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Phytoremediation of cadmium by the facultative halophyte plant Bolboschoenus maritimus (L.) Palla, at different salinities

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Abstract

The cadmium phytoremediation capacity of the halophyte plant Bolboschoenus maritimus (L.) Palla and the influence of water salinity were assessed in a greenhouse experiment, in order to better understand the bioremediation capacity of this plant. Three concentrations of cadmium (0, 50 and 100 μg l−1) and four salinity conditions (0, 5, 10 and 20) were chosen to evaluate the cadmium accumulation, in order to test these plants as a potential phytoremediation tool in brackish environments. The cadmium content in water and plants (underground organs, stems and leaves) was analysed with graphite furnace atomic absorption spectrometry. All the plants submitted to salinity 20 and in the three cadmium treatments died. The plants’ survival was highest in the lowest salinities, where highest growth and biomasses were also obtained. The plants presented more cadmium content in the rhizomes, followed by stems and even less in leaves. The salt stress of the plants interfered with their cadmium accumulation capacity. The highest cadmium accumulation in the rhizomes occurred at salinity 0, while the salinities 0 and 5 were the most adequate for stems and leaves. The experiment pointed out that B. maritimus represents a good possible intervenient for cadmium bioremediation in freshwater and low salinity brackish water environments, but its use is limited in the habitats of higher salinity.

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References

  • Barzev A, Dobreva D, Futekov L, Rusev V, Bekjarov G, Toneva G (1986) Determination of detection limits in graphite furnace atomic absorption spectrometry by using ensemble summation of signals. Freserfius Z, Anal Chem 325:255–57. doi:10.1007/BF00498168

    Article  CAS  Google Scholar 

  • Benavides MP, Gallegos SM, Tomaro M (2005) Cadmium toxicity in plants. Braz JPlant Physiol 17(1):21–34. doi:10.1590/S1677-04202005000100003

    CAS  Google Scholar 

  • Bragato C, Brix H, Malagoli M (2006) Accumulation of nutrients and heavy metals in Phragmites australis (Cav.) Trin. ex Steudel and Bolboschoenus maritimus (L.) Palla in a constructed wetland of the Venice lagoon watershed. Environ Pollut 144:967–975. doi:10.1016/j.envpol.2006.01.046

    Article  CAS  Google Scholar 

  • Carranza-Álvarez C, Alonso-Castro A, La Torre M, La Cruz R (2008) Accumulation and distribution of heavy metals in Scirpus americanus and Typhia latifolia from an artificial lagoon in San Luis Potosí, Mexico. Water Air Soil Poll 188:297–309. doi:10.1007/s11270-007-9545-3

    Article  Google Scholar 

  • Cheraghi M, Lorestani B, Yousefi N (2011) Introduction of hyperaccumulator plants with phytoremediation potential of a lead-zinc mine in Iran. WASET 77: 163-168. http://waset.org/publications/1833

  • Costa JC, Arsénio P, Monteiro-Henriques T, Neto C, Pereira E, Almeida T, Izco T (2009) Finding the boundary between Eurosiberian and Mediterranean salt marshes. J Coastal Res Si 56: 1340-1344. http://www.jstor.org/stable/25738007

  • Cronk JK, Fennessy MS (2001) Wetland plants: biology and ecology. Lewis Publishers, Boca Raton

    Book  Google Scholar 

  • Directive 2000/60/EC of the European Parliament and of the Council, of 23 October 2000, establishing a framework for community action in the field of water policy. Official Journal of the European Communities, L327/1-L327/72

  • Dong J, Mao WH, Zhang GP, Wu FB, Cai Y (2007) Root excretion and plant tolerance to cadmium toxicity—a review. Plant Soil Environ 53(5):193–200

    CAS  Google Scholar 

  • Duffus JH (2002) “Heavy metal”—a meaningless term? Pure Appl Chem 74:793–807

    Article  CAS  Google Scholar 

  • Eleftheriou A, McIntyre AD (ed) (2005) Methods for the study of marine benthos. 3rd edition. Blackwell Science: Oxford. ISBN 0-632-05488-3. XXI, 418 pp

  • Fortunato AB, Oliveira A (2005) Influence of intertidal flats on tidal asymmetry. JCR 21(5):1062–1067. doi:10.2112/03-0089.1

    Google Scholar 

  • Gosh M, Singh SP (2005) A comparative study of cadmium phytoextraction by accumulator and weed species. Environ Pollut 133:365–371. doi:10.1016/j.envpol.2004.05.015

    Article  Google Scholar 

  • Hegedus H, Kerepeczki E, Gál D, Pekár F, Bíróné O, Lakatos G (2010) Potential role of halophytic macrophytes in saline effluent treatment. Waste 64: 273-277. http://waset.org/publications/6467

  • Hroudová Z, Zákravsky P, Flegrová M (2014) The tolerance to salinity and nutrient supply in four European Bolboschoenus species (B. maritimus, B. laticarpus, B. planiculmis and B. yagara) affects their vulnerability or expansiveness. Aquat Bot 112:66–75. doi:10.1016/j.aquabot.2013.07.012

    Article  Google Scholar 

  • Hseu Z (2004) Evaluating heavy metal contents in nine composts using four digestion methods. Bioresource Technol 95:53–59. doi:10.1016/j.biortech.2004.02.008

    Article  CAS  Google Scholar 

  • Kamnev AA, Lelie D (2000) Chemical and biological parameters as tools to evaluate and improve heavy metal phytoremediation. Biosci Rep 20(4):239–58

    Article  CAS  Google Scholar 

  • Kantrud HA (1996) The alkali (Scirpus maritimus L.) and saltmarsh (S. robustus Pursh) bulrushes: a literature review. National Biological Service, Information and Technology Report 6. Northern Prairie Wildlife Research Centre, Jamestown, ND (http://www.npwrc.usgs.gov/resource/literatr/bulrush/bulrush.htm, Version 16JUL97 Access in July 2012)

  • Kavamura VN, Esposito E (2010) Biotechnological strategies applied to the decontamination of soils polluted with heavy metals. Biotechnol Adv 28:61–69. doi:10.1016/j.biotechadv.2009.09.002

    Article  CAS  Google Scholar 

  • Leita L, De Nobili M, Mondini C, Baca García MT (1993) Response of Leguminosae to cadmium exposure. J Plant Nutrition 16:2001–2012. doi:10.1080/01904169309364670

    Article  CAS  Google Scholar 

  • Lillebø AI, Flindt AC, Pardal M, Neto J, Marques JC (2003) Salinity as the major factor affecting Scirpus maritimus annual dynamics. Evidence from field data and greenhouse experiment. Aquat Bot 77:111–120. doi:10.1016/S0304-3770(03)00088-3

    Article  Google Scholar 

  • Lillebø AI, Flindt MR, Pardal MA, Cardoso PG, Ferreira SM, Marques JC (2007) The faunal role in degradation of the common intertidal salt marsh plant Scirpus maritimus. Hydrobiologia 579:369–378. doi:10.1007/s10750-006-0535-z

    Article  Google Scholar 

  • Lillebø AI, Válega M, Otero M, Pardal MA, Pereira E, Duarte AC (2010) Daily and inter-tidal variations of Fe, Mn and Hg in the water column of a contaminated salt marsh: halophytes effect. Estuar Coast Shelf S88:91–98. doi:10.1016/j.ecss.2010.03.014

    Article  Google Scholar 

  • Lone MI, He Z, Stoffella PJ, Yang X (2008) Phytoremediation of heavy metal polluted soils and water: progresses and perspectives. J Zhejiang Univ Sci B Mar 9(3):1862–1783. doi:10.1631/jzus.B0710633

    Google Scholar 

  • Madejón P, Murillo JM, Marañón T, Espinar JL, Cabrera F (2006) Accumulation of As, Cd and selected trace elements in tubers of Scirpus maritimus L. from Doñana marshes (South Spain). Chemosphere 64:742–748. doi:10.1016/j.chemosphere.2005.11.032

    Article  Google Scholar 

  • Marchiol L, Leita L, Martin M, Peressotti A, Zeri G (1996) Physiological responses of two soyabean cultivars to cadmium. J Environ Qual 25:562–566. doi:10.2134/jeq1996.00472425002500030022x

    Article  CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. doi:10.1146/annurev.arplant.59.032607.092911

    Article  CAS  Google Scholar 

  • Neumann P (1997) Salinity resistance and plant growth revisited. Plant Cell Environ 20:1193–1198. doi:10.1046/j.1365-3040.1997.d01-139.x

    Article  CAS  Google Scholar 

  • Ololade IA, Ologundudu A (2007) Concentration and bioavailability of cadmium by some plants. AJB 6(16):1916–1921, ISSN 1684–5315

  • Ozawa T, Miura M, Fukuda M, Kakuta S (2009) Cadmium tolerance and accumulation in a halophyte Salicornia europaea as a new candidate for phytoremediation of saline soils. Scientific report of the Graduate School of Life and Environmental Sciences, Osaka Prefecture University, 60:1-8. http://hdl.handle.net/10466/8954

  • Pedro CA, Santos MS, Ferreira SM, Gonçalves SC (2013) The influence of cadmium contamination and salinity on the survival, growth and phytoremediation capacity of the saltmarsh plant Salicornia ramosissima. Mar Environ Res 92:197–205. doi:10.1016/j.marenvres.2013.09.018

    Article  CAS  Google Scholar 

  • Pereira P, Pablo H, Vale C, Franco V, Nogueira M (2009a) Spatial and seasonal variation of water quality in an impacted coastal lagoon (Óbidos Lagoon, Portugal). Environ Monit Assess 153:281–292. doi:10.1007/s10661-008-0355-x

    Article  CAS  Google Scholar 

  • Pereira P, Pablo H, Vale C, Rosa-Santos F, Cesário R (2009b) Metal and nutrient dynamics in a eutrophic coastal lagoon (Óbidos, Portugal): the importance of observations at different time scales. Environ Monit Assess 158:405–418. doi:10.1007/s10661-008-0593-y

    Article  CAS  Google Scholar 

  • Portuguese Decree Law 236/98, of 1 August 1998, establishing standards, criteria and quality objectives in order to protect the aquatic environment and improve the water quality, according to its main applications. J. Govern. Port. Repúb. D. Repúb. 176, 3676e3722

  • Reboreda R, Caçador I (2007) Halophyte vegetation influences in salt marsh retention capacity for heavy metals. Environ Pollut 146:147–154. doi:10.1016/j.envpol.2006.05.035

    Article  CAS  Google Scholar 

  • Riis T, Lambertini C, Oleseu B, Clayton JS, Brix H, Sonel BK (2010) Invasion strategies in clonal aquatic plants: are phenotypic differences caused by phenotypic plasticity or local adaptation? AnnBot 106:813–822. doi:10.1093/aob/mcq176

    CAS  Google Scholar 

  • Shuping, LS (2008). Biomonitoring of metal contamination in the lower Diep River, Milnerton, Western Cape. Dissertation submitted in fulfilment of the requirements for the degree M. Tech: Environmental Health In the Faculty of Applied Sciences at the Cape Peninsula University of Technology. http://hdl.handle.net/11189/412

  • Sousa AI, Lillebø AI, Pardal MA, Caçador I (2011) Influence of multiple stressors on the auto-remediation processes occurring in salt marshes. Mar Pollut Bull 62:1584–1587. doi:10.1016/j.marpolbul.2011.04.025

    Article  CAS  Google Scholar 

  • U.S. Environmental Protection Agency, Method 3020A. Acid digestion of aqueous samples and extracts for total metals for analysis by GFAA Spectroscopy. Revision 1, July 1992; (http://www.epa.gov/osw/hazard/testmethods/sw846/pdfs/3020a.pdf access in July 2012)

  • Underwood AJ (1997) Chapter 4. Statistical tests of null hypotheses, 50-59. Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press

  • Weis J, Weis P (2004) Metal uptake, transport and release by wetland plants: implications for phytoremediation and restoration. Environ Int 30:685–700. doi:10.1016/j.envint.2003.11.002

    Article  CAS  Google Scholar 

  • Yilmaz DD (2007) Effects of salinity on growth and nickel accumulation capacity of Lemna gibba (Lemnaceae). J Hazard Mater 147:74–77. doi:10.1016/j.jhazmat.2006.12.047

    Article  CAS  Google Scholar 

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Acknowledgments

The authors gratefully acknowledge professors José Pestana and Carla Tecelão for their technical support in some steps of this work and all the colleagues at GIRM who assisted in the field and laboratory work. Also, the authors would like to acknowledge the two anonymous reviewers for their helpful comments on the early versions of this work. The research conducted complies with the current Portuguese Law.

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Correspondence to Sílvia C. Gonçalves.

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Santos, M.S.S., Pedro, C.A., Gonçalves, S.C. et al. Phytoremediation of cadmium by the facultative halophyte plant Bolboschoenus maritimus (L.) Palla, at different salinities. Environ Sci Pollut Res 22, 15598–15609 (2015). https://doi.org/10.1007/s11356-015-4750-x

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