Abstract
In several countries, mining generates a high volume of tailing deposits, significantly impacting on soils. One of the non-metallic elements found in high concentrations in mine tailings is sulphur (S), in the form of sulphide minerals, whose oxidation causes acid drainage and metal mobility. The absorption of S in plants cultivated in mine tailings has been scarcely investigated. The objective of this study was to evaluate the extent to which a commercial humic substances and a vegetable waste compost can enhance the phytoremediation capacity of Atriplex nummularia for S and metals (Cu, Mo) in mine tailings. The plants were cultivated for 120 days under greenhouse conditions in pots with mine tailings (MT), with the addition of vegetable waste compost (VC) and a commercial humic substance (HS) in a 5% dose (W/W). At the end of the assay, the concentration of S in the aerial parts of plants cultivated in mine tailings, without amendments, reached 19,538 ± 4554 mg kg−1, indicating a potential thiophore plant. In MT in which HS were applied, S and Cu concentration decreased significantly in aerial parts, while VC significantly increased Mo. The addition of HS generated significantly greater dry weight, reaching 11.55 ± 1.92 g in the aerial parts versus 2.08 ± 0.52 g in MT, which increased significantly S and Cu content in plant root and therefore favourable to phytostabilization. Regarding organic amendments, their chemical characteristics, availability, cost and quality in relation to organic matter are very important aspects for phytoremediation of mine tailings.
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References
Abrol, Y., & Ahmad, A. (2003). Sulphur in plants. Dordrecht: Kluwer Academic Publishers 398 p.
Acosta, J. A., Abbaspour, A., Martínez, G. R., Martínez-Martínez, S., Zornoza, R., Gabarrón, M., & Faz, A. (2018). Phytoremediation of mine tailings with Atriplex halimus and organic/inorganic amendments: A five-year field case study. Chemosphere, 204, 71–78. https://doi.org/10.1016/j.chemosphere.2018.04.027.
Adriano, D. C. (2001). Trace elements in terrestrial environments (2nd ed.). New York: Springer.
Aguilera, M., Mora, M., Borie, G., Peirano, P., & Zunino, H. (2002). Balance and distribution of sulphur in volcanic ash-derived soils in Chile. Soil Biology Biochemistry, 34, 1355–1361.
Alazzeh, A. Y., & Abu-Zanat, M. M. (2004). Impact of feeding saltbush (Atriplex sp.) on some mineral concentrations in the blood serum of lactating Awassi ewes. Small Ruminant Research, 54, 81–88. https://doi.org/10.1016/j.smallrumres.2003.09.007.
Alloway, B. J. (2010). Heavy metals in soils. In Trace Metals and Metalloids in Soil and Their Bioavailability (3rd ed.). New York: Springer.
Belkheiri, O., & Mulas, M. (2013). The effects of salt stress on growth, water relations and ion accumulation in two halophyte Atriplex species. Environmental and Experimental Botany, 86, 17–28. https://doi.org/10.1016/j.envexpbot.2011.07.001.
Bolan, N. S., Adriano, D. C., Kunhikrishnan, A., James, T., McDowell, R., & Senesi, N. (2011). Dissolved organic matter: biogeochemistry, dynamics, and environmental significance in soils. Advances in Agronom, 110, 1–74. https://doi.org/10.1016/B978-0-12-385531-2.00001-3.
Chowdhury, M., Kouno, K., Ando, T., & Nagaoka, T. (2000). Microbial biomass, S mineralization and S uptake by African millet from soil amended with various composts. Soil Biology and Biochemistry, 32, 845–852. https://doi.org/10.1016/S0038-0717(99)00214-X.
Clemente, R., & Bernal, M. P. (2006). Fractionation of heavy metals and distribution of organic carbon in two contaminated soils amended with humic acids. Chemosphere, 64, 1264–1273. https://doi.org/10.1016/j.chemosphere.2005.12.058.
Clemente, R., Walker, D. J., Pardo, T., Martínez-Fernández, D., & Bernal, M. P. (2012). The use of a halophytic plant species and organic amendments for the remediation of a trace elements-contaminated soil under semi-arid conditions. Journal of Hazardous Materials, 223–224, 63–71. https://doi.org/10.1016/j.jhazmat.2012.04.048.
Diaz, O., Tapia, Y., Pastene, R., Montes, S., Nuñez, N., Vélez, D., & Montoro, R. (2011). Total and bioavailable arsenic concentration in arid soils and its uptake by native plants. Bulletin of Environmental Contamination and Toxicology, 86, 666–669. https://doi.org/10.1007/s00128-011-0269-0.
Dold, B., & Fontboté, L. (2001). Element cycling and secondary mineralogy in porphyry copper tailings as a function of climate, primary mineralogy, and mineral processing. Journal of Geochem Exploration, 74, 3–55.
Dreesen D, Henson J (1996) Molybdenum uptake by 33 grass, forb and shrub species grown in molybdenum tailings and soil. In Proceedings High Altitude Revegetation Workshop No. 12 Edited by Warren R. Keammerer Colorado University pp 266-281.
Ernst, W. H. O. (1998). Sulphur metabolism in higher plants: potential for phytoremediation. Biodegradation, 9, 311–318.
Gil-Loaiza, J., White, S., Root, R., Solís-Dominguez, F., Hammond, C., Chorover, J., & Maier, R. (2016). Phytostabilization of mine tailings using compost-assisted direct planting: translating greenhouse results to the field. Sci Total Environ, 565, 451–461. https://doi.org/10.1016/j.scitotenv.2016.04.168.
Ginocchio, R. (1996). Cuantificación de la tolerancia al cobre y al sulfato en dos especies leñosas de Chile central. Revista Chilena de Historia Natural, 69, 413–424.
Havlin, J., Tisdale, S., Nelson, W., & Beaton, J. (2014). Soil fertility and fertilizers: an introduction to nutrient management (8th ed.). New Jersey: Pearson.
Kabata-Pendias, A. (2011). Trace elements in soils and plants. Boca Raton: CRC Press.
Kabata-Pendias A, Mukherjee A (2007) Trace elements from soil to human. Springer.
Kelm, U., Helle, S., Matthie, R., Morales, A. (2009). Distribution of trace elements in soils surrounding the El Teniente porphyry copper deposit, Chile: the influence of smelter emissions and a tailings deposit. Environmental Geology 57:365–376. https://doi.org/10.1007/s00254-008-1305-1.
Kossoff, D., Dubbin, W. E., Alfredsson, M., Edwards, S. J., Macklin, M. G., & Hudson-Edwards, K. A. (2014). Mine tailings dams: characteristics, failure, environmental impacts and remediation. Applied Geochemistry, 51, 229–245. https://doi.org/10.1016/j.apgeochem.2014.09.010.
Lachica, M., Aguilar, A., & Yañez, J. (1973). Análisis foliar. Métodos analíticos utilizados en la Estación Experimental del Zaidín. Anal Edafol Agrobiol, 32, 1033–1047.
Lam, E., Cánovas, M., Gálvez, M., Montofré, I. L., Keith, B. F., & Faz, A. (2017). Evaluation of the phytoremediation potential of native plants growing on a copper mine tailing in northern Chile. Journal of Geochemical Exploration, 182, 210–217. https://doi.org/10.1016/j.gexplo.2017.06.015.
Lee, S., Ji, W., Lee, W., Koo, N., Koh, I., Kim, M., & Park, J. (2014). Influence of amendments and aided phytostabilization on metal availability and mobility in Pb/Zn mine tailings. Journal of Environmental Management, 139, 15–21. https://doi.org/10.1016/j.jenvman.2014.02.019.
Lottermoser, B. G. (2010). Mine wastes. In Characterization, Treatment and Environmental Impacts (3rd ed.). New York: Springer.
Maggioni A, Varanini Z, Nardi S, Pinton R (1987) Actino of soil humic matter on plant roots: Stimulation of ion uptake and effect on (Mg2+ K+) ATPase activity. 62: 355-363. Science of the Total Environment (87) 90522-5 https://doi.org/10.1016/0048-9697
Martínez-Martínez, S., Zornoza, R., Gabarrón, M., Gómez-Garrido, M., Rosales, R., Muñoz, M., Gómez-López, M., Soriano-Disla, J., Faz, A., & Acosta, J. (2019). Is aided phytostabilization a suitable technique for the remediation of tailings? European Journal of Soil Science, 70, 862–875. https://doi.org/10.1111/ejss.12727.
Mateos-Naranjos, E., Andrades-Moreno, L., Cambrollé, J., & Perez-Martin, A. (2013). Assessing the effect of copper on growth, copper accumulation and physiological responses of grazing species of Atriplex halimus: ecotoxicological implications. Ecotox Environ Safe, 90, 136–142. https://doi.org/10.1016/j.ecoenv.2012.12.020.
McGrath, S. P., Micó, C., Curdy, R., & Zhao, F. J. (2010). Predicting molybdenum toxicity to higher plants: Influence of soil properties. Environmental Pollution, 158, 3095–3102. https://doi.org/10.1016/j.envpol.2010.06.027.
Mendez, M., & Maier, R. (2008a). Phytoremediation of mine tailings in temperate and arid environments. Reviews in Environmental Science and Biotechnology, 7, 47–59. https://doi.org/10.1007/s11157-007-9125-4.
Mendez, M., & Maier, R. (2008b). Phytostabilization of mine tailings in arid and semiarid environments an emerging remediation technology. Environmental Health Perspectives, 278–283.
Moreno-Jiménez, E., Esteban, E., Fresno, T., López, C., & Peñalosa, J. M. (2010). Hydroponics as valid tool to assess arsenic availability in mine soils. Chemosphere, 79, 513–517. https://doi.org/10.1016/j.chemosphere.2010.02.034.
Nelson, D. W., Sommers L. E. (1982). Total carbon, and organic matter. In Methods of soil analysis. Page, A. L. (Eds). American Society of Agronomic, Inc., Soil Science Society of American, Inc., Publisher. Madison, Winconsin, USA, pp 571–573.
Nogales, R., Azcón, M., & Gallardo-Lara, F. (1985). Sequential sulphur availability affected by town refuse compost application. Biological Agriculture and Horticulture, 4, 323–328. https://doi.org/10.1080/01448765.1985.9754446.
Norman, H. C., Masters, D. G., & Barret-Lennard, E. (2013). Halophytes as forages in saline ladnscapes: interactions between plant fenotype and environment change their feeding value to ruminants. Environmental and Experimental Botany, 92, 96–109. https://doi.org/10.1016/j.envexpbot.2012.07.003.
Osmond, C. B., Björkman, O., & Anderson, D. J. (1980). Physiological processes in plant ecology. Toward a synthesis with Atriplex. Berlin Heidelberg: Springer-Verlag.
Oyarzún, J., Oyarzun, R., Lillo, J., Higueras, P., Maturana, H., & Oyarzún, R. (2016). Distribution of chemical elements in calc-alkaline igneous rocks, soils, sediments and tailings deposits in northern Central Chile. Journal of South American Earth Sciences, 69, 25–42. https://doi.org/10.1016/j.jsames.2016.03.004.
Pardo, T., Bernal, M., & Clemente, R. (2017). Phytostabilisation of severely contaminated mining tailings using halophytes and field addition of organic and inorganic amendments. Chemosphere, 178, 556–564. https://doi.org/10.1016/j.chemosphere.2017.03.079.
Parraga-Aguado, I., Nazaret, M., Álvarez-Rogel, J., & Conesa, H. (2014). Assessment of the employment of halophyte plant species for the phytomanagement of mining tailings in semiarid areas. Ecological Engineering, 71, 598–604. https://doi.org/10.1016/j.ecoleng.2014.07.061.
Pérez-Esteban, J., Escolástico, C., Ruiz-Fernández, J., Masaguer, A., & Moliner, A. (2013). Bioavailability and extraction of heavy metals from contaminated soil by Atriplex halimus. Environmental and Experimental Botany, 88, 53–59. https://doi.org/10.1016/j.envexpbot.2011.12.003.
Reid N, Robson, T. C., Radcliffe, B., Verrall, M. (2016). Excessive sulphur accumulation and ionic storage behaviour identified in species of Acacia (Leguminosae: Mimosoideae). Annals of Botany 117, 653–666. https://doi.org/10.1093/aob/mcw009
Rodriguez J (1993) Manual de fertilización. Colección en Agricultura. Facultad de Agronomía. Pontificia Universidad Católica de Chile. Inscripción N° 84984. Santiago, pp 362.
Roletto, E., Barberis, R., Consiglio, M., & Jodice, R. (1985). Chemical parameters for evaluating compost maturity. Biocycle, 26, 46–47.
Romero, R., Plaza, C., Senesi, N., Nogales, R., & Polo, A. (2007). Humic acid-like fractions in raw and vermicomposted winery and distillery wastes. Geoderma, 139, 397–406. https://doi.org/10.1016/j.geoderma.2007.03.009.
Sadzawka A, Grez R, Carrasco M, Mora M (2004) Métodos de análisis de tejidos vegetales. Comisión de Normalización y Acreditación, Sociedad Chilena de la Ciencia del Suelo, Santiago, Chile. Instituto de Investigaciones Agropecuarias, Santiago, Chile. http://www.schcs.cl/comision-de-normalizacion-y-acreditacion-cna.html.
Sai, S., Ben, A., Jaffel, K., Leclerc, J. C., Rejeb, M. N., & Ouerghi, Z. (2011). Leaf–water relations and ion concentrations of the halophyte Atriplex hortensis in response to salinity and water stress. Acta Physiologiae Plantarum, 33, 335–342. https://doi.org/10.1007/s11738-010-0552-4.
Salem, H. B., Norman, H. C., Nefzaoui, A., Mayberry, D. E., Pearce, K. L., & Revell, D. K. (2010). Potential use of oldman saltbush (Atriplex nummularia Lindl.) in sheep and goat feeding. Small Ruminant Res, 91, 13–28. https://doi.org/10.1016/j.smallrumres.2009.10.017.
Santibáñez F. (2017). Atlas Agroclimático de Chile. Tomo III. ISBN 978-956-19-1047-8. Universidad de Chile. Fundación para la Innovación Agraria.
Santibáñez, C., Verdugo, C., & Ginocchio, R. (2008). Phytostabilization of copper mining tailings with biosolids: Implications for metal uptake and productivity of Lolium perenne. Sci Total Environ, 395, 1–10. https://doi.org/10.1016/j.scitotenv.2007.12.033.
Schnitzer M (1982) Organic matter characterization. In Methods of soil analysis. Page, A.L. Editor. American Society of Agronomic, Inc., Soil Science Society of American, Inc., Publisher. Madison, Winconsin, USA, pp. 581-584.
Senesi, N. (1989). Composted materials as organic fertilizers. Science of the Total Environment, 81(82), 521–542.
Skierszkan, E. K., Mayer, K. U., Weis, D., & Beckie, R. D. (2016). Molybdenum and zinc stable isotope variation in mining waste rock drainage and waste rock at the Antamina mine, Peru. Science of the Total Environment, 550, 103–113. https://doi.org/10.1016/j.scitotenv.2016.01.053.
Soler-Rovira, P., Madejón, E., Madejón, P., & Plaza, C. (2010). In situ remediation of metal-contaminated soils with organic amendments: role of humic acids in copper bioavailability. Chemosphere, 79, 844–849. https://doi.org/10.1016/j.chemosphere.2010.02.054.
Squella, N., Meneses, R., & Gutierrez, T. (1985). Evaluation of range browse under arid Mediterranean climate conditions. Agricultura Técnica (Chile), 45(4), 303–314 http://www.chileanjar.cl/m/journal.
Stevenson, F. J. (1994). Humus chemistry. New York: John Wiley and Sons Inc..
Tapia, Y., Cala, V., Eymar, E., Frutos, I., Gárate, A., & Masaguer, A. (2010). Chemical characterization and evaluation of composts as organic amendments for immobilizing cadmium. Bioresource Technology, 101, 5437–5443. https://doi.org/10.1016/j.biortech.2010.02.034.
Tapia, Y., Eymar, E., Gárate, A., & Masaguer, A. (2013a). Effect of citric acid on metals mobility in pruning wastes and biosolids compost and metals uptake in Atriplex halimus and Rosmarinus officinalis. Environmental Monitoring and Assessment, 185, 4221–4229. https://doi.org/10.1007/s10661-012-2863-y.
Tapia, Y., Diaz, O., Pizarro, C., Segura, S., Vines, M., Zúñiga, G., & Moreno-Jiménez, E. (2013b). Atriplex atacamensis and Atriplex halimus resist as contamination in pre-Andean soils (northern Chile). Science of the Total Environment, 450-451, 188–196. https://doi.org/10.1016/j.scitotenv.2013.02.021.
Tapia, Y., Diaz, O., Acuña, E., Casanova, M., Salazar, O., & Masaguer, A. (2016). Phytostabilization of arsenic in soils with plants of the genus Atriplex established in situ in the Atacama Desert. Environmental Monitoring and Assessment, 188, 235. https://doi.org/10.1007/s10661-016-5247-x.
Tapia, Y., Bustos, P., Salazar, O., Casanova, M., Castillo, B., Acuña, E., & Masaguer, A. (2017). Phytostabilization of Cu in mine tailings using native plant Carpobrotus aequilaterus and the addition of potassium humates. Journal of Geochemical Exploration, 183, 102–113. https://doi.org/10.1016/j.gexplo.2017.10.008.
Tapia, Y., Casanova, M., Castillo, B., Acuña, E., Covarrubias, J., Antilén, M., & Masaguer, A. (2019). Availability of copper inmine tailings with humic substance addition and uptake by Atriplex halimus. Environmental Monitoring and Assessment, 119, 650–662. https://doi.org/10.1007/s10661-019-7832-2.
Tipping E (2002) Cation binding by humic substances. Cambridge Environmental Chemistry Series 12 Cambridge University Press, N.Y., USA.
Touceda-González, M., Álvarez-López, V., Prieto-Fernández, Á., Rodríguez-Garrido, B., Trasar-Cepeda, C., Mench, M., Puschenreiter, M., Quintela-Sabarís, C., Macías-García, F., & Kidd, P. S. (2017). Aided phytostabilisation reduces metal toxicity, improves soil fertility and enhances microbial activity in Cu-rich mining tailings. Journal of Environmental Management, 186, 301–313. https://doi.org/10.1016/j.jenvman.2016.09.019.
Verdugo, C., Sánches, P., Santibañez, C., Urrestarazu, P., Bustamante, E., Silva, Y., Gourdon, D., & Ginocchio, R. (2011). Efficacy of lime, biosolids and mycorrhiza for the phytostabilization of sulfidic Cu tailings in Chile: a greenhouse experiment. International Journal of Phytoremediation, 13, 107–125. https://doi.org/10.1080/15226510903535056.
Walker, D. J., Lutts, S., Sánchez-García, M., & Correal, E. (2014). Atriplex halimus L.: its biology and uses. Journal of Arid Environments, 100-101, 111–121. https://doi.org/10.1016/j.jaridenv.2013.09.004.
Watson, M. C., Banuelos, G. S., O’Leary, J. W., & Riley, J. J. (1994). Trace element composition of Atriplex grown with saline drainage water. Agriculture, Ecosystems & Environment, 48, 157–162.
Weil R, Brady NC, 2017. The nature and properties of soils. 5th. Pearson.
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This work was supported by the National Commission for Scientific and Technological Research (CONICYT) of the Ministry of Education Project FONDECYT REGULAR 1150513 (2015-2017) and Project PIA ANILLO ACM 170002 (2018-2020) Chile.
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Tapia, Y., Loch, B., Castillo, B. et al. Accumulation of Sulphur in Atriplex nummularia Cultivated in Mine Tailings and Effect of Organic Amendments Addition. Water Air Soil Pollut 231, 8 (2020). https://doi.org/10.1007/s11270-019-4356-x
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DOI: https://doi.org/10.1007/s11270-019-4356-x