Using plants to remediate or manage metal-polluted soils: an overview on the current state of phytotechnologies
Resumo
Soil contamination by metals threatens both the environment and human health and hence requires remedial actions. The conventional approach of removing polluted soils and replacing them with clean soils (excavation) is very costly for low-value sites and not feasible on a large scale. In this scenario, phytoremediation emerged as a promising cost-effective and environmentally-friendly technology to render metals less bioavailable (phytostabilization) or clean up metal-polluted soils (phytoextraction). Phytostabilization has demonstrable successes in mining sites and brownfields. On the other hand, phytoextraction still has few examples of successful applications. Either by using hyperaccumulating plants or high biomass plants induced to accumulate metals through chelator addition to the soil, major phytoextraction bottlenecks remain, mainly the extended time frame to remediation and lack of revenue from the land during the process. Due to these drawbacks, phytomanagement has been proposed to provide economic, environmental, and social benefits until the contaminated site returns to productive usage. Here, we review the evolution, promises, and limitations of these phytotechnologies. Despite the lack of commercial phytoextraction operations, there have been significant advances in understanding phytotechnologies' main constraints. Further investigation on new plant species, especially in the tropics, and soil amendments can potentially provide the basis to transform phytoextraction into an operational metal clean-up technology in the future. However, at the current state of the art, phytotechnology is moving the focus from remediation technologies to pollution attenuation and palliative cares.
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Referências
Ali, H., Khan, E., & Sajad, M. A. (2013). Phytoremediation of heavy metals – concepts and applications. Chemosphere, 91, 869-881. DOI: 10.1016/j.chemosphere.2013.01.075
Araújo, P. R. M., Biondi, C. M., Nascimento, C. W. A., Silva, F. B. V., & Alvarez, A. M. (2019). Bioavailable and sequential extraction of Mercury in soils and organisms of a mangrove contaminated by a chlor-alkali plant. Ecotoxicology and Environmental Safety, 183, 1-10. DOI: 10.1016/j.ecoenv.2019.109469
Arwidsson, Z., Elgh-Dalgren, K., Kronhelm, T. von, Sjoberg, R., Allard, B., & Hees, P. van (2010). Remediation of heavy metal contaminated soil washing residues with amino polycarboxylic acids. Journal of Hazards Materials, 173(1-2), 697-704. DOI: 10.1016/j.jhazmat.2009.08.141
Bani, A., Echevarria, G., Sulçe, S., & Morel, J. L. (2015a). Improving the Agronomy of Alyssun murale for extensive phytomining: a five-year field study. International Journal of Phytoremediation, 17, 117-127. DOI: 10.1080/15226514.2013.862204
Bani, A., Echevarria, G., Zhang, X., Benizri, E., Laubie, B., Morel, J. L., & Simonnot, M. O. (2015b). The effect of plant density in nickel-phytomining field experiments with Alyssum murale in Albania. Australian Journal of Botany, 63, 72-77. DOI: 10.1071/BT14285
Bañuelos, G. S., Dhillon, K. S. (2011). Developing a sustainable phytomanagement strategy for excessive selenium in westtern United States and India. International Journal of Phytoremediation, 13, 208-228. DOI: 10.1080/15226514.2011.568544
Bañuelos, G. S., Arroyo, I. S., Dangi, S. R., & Zambrano, M. C. (2016). Continued selenium biofortification of carrots and broccoli grown in soils once amended with Se-enriched S. pinnata. Frontiers in Plant Science, 7, 1-11. DOI: 10.3389/fpls.2016.01251
Blaylock, M. J., Salt, D. E., Dushenkov, S., Zakharova, O., Gussman, C., Kapulnik, Y., … Raskin, I. (1997). Enhanced accumulation of Pb in India Mustard by soil-applied chelating agents. Environmental Science and Technology, 31(3), 860-865. DOI: 10.1021/es960552a
Braud, A. M., Gaudin, P., Hazotte, A., Guern, C. L., & Lebeau, T. (2019). Chelate-assisted phytoextraction of lead using Fagopyrum esculentum: laboratory vs. field experiments. International Journal of Phytoremediation, 21(11), 1-8. DOI: 10.1080/15226514.2019.1606778
Brooks, R. R., Reeves, R. D., Baker, A. J. M., Rizzo, J. A., & Diaz Ferreira, H. D. (1990). The brazilian serpentine plant expedition (BRASPEX), 1988. National Geographic Research, 6(20), 205-219. Retrieved from https://www.cabdirect.org/cabdirect/abstract/19911955337
Burges, A., Alkorta, I., Epelde, L., & Garbisu, C. (2018). From phytoremediation of soil contaminants to phytomanagement of ecosystem services in metal contaminated sites. International Journal of Phytoremediation, 20(4), 384-397. DOI: 10.1080/15226514.2017.1365340
Cerdeira-Pérez, A., Monterroso, C., Rodríguez-Garrido, B., Machinet, G., Echevarria, G., Prieto-Fernández, A., & Kidd, P. S. (2019). Implementing nickel phytomining in a serpentine quarry in NW Spain. Journal of Geochemical Exploration, 197, 1-13. DOI: 10.1016/j.gexplo.2018.11.001
Chalot, M., Girardclos, O., Ciadamidaro, L., Zappelini, C., Yung, L., Durand, A., ... Blaudez, D. (2020). Poplar rotation coppice at a trace element-contaminated phytomanagement site: a 10-year study revealing biomass production, element export and impact on extractable elements. Science of the Total Environment, 699, 1342060. DOI: 10.1016/j.scitotenv.2019.134260
Chaney, R. L., & Baklanov, I. A. (2017). Phytoremediation and phytomining: status and promise. Advances in Botanical Research, 83, 1-33. DOI: 10.1016/bs.abr.2016.12.006
Chaney, R. L., Malik, M., Li, Y. M., Brown, S. L., Brewer, E. P., Angle, J. S., & Baker, A. J. M. (1997). Phytoremediation of soil metals. Current Opinion in Biotechnology, 8, 279-284. DOI: 10.1016/s0958-1669(97)80004-3
Chen, Y., Li, X., & Shen, Z. (2004). Leaching and uptake of heavy metals by ten different species of plants during an EDTA-assisted phytoextraction process. Chemosphere, 57, 187-196. DOI: 10.1016/j.chemosphere.2004.05.044
Ciadamidaro, L., Parelle, J., Tatin-Froux, F., Moyen, C., Durand, A., Zappelini, C., ... Chalot, M. (2019). Early screening of new accumulating versus non-accumulating tree species for the phytomanagement of marginal lands. Ecological Engineering, 130, 147-156. DOI: 10.1016/j.ecoleng.2019.02.010
Cundy, A. B., Bardos, R. P., Puschenreiter, M., Mench, M., Bert, V., Friesl-Hanl, W., … Vangronsveld, J. (2016). Brownfields to green fields: realizing wider benefits from practical contaminant phytomanagement strategies. Journal of Environmental Management, 184, 67-77. DOI: 10.1016/j.jenvman.2016.03.028
Dickinson, N. M., Baker, A. J. M., Doronila, A., Laidlaw, S., & Reeves, R. D. (2009). Phytoremediation of inorganics: realism and synergies. International Journal of Phytoremediation, 11, 97-114. DOI: 10.1080/15226510802378368
Ent, A. van der, Baker, A. J. M., Reeves, R. D., Pollard, A. J., & Schat, H. (2013). Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant and Soil, 362, 319-334. DOI: 10.1007/s11104-012-1287-3
Ent, A. van der, Baker, A. J. M., Reeves, R. D., Chaney, R. L., Anderson, C. W. N., Meech, J. A., … Mulligan, D. R. (2015). Agromining: farming for metals in the future? Environmental Science and Technology, 49, 4773-4780. DOI: 10.1021/es506031u
Epelde, L., Burges, A., Mijangos, I., & Garbisu, C. (2014). Microbial properties and atributes of ecological relevance for soil quality monitoring during a chemical stabilization field study. Applied Soil Ecology, 75, 1-12. DOI: 10.1016/j.apsoil.2013.10.003
Ernst, W. H. O. (2005). Phytoextraction of mine wastes – options and impossibilities. Chemie der Erde Geochemistry, 65, 29-42. DOI: 10.1016/j.chemer.2005.06.001
Eugenio, N. R., McLaughlin, M., & Pennock, D. (2018). Soil pollution: a hidden reality. Rome, IT: FAO.
Evangelou, M. W. H., Conesa, H. M., Robinson, B. H., & Schulin, R. (2012). Biomass production on trace element-contaminated land: a review. Environmental Engineering Science, 29(9), 823-839. DOI: 10.1089/ees.2011.0428
Fassler, E., Robison, B. H., Stauffer, W., Gupta, S. K., Papritz, A., & Schulin, R. (2010). Phytomanagement of metal-contaminated agricultural land using sunflower, maize and tobacco. Agriculture, Ecosystems and Enviroment, 136, 49-58. DOI: 10.1016/j.agee.2009.11.007
Food and Agriculture Organization of the Unite Nations [FAO]. (2015). Status of the world’s soil resources – main report. Retrieved from http://www.fao.org/3/a-i5199e.pdf
Freitas, E. V., & Nascimento, C. (2016). Degradability of natural and synthetic agentes applied to a lead-contaminated soil. Journal of Soils and Sediments, 17, 1272-1278. DOI: 10.1007/s11368-015-1350-9
Freitas, E. V., Nascimento, C. W., & Silva, W. M. (2014). Citric acid-assisted phytoextraction of lead in the field: the use of soil amendments. Water, Air and Soil Pollution, 225(1796), 1-9. DOI: 10.1007/s11270-013-1796-6
Freitas, E. V., Nascimento, C. W., Souza, A., & Silva, F. B. (2013). Citric acid-assisted phytoextraction of lead: a field experiment. Chemosphere, 92(2), 213-217. DOI: 10.1016/j.chemosphere.2013.01.103
Freitas, E. V. S., Nascimento, C. W. A., Biondi, C. M., Silva, J. P. S., & Souza, A. P. (2009). Lead desorption and leaching in a Spodosol amended with chelant agents. Revista Brasileira de Ciência do Solo, 33(3), 517-525. DOI: 10.1590/S0100-06832009000300005
French, C. J., Dickinson, N. M., & Putwain, P. D. (2006). Woody biomass phytoremediation of contaminated brownfield land. Environmental Pollution, 141, 387-395. DOI: 10.1016/j.envpol.2005.08.065
Gil-Loaiza, J., White, S. A., Root, R. A., Solís-Dominguez, F. A., Hammond, C. M., Chorover, J., & Maier, R. M. (2016). Phytostabilization of mine tailings using compost-assisted direct planting: translating greenhouse results to the field. Science of the Total Environment, 565, 451-461. DOI: 10.1016/j.scitotenv.2016.04.168
Huang, J. W., Chen, J., Berti, W. R., & Cunningham, S. D. (1997). Phytoremediation of lead-contaminated soils: role of synthetic chelates in lead phytoextraction. Environmental Science and Technology, 31(3), 800-805. DOI: 10.1021/es9604828
Jacobs, A., Drouet, T., Sterckeman, T., & Noret, N. (2017). Phytoremediation of urban soils contaminated with trace metals using Noccaea caerulescens: comparing non-metallicolous populations to the metallicolous ‘Ganges’ in field trials. Environmental Science and Pollution Research, 24, 8176-8188. DOI: 10.1007/s11356-017-8504-9
Johansson, L., Xydas, C., Messios, N., Stoltz, E., & Greger, M. (2005). Growth and Cu accumulation by plants grown on Cu containing mine tailings in Cyprus. Applied Geochemistry, 20, 101-107. DOI: 10.1016/j.apgeochem.2004.07.003
Leclercq-Dransart, J., Demuynck, S., Waterlot, C., Bidar, G., Sahmer, K., Pernin, C., …Douay, F. (2019). Distribution of metals and cell wall compounds in leaf parts of three species suitable for the phytomanagement of heavy metal-contaminated soils. Water, Air and Soil Pollution, 230(237), 1-16. DOI: 10.1007/s11270-019-4290-y
Marques, A. P. G. C., Rangel, A. O. S. S., & Castro, P. M. L. (2009). Remediation of heavy metal contaminated soils: phytoremediation as a potentially promising clean-up technology. Critical Reviews in Environmental Science and Technology, 39, 622-654. DOI: 10.1080/10643380701798272
Marques, M. C., & Nascimento, C. W. A. (2013). Analysis of chlorophyll fluorescence spectra for the Monitoring of Cd toxicity in a bio-energy crop (Jatropha curcas). Journal of Photochemistry and Photobiology B: Biology, 127(5), 88-93. DOI: 10.1016/j.jphotobiol.2013.07.016
Martinez-Oró, D., Parraga-Aguado, I., Querejeta, J. I., & Conesa, H. M. (2017). Importance of intra- and interspecific plant interactions for the phytomanagement of semiarid mine tailings using the tree species Pinus halepensis. Chemosphere, 186, 405-413. DOI: 10.1016/j.chemosphere.2017.08.010
McGrath, S. P., Lombi, E., Gray, C. W., Caille, N., Dunham, S. J., & Zhao, F. J. (2006). Field evaluation of Cd and Zn phytoextraction potential by the hyperaccumulators Thlaspi caerulescens and Arabidopsis halleri. Environemntal Pollution, 141(1), 115-125. DOI: 10.1016/j.envpol.2005.08.022
Meers, E., Van Slycken, S., Adriaensen, K., Ruttens, A., Vangronsveld, J., Du Laing, G., … Tack, F. M. G. (2010). The use of bio-energy crops (Zea mays) for ‘phytoattenuation’ of heavy metals on moderately contaminated soils: a field experiment. Chemosphere, 78, 35-41. DOI: 10.1016/j.chemosphere.2009.08.015
Melo, E. E. C., Guilherme, L. R. G., Nascimento, C. W. A., & Penha, H. G. V. (2012). Availability and accumulation of arsenic in oilseeds grown in contaminated soils. Water, Air and Soil Pollution, 223, 233-240. DOI: 10.1007/s11270-011-0853-2
Nascimento, C. W. A., & Marques, M. C. (2018). Metabolic alterations and X-ray chlorophyll fluorescence for the early detection of lead stress in castor bean (Ricinus communis) plants. Acta Scientarum. Agronomy, 40, 1-9. DOI: 10.4025/actasciagron.v40i1.39392
Nascimento, C. W. A., Amarasiriwardena, D., & Xing, B. (2006). Comparison of natural organic acids and synthetic chelates at enhancing phytoextraction of metals from a multi-metal contaminated soil. Environmental Pollution, 140, 114-123. DOI: 10.1016/j.envpol.2005.06.017
Nascimento, C. W. A., Hesterberg, D., & Tappero, R. (2020a). Effects of exogenous citric acid on the concentrations and spatial distribution of Ni, Zn, Co, Cr, Mn and Fe in leaves of Noccaea caerulescens grown on a serpentine soil. Journal of Hazardous Materials, 398, 122992. DOI: 10.1016/j.jhazmat.2020.122992
Nascimento, C. W. A., Hesterberg, D., Tappero, R., Nicholas, S., & Silva, F. B. V. (2020b). Citric acid-assisted accumulation of Ni and other metals by Odontarrhena muralis: implications for phytoextraction and metal foliar distribution assessed by µ-SXRF. Environmental Pollution, 260, 114025. DOI: 10.1016/j.envpol.2020.114025
Nkrumah, P. N., Baker, A. J. M., Chaney, R. L., Erskine, P. D., Echevarria, G., Morel, J. L., & Ent, A. van der (2016). Current status and challenges in developing nickel phytomining: an agronomic perspective. Plant and Soil, 406, 55-69. DOI: 10.1007/s11104-016-2859-4
Pardo, T., Martínez-Fernández, D., Clemente, R., Walker, D. J., & Bernal, M. P. (2013). The use of olive-mill waste compost to promote the plant vegetation cover in a trace-element-contaminated soil. Environmental Science and Pollution Research, 21, 1029-1038. DOI: 10.1007/s11356-013-1988-z
Pierzynski, G. M., Sims, J. T., & Vance, G. F. (2005). Soils and environmental quality (3rd ed.). Boca Raton, FL: Taylor & Francis Group.
Pulford, I. D., & Watson, C. (2003). Phytoremediation of heavy metal-contaminated land by trees – a review. Environment International, 29, 529-540. DOI: 10.1016/S0160-4120(02)00152-6
Reeves, R. D., Baker, A. J. M., Jaffré, T., Erskine, P. D., Echevarria, G., & Ent, A. van der (2017). A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytologist, 218(2), 397-400. DOI: 10.1111/nph.14907
Regvar, M., Vogel-Mikuš, K., Kugonič, N., Turk, B., & Batič, F. (2006). Vegetational and mycorrhizal successions at a metal polluted site: indications for the direction of phytostabilisation? Environmental Pollution, 144, 976-984. DOI: 10.1016/j.envpol.2006.01.036
Resolução n. 420, de 28 de dezembro de 2009. (2009). Dispõe sobre os critérios e valores orientadores de qualidade do solo quanto à presença de substâncias químicas e estabelece diretrizes para o gerenciamento ambiental de áreas contaminadas por essas substâncias em decorrência de atividades antrópicas. Conselho Nacional do Meio Ambiente. Retrieved from http://www2.mma.gov.br/port/conama/legiabre.cfm?codlegi=620
Robinson, B. H., Bañuelos, G., Conesa, H. M., Evangelou, M. W. H., & Schulin, R. (2009). The phytomanagement of trace elements in soil. Critical Reviews in Plant Science, 28, 240-266. DOI: 10.1080/07352680903035424
Robinson, B. H., Green, S. R., Chancerel, B., Mills, T. M., & Clothier, B. E. (2007). Poplar for the phytomanagement of boron contaminated sites. Environmental Pollution, 150, 225-233. DOI: 10.1016/j.envpol.2007.01.017
Santini, T. C., & Fey, M. V. (2013). Spomtaneous vegetation encroachment upon bauxite residue (red mud) as an indicator and facilitator of in situ remediation processes. Environmental Science and Technology, 47, 12089-12096. DOI: 10.1021/es402924g
Schiavon, M., & Pilon-Smits, E. A. H. (2017). Selenium biofortification and phytoremediation phytotechnologies: a review. Journal of Environmental Quality, 46, 10-19. DOI: 10.2134/jeq2016.09.0342
Silva, F. B. V., Nascimento, C. W. A., Araújo, P. R. M., Silva, L. H. V., & Silva, R. F. (2016). Assessing heavy metal sources in sugarcane Brazilian soils: an approach using multivariate analysis. Environmental Monitoring and Assessment, 188(457), 1-12. DOI: 10.1007/s10661-016-5409-x
Silva, W. R., Silva, F. B. V., Araújo, P. R. M., & Nascimento, C. W. A. (2017). Assessing human health risks and strategies for phytoremediation in soils contaminated with As, Cd, Pb, and Zn by slag disposal. Ecotoxicology and Environmental Safety, 144, 522-530. DOI: 10.1016/j.ecoenv.2017.06.068
Simmons, R. W., Chaney, R. L., Angle, J. S., Kruatrachue, M., Klinphoklap, S., & Reeves, R. D. (2014). Towards practical cadmium phytoextraction with Noccaea caerulescens. International Journal of Phytoremediation, 17, 191-199. DOI: 10.1080/15226514.2013.876961
Šuman, J., Uhlík, O., Viktorová, J., & Macek, T. (2018). Phytoextraction of heavy metals: a promising tool for clean-up of polluted environment? Frontiers in Plant Science, 9, 1-15. DOI: 10.3389/fpls.2018.01476
Tlustoš, P., Břendová, K., Száková, J., Najmanová, J., & Koubová, K. (2016). The long-term variation of Cd and Zn hyperaccumulation by Noccaea spp and Arabidopsis halleri plants in both pot and field conditions. International Journal of Phytoremediation, 18(2), 110-115. DOI: 10.1080/15226514.2014.981243
Vangronsveld, J., Herzig, R., Weyens, N., Boulet, J., Adriaensen, K., Ruttens, A., … Mench, M. (2009). Phytoremediation of contaminated soils and groundwater: lessons from the field. Environmental Science and Pollution Research, 16, 765-794. DOI: 10.1007/s11356-009-0213-6
Vassil, A. D., Kapulnik, Y., Raskin, I., & Salt, D. E. (1998). The role of EDTA in lead transport and accumulation by indian mustard. Plant Physiology, 117, 447-453. DOI: 10.1104/pp.117.2.447
Wan, X., Lei, M., Chen, T., Tan, Y., & Yang, J. (2017). Safe utilization of heavy-metal-contaminated farmland by mulberry tree cultivation and silk production. Science of the Total Environment, 599, 1867-1873. DOI: 10.1016/j.scitotenv.2017.05.150
Zago, V. C. P., Dores, N. C., & Watts, B. A. (2019). Strategy for phytomanagement in an area affected by iron ore dam rupture: a study case in Minas Gerais State, Brazil. Environmental Pollution, 249, 1029-1037. DOI: 10.1016/j.envpol.2019.03.060
Zgorelec, Z., Bilandzija, N., Knez, K., Galic, M., & Zuzul, S. (2020). Cadmium and mercury phytostabilization from soil using Miscanthus×giganteus. Scientific Reports, 10(6685), 1-10. DOI: 10.1038/s41598-020-63488-5
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