Abstract
Besides the human need for mining activities, they contribute to environmental degradation in different ways, such as physical destruction of the environment, emission of dust containing toxic elements into the air, contamination of soils and aquatic environments by toxic elements, and dam collapses. In November 2015, the largest world’s iron mining disaster occurred in Mariana (Minas Gerais state, Brazil) and the environmental damage to the Atlantic Rainforest in that region was inestimable. Both Fe and Mn are commonly found in the same ore, and the Fe mining process extracts most of the Fe and discards all the Mn. In a way, even if Mn is considered inert in terms of health risk to plants and animals, high contents of this element, such as those observed in studies on the tailings of the Fundão dam, are of concern. There are even studies reporting that high concentrations of this plant micronutrient may cause physiological disorders in plants, which can further impact the recovery process in areas contaminated by tailings, using selected exotic species or naturally by native ones. We aimed to evaluate ecophysiological changes and growth-limiting factors in the native species Mucuna pruriens var. utilis (Wall. ex Wight) Baker ex Burck grown on tailings. Five new growth substrates were prepared by mixing different volumes of pure iron ore tailings from the Fundão dam with a fertile soil-substrate: 0 (control, fertile substrate), 25, 50, 75, and 100% tailings. We evaluated different physicochemical properties and mineral composition of the growth substrates. In plants, we also evaluated mineral composition and physiological traits as gas exchange, chlorophyll a fluorescence, carbohydrate and proline contents, dry mass, and superoxide dismutase activity. The most contrasting results were observed comparing the treatment control to the treatment with pure iron ore tailings, with a trend of intermediary results for the other treatments (25–75% tailings). The higher the tailings concentration, the more impaired was the growth. More than just to low tailings fertility, these results were related to the high concentrations of Mn found in substrates and plant leaf tissues. We also observed that photosynthesis was impaired through disturbances in photochemical and gas exchange parameters probably due to the high levels of Mn and the associate ionic imbalance it causes to the Fe/Mn ratio. Thus, more attention should be paid to Mn as an important environmental contaminant and new studies focused on how tailings (and probably Mn toxicity) may affect plant growth should also include histological, metabolic, and molecular approaches, as well as relating the assimilation and contents of Fe and Mn in roots, stem, and leaves.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Afridi MS et al (2022) New opportunities in plant microbiome engineering for increasing agricultural sustainability under stressful conditions. Front Plant Sci. https://doi.org/10.3389/fpls.2022.899464
Andrade GF et al (2018) Agricultural use of Samarco’s spilled mud assessed by rice cultivation: a promising residue use? Chemosphere. https://doi.org/10.1016/j.chemosphere.2017.11.099
Bates LS (1973) Rapid determination of free proline for water-stress studies. Plant Soil. https://doi.org/10.1007/BF00018060
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem. https://doi.org/10.1016/0003-2697(71)90370-8
Biancarosa I et al (2017) Amino acid composition, protein content, and nitrogen-to-protein conversion factors of 21 seaweed species from Norwegian waters. J Appl Phycol. https://doi.org/10.1007/s10811-016-0984-3
Chatzistathis TA et al (2010) Is chlorophyll fluorescence technique a useful tool to assess manganese deficiency and toxicity stress in olive plants? J Plant Nutr. https://doi.org/10.1080/01904167.2011.531362
Conama - Conselho Nacional do Meio Ambiente (2009) Resolução 420/2009. Dispõe sobre 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 atividade. Diário Oficial da União, 249, Brazil.
Cruz FV et al (2020) Does Samarco’s spilled mud impair the growth of native trees of the Atlantic Rainforest? Ecotoxicol Environ Saf. https://doi.org/10.1016/j.ecoenv.2019.110021
Cruz FV et al (2022) Fertilization assures mineral nutrition but does not overcome the effects of Fe accumulation in plants grown in iron ore tailings. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-021-16989-3
Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci. https://doi.org/10.3389/fenvs.2014.00053
Del Longo OT et al (1993) Antioxidant defences under hyperoxygenic and hyperosmotic conditions in leaves of two lines of maize with differential sensitivity to drought. Plant Cell Physiol. https://doi.org/10.1093/oxfordjournals.pcp.a078515
DuBois M et al (1956) Colorimetric method for determination of sugars and related substances. Anal Chem. https://doi.org/10.1021/ac60111a017
El-Jaoual T, Cox DA (1998) Manganese toxicity in plants. J Plant Nutr. https://doi.org/10.1080/01904169809365409
Esteves GF et al (2020) Do tailings from the Mariana, MG (Brazil), disaster affect the initial development of millet, maize, and sorghum? Environ Sci Pollut Res. https://doi.org/10.1007/s11356-020-10013-w
Estrada-Villegas S et al (2021) Lianas do not reduce tree biomass accumulation in young successional tropical dry forests. Oecologia. https://doi.org/10.1007/s00442-021-04877-z
Felizardo JP et al (2021) Sources of sedimentary organic matter and assessment of heavy-metal levels in estuarine sediments after Fundão dam breach. Estuar Coast Shelf Sci. https://doi.org/10.1016/j.ecss.2021.107507
Fernando DR, Lynch JP (2015) Manganese phytotoxicity: new light on an old problem. Ann Bot. https://doi.org/10.1093/aob/mcv111
Freitas JCE et al (2021) Does the water regime differentially modulate the responses to water stress in Lippia alba (Verbenaceae) genotypes with different ploidy levels? Ind Crops Prod. https://doi.org/10.1016/j.indcrop.2020.113137
García-Caparrós P et al (2021) Oxidative stress and antioxidant metabolism under adverse environmental conditions: a review. Bot Rev. https://doi.org/10.1007/s12229-020-09231-1
Giannopolitis CN, Ries SK (1977) Superoxide Dismutases: I. Occurrence in higher plants. Plant Physiol https://doi.org/10.1104/pp.59.2.309
Hati N et al (1979) Liming of acid soil: II—effect on plant available manganese and iron. J Indian Soc Soil Sci 27:394–398
Hu SH, Jinn TL (2022) Impacts of Mn, Fe, and oxidative stressors on MnSOD activation by AtMTM1 and AtMTM2 in Arabidopsis. Plants. https://doi.org/10.3390/plants11050619
Hu SH et al (2021) Significance of AtMTM1 and AtMTM2 for mitochondrial MnSOD activation in Arabidopsis. Front Plant Sci. https://doi.org/10.3389/fpls.2021.690064
Huang Y, Zhao L (2018) The effects of small particles on soil seismic liquefaction resistance: current findings and future challenges. Nat Hazards. https://doi.org/10.1007/s11069-018-3212-4
Huang H et al (2019a) Mechanisms of ROS regulation of plant development and stress responses. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00800
Huang H et al (2019b) Physiological responses of Broussonetia papyrifera to manganese stress, a candidate plant for phytoremediation. Ecotoxicol and Environ Saf. https://doi.org/10.1016/j.ecoenv.2019.05.063
Huang H et al (2020) Improvement of manganese phytoremediation by Broussonetia papyrifera with two plant growth promoting (PGP) Bacillus species. Chemosphere. https://doi.org/10.1016/j.chemosphere.2020.127614
Islam K, Murakami S (2021) Global-scale impact analysis of mine tailings dam failures: 1915–2020. Glob Environ Change. https://doi.org/10.1016/j.gloenvcha.2021.102361
Jordan DB, Ogren WL (1983) Species variation in kinetic properties of ribulose 1,5-bisphosphate carboxylase/oxygenase. Arch Biochem. https://doi.org/10.1016/0003-9861(83)90472-1
Kohno Y, Foy CD (1983) Manganese toxicity in bush bean as affected by concentration of manganese and iron in the nutrient solution. J Plant Nutr. https://doi.org/10.1080/01904168309363097
Lal MK et al (2022) From source to sink: mechanistic insight of photoassimilates synthesis and partitioning under high temperature and elevated [CO2]. Plant Mol Biol. https://doi.org/10.1007/s11103-022-01274-9
Lidon FC (2002) Rice plant structural changes by addition of excess manganese. J Plant Nutr. https://doi.org/10.1081/PLN-100108836
Longo RM et al (2011) Uso da adubação verde na recuperação de solos degradados por mineração na floresta amazônica. Bragantia 70:139–146. https://doi.org/10.1590/S0006-87052011000100020
Lowry OH et al (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
Mara Santana, R (2022) Funed-Pol - Coleção de lâminas de grãos de pólen. Version 1.91. Fundação Ezequiel Dias. Occurrence dataset
Marschner P (2012) Marschner’s Mineral Nutrition of Higher Plants. Elsevier
Matos LP et al. (2020) Limitations to use of Cassia grandis L. in the revegetation of the areas impacted with mining tailings from fundão dam. Water Air Soil Pollut https://doi.org/10.1007/s11270-020-04479-0
Millaleo R et al (2010) Manganese as essential and toxic element for plants: transport, accumulation and resistance mechanisms. J Soil Sci Plant Nutr. https://doi.org/10.4067/S0718-95162010000200008
Mittler R (2017) ROS are good. Trends Plant Sci. https://doi.org/10.1016/j.tplants.2016.08.002
Morgenstern N R et al. (2016) Fundão tailings dam review panel report on the immediate causes of the failure of the Fundão dam. Cleary Gottlieb Steen & Hamilton LLP.
Moura, TM (2022) Mucuna pruriens. Flora e Funga do Brasil. Jardim Botânico do Rio de Janeiro
Nunes FC et al (2022) Phytoremediation strategies for rehabilitation of soils affected by red mud: the Mariana tailing dam collapse (Minas Gerais, Brazil). Eurasian Soil Sci 55:673–685. https://doi.org/10.1134/S1064229322050052
Omachi CY et al (2018) Atlantic Forest loss caused by the world´s largest tailing dam collapse (Fundão Dam. Remote Sens Appl, Mariana, Brazil). https://doi.org/10.1016/j.rsase.2018.08.003
Pathania R et al (2020) An assessment of potential nutritive and medicinal properties of Mucuna pruriens: a natural food legume. 3 Biotech 10:1–15
Peixoto PHP et al (1999) Aluminum effects on lipid peroxidation and on the activities of enzymes of oxidative metabolism in sorghum. Braz J Plant Physiol 11:137–143
Queiroz HM et al (2021) Manganese: The overlooked contaminant in the world largest mine tailings dam collapse. Environ Int. https://doi.org/10.1016/j.envint.2020.106284
R core team, (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Austria
Rocha R et al (2021) Effects of the planting of legume species and soil conditions on the recovery of a sand and pebble mining area. Land Degrad Dev 32:1695–1705. https://doi.org/10.1002/ldr.3805
Rojas-Lillo Y et al (2013) Manganese toxicity and UV-B radiation differentially influence the physiology and biochemistry of highbush blueberry (Vaccinium corymbosum) cultivars. Functional Plant Biol. https://doi.org/10.1071/FP12393
Salo-Väänänen PP, Koivistoinen PE (1996) Determination of protein in foods: comparison of net protein and crude protein (N × 6.25) values. Food Chem. https://doi.org/10.1016/0308-8146(96)00157-4
Santos EF et al (2017) Physiological highlights of manganese toxicity symptoms in soybean plants: Mn toxicity responses. Plant Physiol Biochem. https://doi.org/10.1016/j.plaphy.2017.01.022
Schaefer, CEGR et al. (2016) Paisagens de Lama: Os Tecnossolos para recuperação ambiental de áreas afetadas pelo desastre da barragem do Fundão, em Mariana. In: A Ciência do solo e o desastre de Mariana. Sociedade Brasileira de Ciência do Solo, Viçosa, p. 44.
Silva DR et al (2022) Why is Brachiaria decumbens Stapf. a common species in the mining tailings of the Fundão dam in Minas Gerais, Brazil? Environ Sci Pollut Res. https://doi.org/10.1007/s11356-022-21345-0
Silva FC (2009) Manual de análises químicas de solos, plantas e fertilizantes. Embrapa Informação Tecnológica, Brasília.
Teixeira PC et al. (2017) Manual de métodos de análise de solo. Embrapa.
Weng XY et al (2013) Characteristics of the hyperaccumulator plant Phytolacca acinosa (Phytolaccaceae) in response to excess manganese. J Plant Nutr. https://doi.org/10.1080/01904167.2013.790428
Zago VCP et al (2019) Strategy for phytomanagement in an area affected by iron ore dam rupture: a study case in Minas Gerais State, Brazil. Environ Pollut. https://doi.org/10.1016/j.envpol.2019.03.060
Zhou J et al (2022) Mycorrhizal and rhizobial interactions influence model grassland plant community structure and productivity. Mycorrhiza 32:15–32. https://doi.org/10.1007/s00572-021-01061-2
Acknowledgements
The authors are very grateful to Fapemig and Capes for their financial support; to FINEP for the equipment used in the execution of this project; to the UFJF for financial and logistical support; and especially to those people affected by the disruption of the Fundão dam, for sharing their pain, experiences, and life histories.
Funding
This work was supported by the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (Fapemig) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes) [project CRA—APQ-01187–16, Call 04/2016—Technologies for the Recovery of the Rio Doce River Basin].
Author information
Authors and Affiliations
Contributions
JCEF: Conceptualization, Methodology, Formal analysis, Investigation, Writing—Original Draft, Writing—Review & Editing, Visualization. CFR: Conceptualization, Methodology, Investigation, Writing—Review & Editing, Supervision. MPP: Methodology, Investigation, Writing—Review & Editing. LMF: Methodology, Investigation, Writing—Review & Editing. PRCR: Methodology, Investigation, Writing—Review & Editing. JBM: Methodology, Investigation, Writing—Review & Editing. JCJS: Resources, Writing- Review & Editing, Funding acquisition. DEC: Resources, Writing- Review & Editing, Funding acquisition. FCN: Writing—Original Draft, Writing—Review & Editing, Supervision. PHPP: Conceptualization, Methodology, Resources, Writing—Original Draft, Writing—Review & Editing, Supervision, Project administration, Funding acquisition.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Freitas, J.C.E., de Resende, C.F., de Paula Pimenta, M. et al. Assessing the ecophysiological effects of iron mining tailings on velvet bean: implications for growth limitations based on mineral composition and physicochemical properties of tailings-soil substrates. Braz. J. Bot 46, 715–729 (2023). https://doi.org/10.1007/s40415-023-00911-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40415-023-00911-x