.CrossRefGoogle Scholar
  26. Lusilao-Makiese, J. G., Tessier, E., Amouroux, D., Tutu, H., Chimuka, L., Weiersbye, I., & Cukrowska, E. M. (2014). Seasonal distribution and speciation of mercury in a gold mining area, north-west province, South Africa. Toxicological and Environmental Chemistry, 96(3), 387–402.  https://doi.org/10.1080/02772248.2014.947987.CrossRefGoogle Scholar
  27. Lusilao-Makiese, J. G., Tessier, E., Amouroux, D., Tutu, H., Chimuka, L., Weiersbye, I., & Cukrowska, E. M. (2016). Mercury speciation and dispersion from an active gold mine at the west Wits area, South Africa. Environmental Monitoring and Assessment, 188(1), 1–11.  https://doi.org/10.1007/s10661-015-5059-4.CrossRefGoogle Scholar
  28. MacDonald, D. D., Ingersoll, C. G., & Berger, T. A. (2000). Development and evaluation of consensus-based sediment quality guidelines for freshwater ecosystems. Archives of Environmental Contamination and Toxicology, 39(1), 20–31.  https://doi.org/10.1007/s002440010075.CrossRefGoogle Scholar
  29. Maggi, C., Berducci, M. T., Bianchi, J., Giani, M., & Campanella, L. (2009). Methylmercury determination in marine sediment and organisms by Direct Mercury Analyser. Analytica Chimica Acta, 641(1), 32-36.Google Scholar
  30. Mahar, A., Wang, P., Ali, A., Awasthi, M. K., Lahori, A. H., Wang, Q., Li, R., & Zhang, Z. (2016). Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: a review. Ecotoxicology and Environmental Safety, 126, 111–121.  https://doi.org/10.1016/j.ecoenv.2015.12.023.CrossRefGoogle Scholar
  31. Majid, S. N., Khwakaram, A. I., Rasul, G. A. M., & Ahmed, Z. H. (2014). Bioaccumulation, enrichment and translocation factors of some heavy metals in Typha Angustifolia and Phragmites Australis species growing along Qalyasan stream in Sulaimani city / IKR. Zankoy Sulaimani, 16(4), 93–109.CrossRefGoogle Scholar
  32. Marrugo-Negrete, J., Durango-Hernández, J., Pinedo-Hernández, J., Olivero-Verbel, J., & Díez, S. (2015). Phytoremediation of mercury-contaminated soils by Jatropha curcas. Chemosphere, 127, 58–63.  https://doi.org/10.1016/j.chemosphere.2014.12.073.CrossRefGoogle Scholar
  33. McDaniel, W. (1991). Method 200.3 Sample preparation procedure for spectrochemical determination of total recoverable elements in biological tissues (pp. 24–29). Cincinnati, OH: Environmental Protection Agency.Google Scholar
  34. Mendez, M. O., & Maier, R. M. (2008). Phytoremediation of mine tailings in temperate and arid environments. Reviews in Environmental Science and Biotechnology, 7(1), 47–59.  https://doi.org/10.1007/s11157-007-9125-4.CrossRefGoogle Scholar
  35. Mukherjee, D. (2014). Selection and application of lime stabilizer for soil subgrade stabilization. International Journal of Innovative Science, Engineering & Technology, 1(7), 66–76 http://www.ijiset.com/v1s7/IJISET_V1_I7_12.pdf. Accessed July 2018
  36. Núñez, S. E. R., Negrete, J. L. M., Rios, J. E. A., Hadad, H. R., & Maine, M. A. (2011). Hg, Cu, Pb, Cd, and Zn accumulation in macrophytes growing in tropical wetlands. Water, Air, and Soil Pollution, 216(1–4), 361–373.  https://doi.org/10.1007/s11270-010-0538-2.CrossRefGoogle Scholar
  37. Odumo, B. O., Carbonell, G., Angeyo, H. K., Patel, J. P., Torrijos, M., & Rodríguez Martín, J. A. (2014). Impact of gold mining associated with mercury contamination in soil, biota sediments and tailings in Kenya. Environmental Science and Pollution Research, 21(21), 12426–12435.  https://doi.org/10.1007/s11356-014-3190-3.CrossRefGoogle Scholar
  38. Oluyemi, E. A., Feuyit, G., Oyekunle, J. A. O., & Ogunfowokan, A. O. (2008). Seasonal variations in heavy metal concentrations in soil and some selected crops at a landfill in Nigeria. African Journal of Environmental Science and Technology, 2(5), 89–96.Google Scholar
  39. Pacyna, E. G., Pacyna, J. M., Steenhuisen, F., & Wilson, S. (2006). Global anthropogenic mercury emission inventory for 2000. Atmospheric Environment, 40, 4048–4063.  https://doi.org/10.1016/j.atmosenv.2006.03.041.CrossRefGoogle Scholar
  40. Padmavathiamma, P. K., & Li, L. Y. (2007). Phytoremediation technology: hyper-accumulation metals in plants. Water, Air, and Soil Pollution, 184(1–4), 105–126.  https://doi.org/10.1007/s11270-007-9401-5.CrossRefGoogle Scholar
  41. Pinedo-Hernández, J., Marrugo-Negrete, J., & Díez, S. (2015). Speciation and bioavailability of mercury in sediments impacted by gold mining in Colombia. Chemosphere, 119, 1289–1295.  https://doi.org/10.1016/j.chemosphere.2014.09.044.CrossRefGoogle Scholar
  42. Pirrone, N., Cinnirella, S., Feng, X., Finkelman, R. B., Friedli, H. R., Leaner, J., Mason, R., Mukherjee, A. B., Stracher, G. B., Streets, D. G., & Telmer, K. (2010). Global mercury emissions to the atmosphere from anthropogenic and natural sources. Atmospheric Chemistry and Physics, 10, 5951–5964.  https://doi.org/10.5194/acp-10-5951-2010.CrossRefGoogle Scholar
  43. Puga, A. P., Abreu, C. A., Melo, L. C. A., Paz-Ferreiro, J., & Beesley, L. (2015). Cadmium, lead, and zinc mobility and plant uptake in a mine soil amended with sugarcane straw biochar. Environmental Science and Pollution Research, 22(22), 17606–17614.  https://doi.org/10.1007/s11356-015-4977-6.CrossRefGoogle Scholar
  44. Radulescu, C., Stihi, C., Popescu, I. V., Dulama, I. D., Chelarescu, E. D., & Chilian, A. (2013). Heavy metal accumulation and translocation in different parts of Brassica oleracea L. Romanian Journal of Physics, 58(9–10), 1337–1354.Google Scholar
  45. Rai, P. K. (2008). Heavy metal pollution in aquatic ecosystems and its phytoremediation using wetland plants: an ecosustainable approach. International Journal of Phytoremediation, 10(2), 133–160.  https://doi.org/10.1080/15226510801913918.CrossRefGoogle Scholar
  46. Rai, U. N., Upadhyay, A. K., Singh, N. K., Dwivedi, S., & Tripathi, R. D. (2015). Seasonal applicability of horizontal sub-surface flow constructed wetland for trace elements and nutrient removal from urban wastes to conserve Ganga river water quality at Haridwar, India. Ecological Engineering, 81, 115–122.  https://doi.org/10.1016/j.ecoleng.2015.04.039.CrossRefGoogle Scholar
  47. Rezania, S., Mat, S., & Fadhil, M. (2016). Comprehensive review on phytotechnology: heavy metals removal by diverse aquatic plants species from wastewater. Journal of Hazardous Materials, 318, 587–599.  https://doi.org/10.1016/j.jhazmat.2016.07.053.CrossRefGoogle Scholar
  48. Robinson, J. B., & Tuovinen, O. H. (1984). Mechanisms of microbial resistance and detoxification of mercury and organomercury compounds: physiological, biochemical, and genetic analyses. Microbiological Reviews, 48(2), 95–124.Google Scholar
  49. Sarwar, N., Imran, M., Shaheen, M. R., Ishaque, W., Kamran, M. A., Matloob, A., Rehim, A., & Hussain, S. (2017). Phytoremediation strategies for soils contaminated with heavy metals: modifications and future perspectives. Chemosphere, 171, 710–721.  https://doi.org/10.1016/j.chemosphere.2016.12.116.CrossRefGoogle Scholar
  50. Schonfeld, S. J., Winde, F., Albrecht, C., Kielkowski, D., Liefferink, M., Patel, M., Sewram, V., Stoch, L., Whitaker, C., Schüz, J., & workshop participants. (2014). Health effects in populations living around the uraniferous gold mine tailings in South Africa: gaps and opportunities for research. Cancer Epidemiology, 38(5), 628–632.  https://doi.org/10.1016/j.canep.2014.06.003.CrossRefGoogle Scholar
  51. Schroeder, W. H., & Munthe, J. (1998). Atmospheric mercury: an overview. Atmospheric Environment, 32(5), 809–822.  https://doi.org/10.1016/S1352-2310(97)00293-8.CrossRefGoogle Scholar
  52. Song, S., Selin, N. E., Soerensen, A. L., Angot, H., Artz, R., Brooks, S., Brunke, E. G., Conley, G., Dommergue, A., Ebinghaus, R., Holsen, T. M., Jaffe, D. A., Kang, S., Kelley, P., Luke, W. T., Magand, O., Marumoto, K., Pfaffhuber, K. A., Ren, X., Sheu, G. R., Slemr, F., Warneke, T., Weigelt, A., Weiss-Penzias, P., Wip, D. C., & Zhang, Q. (2015). Top-down constraints on atmospheric mercury emissions and implications for global biogeochemical cycling. Atmospheric Chemistry and Physics, 15(12), 7103–7125.  https://doi.org/10.5194/acp-15-7103-2015.CrossRefGoogle Scholar
  53. Tangahu, B. V., Sheikh Abdullah, S. R., Basri, H., Idris, M., Anuar, N., & Mukhlisin, M. (2011). A review on heavy metals (As, Pb, and Hg) uptake by plants through phytoremediation. International Journal of Chemical Engineering, 2011, 1–31.  https://doi.org/10.1155/2011/939161.CrossRefGoogle Scholar
  54. Tsang, D. C. W., & Yip, A. C. K. (2014). Comparing chemical-enhanced washing and waste-based stabilisation approach for soil remediation. Journal of Soils and Sediments, 14(5), 936–947.  https://doi.org/10.1007/s11368-013-0831-y.CrossRefGoogle Scholar
  55. Tutu, H., Cukrowska, E. M., Dohnal, V., & Havel, J. (2005). Application of artificial neural networks for classification of uranium distribution in the central rand goldfield, South Africa. Environmental Modeling and Assessment, 10(2), 143–152.  https://doi.org/10.1007/s10666-005-0214-x.CrossRefGoogle Scholar
  56. Ullah, A., Heng, S., Munis, M. F. H., Fahad, S., & Yang, X. (2015). Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: a review. Environmental and Experimental Botany, 117, 28–40.  https://doi.org/10.1016/j.envexpbot.2015.05.001.CrossRefGoogle Scholar
  57. Ullrich, S. M., Tanton, T. W., & Abdrashitova, S. A. (2001). Mercury in the aquatic environment: a review of factors affecting methylation. Critical Reviews in Environmental Science and Technology, 31(3), 241–293.  https://doi.org/10.1080/20016491089226.CrossRefGoogle Scholar
  58. Wang, J., Feng, X., Anderson, C. W. N., Xing, Y., & Shang, L. (2012). Remediation of mercury contaminated sites: a review. Journal of Hazardous Materials, 221–222, 1–18.  https://doi.org/10.1016/j.jhazmat.2012.04.035.CrossRefGoogle Scholar
  59. Weiersbye, I. M., Witkowski, E. T. F., & Reichardt, M. (2006). Floristic composition of gold and uranium tailings dams, and adjacent polluted areas, on South Africa’s deep-level mines. Bothalia, 36(May), 101–127.Google Scholar
  60. Weis, J. S., & Weis, P. (2004). Metal uptake, transport and release by wetland plants: implications for phytoremediation and restoration. Environment International, 30(5), 685–700.  https://doi.org/10.1016/j.envint.2003.11.002.CrossRefGoogle Scholar
  61. Windham, L., Weis, J. S., Weis, P., & Peddrick, W. (2001). Patterns and processes of mercury release from leaves of two dominant salt marsh macrophytes Phragmites australis and Spartina alterniflora. Estuaries, 24(6A), 787–795.  https://doi.org/10.2307/1353170.CrossRefGoogle Scholar
  62. Xu, J., Bravo, A. G., Lagerkvist, A., Bertilsson, S., Sjöblom, R., & Kumpiene, J. (2014). Sources and remediation techniques for mercury contaminated soil. Environment International, 74, 42–53.  https://doi.org/10.1016/j.envint.2014.09.007.CrossRefGoogle Scholar
  63. Yang, S., Liang, S., Yi, L., Xu, B., Cao, J., Guo, Y., & Zhou, Y. (2014). Heavy metal accumulation and phytostabilization potential of dominant plant species growing on manganese mine tailings. Frontiers of Environmental Science and Engineering, 8(3), 394–404.  https://doi.org/10.1007/s11783-013-0602-4.CrossRefGoogle Scholar
  64. Zhang, L., Wang, S., Wang, L., Wu, Y., Duan, L., Wu, Q., Wang, F., Yang, M., Yang, H., Hao, J., & Liu, X. (2015). Updated emission inventories for speciated atmospheric mercury from anthropogenic sources in China. Environmental Science and Technology, 49(5), 3185–3194.  https://doi.org/10.1021/es504840m.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Odwa Mbanga
    • 1
  • Somandla Ncube
    • 1
  • Hlanganani Tutu
    • 1
  • Luke Chimuka
    • 1
  • Ewa Cukrowska
    • 1
    Email author
  1. 1.Molecular Sciences Institute, School of ChemistryUniversity of the WitwatersrandJohannesburgSouth Africa

Personalised recommendations