Acessibilidade / Reportar erro

Ultramafic soils and nickel phytomining opportunities: A review

ABSTRACT

Ultramafic soils are originated from ultramafic rocks such as peridotite and serpentinite and are highly enriched in metals (e.g., Ni, Cr, and Co) and depleted in plant nutrients (e.g., P, K, and Ca). Such characteristics make these soils unfavorable for agriculture and have raised environmental concerns on metal release to the environment. From another perspective, ultramafic soils host a diverse flora with higher endemism than surrounding non-ultramafic areas, which has provided scientists with an opportunity to investigate the evolutionary genetics of plant adaptation. Some plant species adapted to these stressful edaphic conditions developing the ability to accumulate uncommonly high metal concentrations in the harvestable biomass. Such species, called metal hyperaccumulators, can extract metals from ultramafic soils, especially Ni, in a circular economy approach in which the metal-rich biomass is incinerated to generate valuable bio-ores. Phytomining promises to turn ultramafic soils and low-grade ore bodies into economically viable alternatives to metal extraction. Here, we review the current knowledge on ultramafic soils and the most promising hyperaccumulators used to exploit them in temperate and tropical climates. In the tropics, including Brazil, the search for new hyperaccumulator candidates for phytomining and the knowledge to crop these species is incipient and holds untapped opportunities. Despite the feasibility of the phytomining chain has been proven, large-scale demonstrations of profitability are needed to establish the technology.

phytoextraction; serpentine soils; soil fractionation; trace elements

INTRODUCTION

Ultramafic soils result from the weathering of ultramafic rocks, such as peridotite and serpentinite, which contains predominantly ferromagnesian silicate minerals and less than 45 % silica (SiO2) (Alexander, 2009Alexander EB. Soil and vegetation differences from peridotite to serpentinite. Northeast Nat. 2009;16:178-92. https://doi.org/10.1656/045.016.0515
https://doi.org/10.1656/045.016.0515...
; Alfaro et al., 2015Alfaro MR, Montero A, Ugarte OM, Nascimento CWA, Accioly AMA, Biondi CM, Silva YJAB. Background concentrations and reference values for heavy metals in soils of Cuba. Environ Monit Assess. 2015;187:4198. https://doi.org/10.1007/s10661-014-4198-3
https://doi.org/10.1007/s10661-014-4198-...
; Galey et al., 2017Galey ML, van der Ent A, Iqbal MCM, Rajakaruna N. Ultramafic geoecology of South and Southeast Asia. Bot Stud. 2017;58:18. https://doi.org/10.1186/s40529-017-0167-9
https://doi.org/10.1186/s40529-017-0167-...
). Peridotite is an ultramafic igneous rock containing olivines and pyroxenes with minor amounts of chromite. Serpentinite, in turn, is produced from peridotite by the addition of water in a metamorphic process called serpentinization. The complete transformation of peridotite into serpentinite requires about 13-14 % water (Alexander and DuShey, 2011Alexander EB, DuShey J. Topographic and soil differences from peridotite to serpentinite. Geomorphology. 2011;135:271-6. https://doi.org/10.1016/j.geomorph.2011.02.007
https://doi.org/10.1016/j.geomorph.2011....
). In the process, olivines and pyroxenes are transformed into or replaced by serpentine minerals such as lizardite, chrysotile, and antigorite, with the formula X3Si2O5(OH)4, in which X can represent Mg, Fe, Ni, Mn, Al, and Zn (Alexander and DuShey, 2011Alexander EB, DuShey J. Topographic and soil differences from peridotite to serpentinite. Geomorphology. 2011;135:271-6. https://doi.org/10.1016/j.geomorph.2011.02.007
https://doi.org/10.1016/j.geomorph.2011....
; Russell and Ponce, 2020Russell MJ, Ponce A. Six ‘must-have’ minerals for life’s emergence: Olivine, pyrrhotite, bridgmanite, serpentine, fougerite and mackinawite. Life. 2020;10:291. https://doi.org/10.3390/life10110291
https://doi.org/10.3390/life10110291...
). Because most ultramafic rocks (85-95 %) are serpentinized (Kodolányi et al., 2012Kodolányi J, Pettke T, Spandler C, Kamber BS, Ling KG. Geochemistry of ocean floor and fore-arc serpentinites: Constraints on the ultramafic input to subduction zones. J Petrol. 2012;53:237-70. https://doi.org/10.1093/petrology/egr058
https://doi.org/10.1093/petrology/egr058...
), ultramafic soils are commonly called serpentine, although the term is more accurately used to designate a group of minerals.

Phytomining is part of the so-called phytotechnologies, an umbrella term that includes plant-based techniques to extract, volatilize, or immobilize metals in contaminated soils (Nascimento et al., 2021Nascimento CWA, Biondi CM, Silva FBV, Lima LHV. Using plants to remediate or manage metal-polluted soils: An overview on the current state of phytotechnologies. Acta Sci-Agron. 2021;43:e58283. https://doi.org/10.4025/actasciagron.v43i1.58283
https://doi.org/10.4025/actasciagron.v43...
). Although the capacity of certain plants to hyper accumulate metals has been long known (Sachs, 1865Sachs J. Handbuch der Physiologischen Botanik. In: Hofmeister W, editor. Handbuch der Experimental-Physiologie der Pflanzen. Leipzig: Engelmann; 1865. v. IV. p. 153-4. https://www.biodiversitylibrary.org/item/197154#page/10/mode/1up.
https://www.biodiversitylibrary.org/item...
; Jaffré et al., 1976Jaffré T, Brooks RR, Lee J, Reeves RD. Sebertia acuminata: A hyperaccumulator of nickel from New Caledonia. Science. 1976;193:579-80. https://doi.org/10.1126/science.193.4253.579
https://doi.org/10.1126/science.193.4253...
), the plan of using such plants to remediate metal-polluted sites or to mine Ni, Co and other metals from metal-enriched soils and substrates was first proposed by Ruffus Chaney, a Research Agronomist at USDA (Chaney, 1983, 1998). These seminal publications boosted a large number of scientific papers with the words ‘phytoremediation’ (17,411) and ‘phytoextraction’ (4,615) on Web of Science search in the last 25 years (Figure 1). The keywords ‘phytomining’ and ‘agromining’ appeared 247 and 50 times in the same period, with an average of 19 and 11 references in the last five years, respectively. The concept of agromining is derived from phytomining to cover the agronomical chain that goes from the cultivation of hyperaccumulators to the production of bio-based metals (Morel, 2015Morel JL. Agromining: A new concept. In: Echevarria G, Morel JL, Simonnot MO, leaders. Workshop 3 “Agromining: From soils to refined metal products”. Nancy: SGA Biennial Meeting; 2015. p. 24-7. Available from: https://e-sga.org/nc/publications/sga-biennial-meetings-abstract-volumes/2015-nancy/.
https://e-sga.org/nc/publications/sga-bi...
).

Figure 1
Number of publications per year (1993-2020) and in the last 25 years (small square) on Web of Science search with the words ‘phytoremediation’, ‘phytoextraction’, ‘ultramafic soils’, ‘phytomining’, and ‘agromining’ in the article title, abstract or keywords.

The research in ‘ultramafic soils’ also significantly increased from an annual mean publication of 30 articles in the 1993-2010 span to 134 papers published yearly in the last decade (Figure 1). The genesis, chemistry, and flora of these types of soils have been extensively studied because of their unique biogeochemistry and promising opportunity to economically extract Ni, Co, Mn, and other metals (Garnier et al., 2009Garnier J, Quantin C, Guimarães E, Garg VK, Martins ES, Becquer T. Understanding the genesis of ultramafic soils and catena dynamics in Niquelândia, Brazil. Geoderma. 2009;151:204-14. https://doi.org/10.1016/j.geoderma.2009.04.020
https://doi.org/10.1016/j.geoderma.2009....
; Kierczak et al., 2016Kierczak J, Pedziwiatr A, Waroszewski J, Modelska M. Mobility of Ni, Cr and Co in serpentine soils derived on various ultrabasic bedrocks under temperate climate. Geoderma. 2016;268:78-91. https://doi.org/10.1016/j.geoderma.2016.01.025
https://doi.org/10.1016/j.geoderma.2016....
; Nkrumah et al., 2016Nkrumah PN, Baker AJM, Chaney RL, Erskine PD, Echevarria G, Morel JL, van der Ent A. Current status and challenges in developing nickel phytomining: An agronomic perspective. Plant Soil. 2016;406:55-69. https://doi.org/10.1007/s11104-016-2859-4
https://doi.org/10.1007/s11104-016-2859-...
; Vithanage et al., 2019Vithanage M, Kumarathilaka P, Oze C, Karunatilake S, Seneviratne M, Hseu ZY, Gunarathne V, Dassanayake M, Ok YS, Rinklebe J. Occurrence and cycling of trace elements in ultramafic soils and their impacts on human health: A critical review. Environ Int. 2019;131:104974. https://doi.org/10.1016/j.envint.2019.104974
https://doi.org/10.1016/j.envint.2019.10...
). Here, we discuss the chemistry, likely impacts on the environment, and ecological importance of ultramafic soils. In addition, the metal hyperaccumulation phenomenon, the search for new plant species able to mine ultramafic soils, and the process of recovering metals from ash biomass are reviewed. The recent advances in phytomining research have paved the way for the sustainable use of plants to produce metals, especially nickel, in a circular economy based on metal-rich soils and hyperaccumulating plants. However, some limitations remain and must be overcome to make phytomining a large-scale and economically feasible technology.

GEOCHEMISTRY OF ULTRAMAFIC SOILS

Ultramafic bedrocks and the soils developed from them have high concentrations of magnesium (Mg), iron (Fe), chromium (Cr), manganese (Mn), nickel (Ni), and cobalt (Co). Ultramafic outcrops occur in all continents and are estimated to cover roughly 3 % of the Earth’s surface (Guillot and Hatori, 2013), with significant massifs in temperate (Southern Europe, Turkey and California) and tropical settings (Cuba, New Caledonia, Brazil, The Philippines, Malaysia, Indonesia and Oman), and small and occasional patches worldwide (Galey et al., 2017Galey ML, van der Ent A, Iqbal MCM, Rajakaruna N. Ultramafic geoecology of South and Southeast Asia. Bot Stud. 2017;58:18. https://doi.org/10.1186/s40529-017-0167-9
https://doi.org/10.1186/s40529-017-0167-...
; Echevarria, 2018Echevarria G. Genesis and behaviour of ultramafic soils and consequences for nickel biogeochemistry. In:van der Ent A, Echevarria G, Baker AJM, Morel JL, editors. Agromining: Farming for metals. Extracting unconventional resources using plants. Cham: Springer; 2018. p. 135-56.; Kierczak et al., 2021Kierczak J, Pietranik A, Pędziwiatr A. Ultramafic geoecosystems as a natural source of Ni, Cr, and Co to the environment: A review. Sci Total Environ. 2021;755:142620. https://doi.org/10.1016/j.scitotenv.2020.142620
https://doi.org/10.1016/j.scitotenv.2020...
). Besides the high concentration of geogenic metals, especially the triad Cr-Ni-Co that can be toxic to plants, ultramafic soils pose a hostile environment for plant growth due to their scarcity of macronutrients such as nitrogen (N), phosphorus (P), potassium (K), or calcium (Ca) and micronutrients such as boron (B) or molybdenum (Mo), and low Ca-to-Mg molar ratios (Nkrumah et al., 2016Nkrumah PN, Baker AJM, Chaney RL, Erskine PD, Echevarria G, Morel JL, van der Ent A. Current status and challenges in developing nickel phytomining: An agronomic perspective. Plant Soil. 2016;406:55-69. https://doi.org/10.1007/s11104-016-2859-4
https://doi.org/10.1007/s11104-016-2859-...
; Nascimento et al., 2020Nascimento CWA, Hesterberg D, Tappero R, Nicholas S, Silva FBV. Citric acid-assisted accumulation of Ni and other metals by Odontarrhena muralis: Implications for phytoextraction and metal foliar distribution assessed by µ-SXRF. Environ Pollut. 2020;245:114025. https://doi.org/10.1016/j.envpol.2020.114025
https://doi.org/10.1016/j.envpol.2020.11...
). Therefore, the vegetation covering ultramafic soils is generally less massive and stunted than the vegetative cover of non-ultramafic soils (Figure 2).

Figure 2
Ultramafic soil landscape in Niquelândia, Brazil, shows the characteristically sparse and stunted vegetation compared to the vegetation of the non-ultramafic soil in the background. Photo by Clístenes Williams Araújo do Nascimento.

Ultramafic rocks in tropical countries commonly originate very deep, clayey, and highly weathered soils, with different serpentinization degrees and nickeliferous deposits formation as is the case in Brazil (Vidal-Torrado et al., 2006Vidal-Torrado P, Macias F, Calvo R, Carvalho SG, Silva AC. Genese de solos derivados de rochas ultramaficas serpentinizadas no sudoeste de Minas Gerais. Rev Bras Geocienc. 2006;30:523-41. https://doi.org/10.1590/S0100-06832006000300013
https://doi.org/10.1590/S0100-0683200600...
; Garnier et al., 2009Garnier J, Quantin C, Guimarães E, Garg VK, Martins ES, Becquer T. Understanding the genesis of ultramafic soils and catena dynamics in Niquelândia, Brazil. Geoderma. 2009;151:204-14. https://doi.org/10.1016/j.geoderma.2009.04.020
https://doi.org/10.1016/j.geoderma.2009....
; Vilela et al., 2019Vilela EF, Inda AV, Zinn YL. Soil genesis, mineralogy and chemical composition in a steatite outcrop under tropical humid climate in Brazil. Catena. 2019;183:104234. https://doi.org/10.1016/j.catena.2019.104234
https://doi.org/10.1016/j.catena.2019.10...
; Ratié et al., 2021Ratié G, Garnier J, Vieira LC, Araújo DF, Komárek M, Poitrasson F, Quantin C. Investigation of Fe isotope systematics for the complete sequence of natural and metallurgical processes of Ni lateritic ores: Implications for environmental source tracing. Appl Geochem. 2021;127:104930. https://doi.org/10.1016/j.apgeochem.2021.104930
https://doi.org/10.1016/j.apgeochem.2021...
). These soils likely develop into Ultisols, Nitosols, or Oxisols, with a predominance of 1:1 minerals and Fe oxides. However, less developed ultramafic soils (e.g., Cambisols and Entisols) can also occur, such as the ones derived from the Limoeiro deposit (Figure 3), which have easily weatherable minerals (e.g., olivine, orthopyroxene, and chromite). The Limoeiro deposit - located in a high-grade mobile belt of the Brasiliano orogenic cycle (650–500 Ma) – is originated by the orthopyroxenite-harzburgite intrusion of the Borborema Province, Northeast Brazil (Silva et al., 2013Silva JM, Ferreira Filho CF, Giustina MESD. The Limoeiro deposit: Ni-Cu-PGE sulfide mineralization hosted within an ultramafic tubular magma conduit in the Borborema Province, northeastern Brazil. Econ Geol. 2013;108:1753-71. https://doi.org/10.2113/econgeo.108.7.1753
https://doi.org/10.2113/econgeo.108.7.17...
).

Figure 3
Ultramafic soil profile (a) derived from serpentinized harzburgite-orthopyroxenite intrusion (b) of the Borborema Province (Santos et al., 2020Santos CA, Brito MFL, Pereira CS, Fernandes PR. Levantamento geológico e de potencial mineral de novas fronteiras: projeto Rio Capibaribe. Recife: Serviço Geológico do Brasil; 2020.) in Limoeiro, Pernambuco State, Brazil. Photo by Clístenes Williams Araújo do Nascimento.

The Ni, Cr, and Co concentrations found in ultramafic soils commonly exceed the soil guideline metal values set by environmental agencies to secure soil quality (Kanellopoulos, 2020Kanellopoulos C. Influence of ultramafic rocks and hot springs with travertine depositions on geochemical composition and baseline of soils. Application to eastern central Greece. Geoderma 2020;380:1146-9. https://doi.org/10.1016/j.geoderma.2020.114649
https://doi.org/10.1016/j.geoderma.2020....
; Yan et al., 2021Yan T, Wang X, Liu D, Chi Q, Zhou J, Xu J, Xu S, Zhang B, Nie L, Wang W. Continental-scale spatial distribution of chromium (Cr) in China and its relationship with ultramafic-mafic rocks and ophiolitic chromite deposit. Appl Geochem. 2021;126:104896. https://doi.org/10.1016/j.apgeochem.2021.104896
https://doi.org/10.1016/j.apgeochem.2021...
). Therefore, concerns have been raised about the potential of ultramafic rocks and their related soils to threaten the environment by releasing potentially toxic metals to groundwater, with consequences on animal and human health (Becquer et al., 2010Becquer T, Quantin C, Boudot JP. Toxic levels of metals in Ferralsols under natural vegetation and crops in New Caledonia. Eur Soil Sci. 2010;61:994-1004. https://doi.org/10.1111/j.1365-2389.2010.01294
https://doi.org/10.1111/j.1365-2389.2010...
; McClain et al., 2017McClain CN, Fendorf S, Webb SM, Maher K. Quantifying Cr(VI) production and export from serpentine soil of the California coast range. Environ Sci Technol. 2017;51:141-9. https://doi.org/10.1021/acs.est.6b03484
https://doi.org/10.1021/acs.est.6b03484...
; Vithanage et al., 2019Vithanage M, Kumarathilaka P, Oze C, Karunatilake S, Seneviratne M, Hseu ZY, Gunarathne V, Dassanayake M, Ok YS, Rinklebe J. Occurrence and cycling of trace elements in ultramafic soils and their impacts on human health: A critical review. Environ Int. 2019;131:104974. https://doi.org/10.1016/j.envint.2019.104974
https://doi.org/10.1016/j.envint.2019.10...
; Garnier et al., 2021Garnier J, Quantin C, Sophei R, Guimarães E, Becquer T. Field availability and mobility of metals in Ferralsols developed on ultramafic rock of Niquelândia, Brazil. Braz J Geol. 2021;51:e20200092. https://doi.org/10.1590/2317-4889202120200092
https://doi.org/10.1590/2317-48892021202...
). Ultramafic soils are probably the primary source of Ni and Co for the terrestrial ecosystem (Estrade et al., 2015Estrade N, Cloquet C, Echevarria G, Sterckeman T, Deng THB, Tang YT, Morel JL. Weathering and vegetation controls on nickel isotope fractionation in surface ultramafic environments (Albania). Earth Planet Sci Lett. 2015;423:24-5. https://doi.org/10.1016/j.epsl.2015.04.018
https://doi.org/10.1016/j.epsl.2015.04.0...
; Echevarria, 2018Echevarria G. Genesis and behaviour of ultramafic soils and consequences for nickel biogeochemistry. In:van der Ent A, Echevarria G, Baker AJM, Morel JL, editors. Agromining: Farming for metals. Extracting unconventional resources using plants. Cham: Springer; 2018. p. 135-56.), but Cr and Mn can also be released in significant amounts from ultramafic soils to groundwaters (Rajapaksha et al., 2013Rajapaksha AU, Vithanage M, Ok YS, Oze C. Cr(VI) formation related to Cr (III)-muscovite and birnessite interactions in ultramafic environments. Environ Sci Technol. 2013;47:9722-9. https://doi.org/10.1021/es4015025
https://doi.org/10.1021/es4015025...
; Papazotos et al., 2019Papazotos P, Vasileiou E, Perraki M. The synergistic role of agricultural activities in groundwater quality in ultramafic environments: The case of the Psachna basin, central Euboea, Greece. Environ Monit Assess. 2019;191:317. https://doi.org/10.1007/s10661-019-7430-3
https://doi.org/10.1007/s10661-019-7430-...
; Vithanage et al., 2014Vithanage M, Rajapaksha AU, Oze C, Rajakaruna M, Dissanayake CB. Metal release from serpentine soils in Sri Lanka. Environ Monit Assess. 2014;186:3415-29. https://doi.org/10.1007/s10661-014-3626-8
https://doi.org/10.1007/s10661-014-3626-...
).

Chromite (FeCr2O4) and other Cr minerals can be sources of the metal in ultramafic soils as Cr oxidation is induced by Fe, Mn, and dissolved organic matter (Rajapaksha et al., 2013Rajapaksha AU, Vithanage M, Ok YS, Oze C. Cr(VI) formation related to Cr (III)-muscovite and birnessite interactions in ultramafic environments. Environ Sci Technol. 2013;47:9722-9. https://doi.org/10.1021/es4015025
https://doi.org/10.1021/es4015025...
; McClain and Maher, 2016McClain CN, Maher K. Chromium fluxes and speciation in ultramafic catchments and global rivers. Chem Geol. 2016;426:135-57. https://doi.org/10.1016/j.chemgeo.2016.01.021
https://doi.org/10.1016/j.chemgeo.2016.0...
). For instance, Fantoni et al. (2002)Fantoni D, Brozzo G, Canepa M, Cipolli F, Marini L, Ottonello G, Zuccolini M. Natural hexavalent chromium in groundwaters interacting with ophiolitic rocks. Environ Geol. 2002;42:871-82. https://doi.org/10.1007/s00254-002-0605-0
https://doi.org/10.1007/s00254-002-0605-...
found Cr concentration in groundwaters of La Sapienza Province, Italy, above the maximum allowable concentration for drinking water; the authors attributed the high water Cr concentration to local serpentinites that release Cr through the oxidation of Cr(III) in the rock minerals to Cr(VI) by different electron acceptors (Mn and Fe oxides, H2O2, gaseous O2). The local ultramafic environment had no influence on the Cr, Ni, and Co concentrations in surface waters in Malaysia, but subsurface waters were highly enriched with these elements and exceeded water quality standards (Tashakor et al., 2018Tashakor M, Modabberi S, van der Ent A. Impacts of ultramafic outcrops in Peninsular Malaysia and Sabah on soil and water quality. Environ Monit Assess. 2018;190:333. https://doi.org/10.1007/s10661-018-6668-5
https://doi.org/10.1007/s10661-018-6668-...
). Groundwater contamination by metals released from ultramafic soils has also been reported in Mexico (Robles-Camacho and Armienta, 2000Robles-Camacho J, Armienta M. Natural chromium contamination of groundwater at Leon Valley, Mexico. J Geochem Explor. 2000;68:167-81. https://doi.org/10.1016/S0375-6742(99)00083-7
https://doi.org/10.1016/S0375-6742(99)00...
), Greece (Kaprara et al., 2015Kaprara E, Kazakis N, Simeonidis K, Coles S, Zouboulis AI, Samaras P, Mitrakas M. Occurrence of Cr(VI) in drinking water of Greece and relation to the geological background. J Hazard Mater. 2015;281:2-11. https://doi.org/10.1016/j.jhazmat.2014.06.084
https://doi.org/10.1016/j.jhazmat.2014.0...
), and the USA (McClain et al., 2017McClain CN, Fendorf S, Webb SM, Maher K. Quantifying Cr(VI) production and export from serpentine soil of the California coast range. Environ Sci Technol. 2017;51:141-9. https://doi.org/10.1021/acs.est.6b03484
https://doi.org/10.1021/acs.est.6b03484...
).

Bioavailability and mobility of metals in soils are governed by the geochemical pools in which they are bound (Silva et al., 2017Silva WR, Silva FBV, Araújo PRM, Nascimento CWA. Assessing human health risks and strategies for phytoremediation in soils contaminated with As, Cd, Pb, and Zn by slag disposal. Ecotox Environ Safe. 2017;144:522-30. https://doi.org/10.1016/j.ecoenv.2017.06.068
https://doi.org/10.1016/j.ecoenv.2017.06...
), which indicates that measuring the total concentrations of metals in soils does not suffice to assess environmental risks. Therefore, it is paramount to perform single and sequential extractions of metals in ultramafic soils to understand environmental risks better. For instance, ultramafic soils from Sri Lanka showed Ni (72 %; 4,697 mg kg-1) and Cr (83 %; 8,567 mg kg-1) predominantly associated with the residual fractions, with a remarkable association of Cr with soil organic matter (4.6 %; 508 mg kg-1), which can increase the metal mobility; Mn, in its turn, was evenly distributed between Fe-Mn oxides (37 %; 420 mg kg-1) and residual (31 %; 351 mg kg-1) fractions (Vithanage et al., 2014Vithanage M, Rajapaksha AU, Oze C, Rajakaruna M, Dissanayake CB. Metal release from serpentine soils in Sri Lanka. Environ Monit Assess. 2014;186:3415-29. https://doi.org/10.1007/s10661-014-3626-8
https://doi.org/10.1007/s10661-014-3626-...
). The DTPA-available contents of metals were 353 mg kg-1 (Ni), 76 mg kg-1 (Mn), and 0.35 mg kg-1 (Cr). Therefore, the ultramafic soils in the study area offer a highly labile source of metals.

We found that ultramafic soils from Brazil and the USA had different total and available Ni, Cr, and Co concentrations and that these metals were differently distributed into soil fractions (Table 1). The varied composition of the ultramafic soils may be partially due to complexes they form with other co-existing rocks such as gabbros, basalts, carbonates, and gneiss (Kierczak et al., 2021Kierczak J, Pietranik A, Pędziwiatr A. Ultramafic geoecosystems as a natural source of Ni, Cr, and Co to the environment: A review. Sci Total Environ. 2021;755:142620. https://doi.org/10.1016/j.scitotenv.2020.142620
https://doi.org/10.1016/j.scitotenv.2020...
). However, despite the diverse composition, all the ultramafic soils have in common the high Ni, Cr, and Co concentrations inherited and redistributed from the parent material during the soil-forming processes.

Table 1
Total and available Co, Cr, and Ni contents and percentage of these metals in exchangeable (Exc), organic matter (OM), iron and manganese oxides (Fe-Mn Ox), and residual fractions in ultramafic soils from Brazil and the USA

Regardless of the soil origin, Cr residual percentage was very high (~ 99 %), which is in agreement with other studies on ultramafic soils in temperate (Kierczak et al., 2016Kierczak J, Pedziwiatr A, Waroszewski J, Modelska M. Mobility of Ni, Cr and Co in serpentine soils derived on various ultrabasic bedrocks under temperate climate. Geoderma. 2016;268:78-91. https://doi.org/10.1016/j.geoderma.2016.01.025
https://doi.org/10.1016/j.geoderma.2016....
) and tropical (Tashakor et al., 2017Tashakor M, Hochwimmer B, Brearley FQ. Geochemical assessment of metal transfer from rock and soil to water in serpentine areas of Sabah (Malaysia). Environ Earth Sci. 2017;76:281. https://doi.org/10.1007/s12665-017-6585-x
https://doi.org/10.1007/s12665-017-6585-...
) countries. Nickel total concentrations and allocation in soil fractions were similar in Limoeiro (Brazil) and Buck Creek (USA) soils, but Ni availability measured by DTPA was considerably higher in the Limoeiro soil, which also had the highest Co availability. The soil from Niquelândia had the highest DTPA-available concentrations of Ni and Cr and the highest proportion of Ni in residual fractions. However, despite the apparently low mobility, Garnier et al. (2021)Garnier J, Quantin C, Sophei R, Guimarães E, Becquer T. Field availability and mobility of metals in Ferralsols developed on ultramafic rock of Niquelândia, Brazil. Braz J Geol. 2021;51:e20200092. https://doi.org/10.1590/2317-4889202120200092
https://doi.org/10.1590/2317-48892021202...
suggested that the ultramafic soils from Niquelândia are a source of labile Ni and Cr(VI), which can be transferred to surrounding sites either as dissolved metals or associated with Fe-oxides.

ULTRAMAFIC ECOSYSTEM

The unique chemistry of ultramafic soils often drives the evolution of endemic plant communities with morphological and physiological traits that differentiate them from the flora of bordering areas (Kazakou et al., 2008Kazakou E, Dimitrakopoulos PG, Baker AJM, Reeves RD, Troumbis AY. Hypotheses, mechanisms and trade-offs of tolerance and adaptation to ultramafic soils: From species to ecosystem level. Biol Rev. 2008;83:495-508. https://doi.org/10.1111/j.1469-185X.2008.00051.x
https://doi.org/10.1111/j.1469-185X.2008...
; Anacker, 2014Anacker BL. The nature of serpentine endemism. Am J Bot. 2014;101:219-24. https://doi.org/10.3732/ajb.1300349
https://doi.org/10.3732/ajb.1300349...
; Mesjasz-Przybyłowicz and Przybyłowicz, 2020Mesjasz-Przybyłowicz J, Przybyłowicz WJ. Ecophysiology of nickel hyperaccumulating plants from South Africa – from ultramafic soil and mycorrhiza to plants and insects. Metallomics. 2020;12:1018-35. https://doi.org/10.1039/c9mt00282k
https://doi.org/10.1039/c9mt00282k...
). For example, the diversity and spatial variability of ultramafic soils are considered the primary driver for the plant richness and distinctiveness of New Caledonia, which has >30 % of its territory covered by ultramafic outcrops (Jaffré et al., 2013Jaffré T, Pillon Y, Thomine S, Merlot S. The metal hyperaccumulators from New Caledonia can broaden our understanding of nickel accumulation in plants. Front Plant Sci. 2013;4:279. https://doi.org/10.3389/fpls.2013.00279
https://doi.org/10.3389/fpls.2013.00279...
; Mouly and Jeanson, 2015Mouly A, Jeanson M. Specialization to ultramafic substrates and narrow endemism of Cyclophyllum (Rubiaceae) in New Caledonia: Contribution of novel species to the un- derstanding of these singular patterns. Acta Bot Gallica. 2015;162:173-89. https://doi.org/10.1080/12538078.2015.1062799
https://doi.org/10.1080/12538078.2015.10...
; Isnard et al., 2016)Isnard S, L’huillier L, Rigault F, Jaffré T. How did the ultramafic soils shape the flora of the New Caledonian hotspot? Plant Soil. 2016;403:53-76. https://doi.org/10.1007/s11104-016-2910-5
https://doi.org/10.1007/s11104-016-2910-...
. In addition, the high endemism in ultramafic environments contributes greatly to investigating species genetic adaptation and evolutionary theory (von Wettberg and Wright, 2011Von Wettberg EJ, Wright JW. Genomic approaches to understanding adaptation. In: Harrison SP, Rajakaruna N, editors. Serpentine: The evolution and ecology of a model system. Berkeley: University of California Press; 2011. https://doi.org/10.1525/california/9780520268357.003.0006
https://doi.org/10.1525/california/97805...
; Strauss and Cacho, 2013Strauss SY, Cacho NI. Nowhere to run, nowhere to hide: The importance of enemies and apparency in adaptation to harsh soil environments. Am Nat. 2013;182:E1-E14. https://doi.org/10.1086/670754
https://doi.org/10.1086/670754...
; Palm and Van Volkenburgh, 2014)Palm ER, Van Volkenburgh E. Physiological adaptations of plants to serpentine soils. In: Rajakaruna N, Boyd RS, Harris TB, editors. Plant ecology and evolution in harsh environments. Hauppauge: Nova Science Publishers; 2014. p. 1-19..

Plant adaptation to ultramafic soils comprises a set of physiological traits, known as the ‘serpentine syndrome’, a term coined by the American soil scientist Hans Jenny to explain plant survival in these harsh environments. This syndrome includes tolerance to low nutrient contents, high Ni, Cr, and Co levels, Ca-to-Mg ratio imbalance, and water deficit (Isnard et al., 2016Isnard S, L’huillier L, Rigault F, Jaffré T. How did the ultramafic soils shape the flora of the New Caledonian hotspot? Plant Soil. 2016;403:53-76. https://doi.org/10.1007/s11104-016-2910-5
https://doi.org/10.1007/s11104-016-2910-...
; Nkrumah et al., 2016Nkrumah PN, Baker AJM, Chaney RL, Erskine PD, Echevarria G, Morel JL, van der Ent A. Current status and challenges in developing nickel phytomining: An agronomic perspective. Plant Soil. 2016;406:55-69. https://doi.org/10.1007/s11104-016-2859-4
https://doi.org/10.1007/s11104-016-2859-...
). Some species of the ultramafic flora developed the ability to hyper accumulate metals, but most of them deal with the toxicity by avoiding uptake or translocation of metals to shoots. For example, in some genera, Ni hyperaccumulation is found in one species while other related species growing on the same soils do not show such character (Burge and Barker, 2010Burge DO, Barker WR. Evolution of nickel hyperaccumulation by Stackhousia tryonii (Celastraceae), a serpentine-endemic plant from Queensland, Australia. Aust Syst Bot. 2010;23:415-30. https://doi.org/10.1071/SB10029
https://doi.org/10.1071/SB10029...
; Jaffré et al., 2013Jaffré T, Pillon Y, Thomine S, Merlot S. The metal hyperaccumulators from New Caledonia can broaden our understanding of nickel accumulation in plants. Front Plant Sci. 2013;4:279. https://doi.org/10.3389/fpls.2013.00279
https://doi.org/10.3389/fpls.2013.00279...
). Indeed, only 64 out of the 2145 species adapted to the ultramafic soils of New Caledonia are Ni hyperaccumulators (Jaffré et al., 2013Jaffré T, Pillon Y, Thomine S, Merlot S. The metal hyperaccumulators from New Caledonia can broaden our understanding of nickel accumulation in plants. Front Plant Sci. 2013;4:279. https://doi.org/10.3389/fpls.2013.00279
https://doi.org/10.3389/fpls.2013.00279...
).

It has been long suggested that Ni-hyperaccumulators drive a ‘nickel cycle’ resulting in the evolution of Ni-resistant microbial strains in the rhizosphere (Schlegel et al., 1991Schlegel HG, Cosson JP, Baker JM. Nickel hyperaccumulating plants provide a niche for nickel resistant bacteria. Bot Acta. 1991;104:18-25. https://doi.org/10.1111/j.1438-8677.1991.tb00189.x
https://doi.org/10.1111/j.1438-8677.1991...
; Mengoni et al., 2001Mengoni A, Barzanti R, Gonnelli C, Gabbrielli R, Bazzicalupo M. Characterization of nickel-resistant bacteria isolated from serpentine soil. Environ Microbiol. 2001;3:691-708. https://doi.org/10.1046/j.1462-2920.2001.00243.x
https://doi.org/10.1046/j.1462-2920.2001...
; Pal et al., 2004Pal A, Choudhuri P, Dutta S, Mukherjee PK, Paul AK. Isolation and characterization of nickel-resistant microflora from ultramafic soils of Andaman. World J Microbiol Biotechnol. 2004;20:881-6. https://doi.org/10.1007/s11274-004-2776-1
https://doi.org/10.1007/s11274-004-2776-...
). Studies on the microbial ecology of ultramafic soils showed a lower microbial density and activity than non-ultramafic soils but a higher number of metal-resistant microbial strains (Pal et al., 2004Pal A, Choudhuri P, Dutta S, Mukherjee PK, Paul AK. Isolation and characterization of nickel-resistant microflora from ultramafic soils of Andaman. World J Microbiol Biotechnol. 2004;20:881-6. https://doi.org/10.1007/s11274-004-2776-1
https://doi.org/10.1007/s11274-004-2776-...
, 2005Pal A, Dutta S, Mukherjee PK, Paul AK. Occurrence of heavy metal-resistance in microflora from ultramafic soil of Andaman. J Basic Microbiol. 2005;45:207-18. https://doi.org/10.1002/jobm.200410499
https://doi.org/10.1002/jobm.200410499...
). Also, the multiple metal-resistance of the isolates was associated with the resistance to the antibiotics penicillin, ampicillin, cycloserine (Pal et al., 2004Pal A, Choudhuri P, Dutta S, Mukherjee PK, Paul AK. Isolation and characterization of nickel-resistant microflora from ultramafic soils of Andaman. World J Microbiol Biotechnol. 2004;20:881-6. https://doi.org/10.1007/s11274-004-2776-1
https://doi.org/10.1007/s11274-004-2776-...
). In addition, inoculation with arbuscular mycorrhizal fungi (AMF) isolated from ultramafic soils could improve the nutrition and adaptation of plants to ultramafic soils, with potential benefits to agriculture and ecological restoration of mined ultramafic sites (Amir et al., 2013Amir H, Lagrange A, Hassaïne N, Cavaloc Y. Arbuscular mycorrhizal fungi from New Caledonian ultramafic soils improve tolerance to nickel of endemic plant species. Mycorrhiza. 2013;23:585-95. https://doi.org/10.1007/s00572-013-0499-6
https://doi.org/10.1007/s00572-013-0499-...
; Doubková et al., 2013Doubková P, Vlasáková E, Sudová R. Arbuscular mycorrhizal symbiosis alleviates drought stress imposed on Knautia arvensis plants in serpentine soil. Plant Soil. 2013;370:149-61. https://doi.org/10.1007/s11104-013-1610-7
https://doi.org/10.1007/s11104-013-1610-...
; Bourles et al., 2020Bourles A, Guentas L, Charvis C, Gensous S, Majorel C, Crossay T, Cavaloc Y, Burtet-Sarramegna V, Jourang P, Amir H. Co-inoculation with a bacterium and arbuscular mycorrhizal fungi improves root colonization, plant mineral nutrition, and plant growth of a Cyperaceae plant in an ultramafic soil. Mycorrhiza. 2020;30:121-31. https://doi.org/10.1007/s00572-019-00929-8.
https://doi.org/10.1007/s00572-019-00929...
).

The interaction between Ni-hyperaccumulators and insect species via herbivory may transfer Ni to these insects, which can contain relatively high Ni contents (Boyd and Martens, 1998Boyd RS, Martens SN. The significance of metal hyperaccumulation for biotic interactions. Chemoecology. 1998;8:1-7. https://doi.org/10.1007/s000490050002
https://doi.org/10.1007/s000490050002...
; Wall and Boyd, 2002Wall MA, Boyd RS. Nickel accumulation in serpentine arthropods from the Red Hills, California. Pan-Pac Entomol. 2002;78:168-76. https://archive.org/details/biostor-245415/mode/2up
https://archive.org/details/biostor-2454...
; Boyd, 2009Boyd RS. High-nickel insects and nickel hyperaccumulator plants: A review. Insect Sci. 2009;16:19-31. https://doi.org/10.1111/j.1744-7917.2009.00250.x
https://doi.org/10.1111/j.1744-7917.2009...
). Fifteen species of ‘high-Ni’ insects (Ni >500 µg g-1) have been identified in ultramafic areas in New Caledonia, South Africa, and the USA. The highest average Ni concentration found was 3500 µg g-1 for nymphs of a Stenoscepa species from South Africa (Boyd, 2009)Boyd RS. High-nickel insects and nickel hyperaccumulator plants: A review. Insect Sci. 2009;16:19-31. https://doi.org/10.1111/j.1744-7917.2009.00250.x
https://doi.org/10.1111/j.1744-7917.2009...
. Mesjasz-Przybyłowicz and Przybyłowicz (2020)Mesjasz-Przybyłowicz J, Przybyłowicz WJ. Ecophysiology of nickel hyperaccumulating plants from South Africa – from ultramafic soil and mycorrhiza to plants and insects. Metallomics. 2020;12:1018-35. https://doi.org/10.1039/c9mt00282k
https://doi.org/10.1039/c9mt00282k...
found some highly specialized phytophagous insects (leaf beetle Chrysolina pardalina, ladybird Epilachna cf nylanderi, and grasshopper Stenoscepa sp.) fed solely on Ni hyperaccumulators during their complete life cycle in lab conditions for generations with no adverse effect on their development. The investigation of such high-Ni insects in ultramafic ecosystems can aid in the understanding of Ni effects in organisms and how Ni moves through the food chain.

Despite their ecological relevance, endemic ultramafic communities worldwide face a high risk from climate change and anthropogenic activities, as their strict adaptation to ultramafic niches can limit the migration to other edaphic conditions (Harrison et al., 2009Harrison SP, Damschen E, Going BM. Climate gradients, climate change, and special edaphic floras. Northeast Nat. 2009;16:121-30. https://doi.org/10.1656/045.016.0510
https://doi.org/10.1656/045.016.0510...
). Consequently, some hyperaccumulators are at high risk of extinction (Reeves et al., 2017Reeves RD, Baker AJM, Jaffré T, Erskine PD, Echevarria G, van der Ent A. A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytol. 2017;218:407-11. https://doi.org/10.1111/nph.14907
https://doi.org/10.1111/nph.14907...
; Jaffré et al., 2018Jaffré T, Reeves RD, Baker AJM, Schat H, van der Ent A. The discovery of nickel hyperaccumulation in the New Caledonian tree Pycnandra acuminata 40 years on: An introduction to a Virtual Issue. New Phytol. 2018;218:397-400. https://doi.org/10.1111/nph.15105
https://doi.org/10.1111/nph.15105...
). For example, in Albania, climate change can decrease the area potentially explored by the Ni hyperaccumulator Alyssium murale by as much as 48 % by 2070 (Lekaj et al., 2019Lekaj E, Teqja Z, Bani A. The dynamics of land cover changes and the impact of climate change on ultramafic areas of Albania. Period Mineral. 2019;88:69-80. https://doi.org/10.2451/2019PM849
https://doi.org/10.2451/2019PM849...
). Likewise, in Brazil, the environmental degradation caused by mining activities can provoke a soaring extinction rate of plants endemic to metal-rich regions (Jacobi et al., 2011Jacobi CM, Carmo FF, Campos IC. Soaring extinction threats to endemic plants in Brazilian metal-rich regions. Ambio. 2011;40:540-3. https://doi.org/10.1007/s13280-011-0151-7
https://doi.org/10.1007/s13280-011-0151-...
; Salles et al., 2019Salles D, Carmo F, Jacobi C. Habitat loss challenges the conservation of endemic plants in mining-targeted brazilian mountains. Environ Conserv. 2019;46:140-6. https://doi.org/10.1017/S0376892918000401
https://doi.org/10.1017/S037689291800040...
).

In this scenario, ultramafic environments must be protected and their genetic material conserved for current and potential scientific and economic uses. To illustrate, plant species adapted to the high metal stress imposed in ultramafic soils could be helpful in metal tolerance studies, revegetation or reclamation of mined land, remediation of metal-polluted soils, micronutrient biofortification of crops, and phytomining of Ni-enriched soils or substrates (Jaffré et al., 2013Jaffré T, Pillon Y, Thomine S, Merlot S. The metal hyperaccumulators from New Caledonia can broaden our understanding of nickel accumulation in plants. Front Plant Sci. 2013;4:279. https://doi.org/10.3389/fpls.2013.00279
https://doi.org/10.3389/fpls.2013.00279...
; Nkrumah et al., 2016Nkrumah PN, Baker AJM, Chaney RL, Erskine PD, Echevarria G, Morel JL, van der Ent A. Current status and challenges in developing nickel phytomining: An agronomic perspective. Plant Soil. 2016;406:55-69. https://doi.org/10.1007/s11104-016-2859-4
https://doi.org/10.1007/s11104-016-2859-...
; Clemens, 2017Clemens S. How metal hyperaccumulating plants can advance Zn biofortification. Plant Soil. 2017;411:111-20. https://doi.org/10.1007/s11104-016-2920-3
https://doi.org/10.1007/s11104-016-2920-...
).

DEVELOPMENT AND CURRENT STATE OF PHYTOMINING

Hyperaccumulator species

Phytomining relies on the remarkable ability of certain plant species to naturally accumulate metal contents in shoots hundreds to thousands of times higher than other species growing on the same soil (van der Ent et al., 2013van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H. Hyperaccumulators of metal and metalloid trace elements: Facts and fiction. Plant Soil. 2013;362:319-34. https://doi.org/10.1007/s11104-012-1287-3
https://doi.org/10.1007/s11104-012-1287-...
). To date, the countries with the largest quantities of known hyperaccumulators are Cuba (Reeves et al., 1999Reeves RD, Baker AJM, Borhidi A, Berasaín R. Nickel hyperaccumulation in the serpentine flora of Cuba. Ann Bot. 1999;83:29-38. https://doi.org/10.1006/anbo.1998.0786
https://doi.org/10.1006/anbo.1998.0786...
; Berazaín et al., 2007Berazaín R, de la Fuente V, Rufo L, Rodríguez N, Amils R, Díez-Garretas B, Sánchez-Mata D, Asensi A. Nickel localization in tissues of different hyperaccumulator species of Euphorbiaceae from ultramafic areas of Cuba. Plant Soil. 2007;293:99-106. https://doi.org/10.1007/s11104-007-9227-3
https://doi.org/10.1007/s11104-007-9227-...
), New Caledonia (Jaffré et al., 2013Jaffré T, Pillon Y, Thomine S, Merlot S. The metal hyperaccumulators from New Caledonia can broaden our understanding of nickel accumulation in plants. Front Plant Sci. 2013;4:279. https://doi.org/10.3389/fpls.2013.00279
https://doi.org/10.3389/fpls.2013.00279...
), Turkey (Reeves and Adiguzel, 2008Reeves RD, Adiguzel N. The nickel hyperaccumulating plants of Turkey and adjacent areas: A review with new data. Turk J Biol. 2008;32:143-53.), Brazil (Reeves et al., 2007Reeves RD, Baker AJM, Becquer T, Echevarria G, Miranda ZJG. The flora and biogeochemistry of the ultramafic soils of Goias state, Brazil. Plant Soil. 2007;293:107-19. https://doi.org/10.1007/s11104-007-9192-x
https://doi.org/10.1007/s11104-007-9192-...
), and Malaysia (van der Ent et al., 2016van der Ent A, Echevarria G, Tibbett M. Delimiting soil chemistry thresholds for nickel hyperaccumulator plants in Sabah (Malaysia). Chemoecology. 2016;26:67-82. https://doi.org/10.1007/s00049-016-0209-x
https://doi.org/10.1007/s00049-016-0209-...
).

The threshold concentration that identifies the phenomenon of hyperaccumulation varies with the considered metal. For example, plants with more than 1,000 mg kg-1 of Ni in the dry leaf matter are considered hyperaccumulators of the element (the term ‘hypernickelophore’ is reserved to a subset of plants accumulating >10,000 mg kg-1 of Ni). The hyperaccumulation threshold for cadmium (Cd), thallium (Tl), and selenium (Se) is 100 mg kg-1. For cobalt (Co), chromium (Cr), and copper (Cu) above 300 mg kg-1; and zinc (Zn) and manganese (Mn) thresholds are 3,000 and 10,000 mg kg-1, respectively (van der Ent et al., 2015van der Ent A, Baker AJM, Reeves RD, Chaney RL, Anderson CWN, Meech JA, Erskine PD, Simonnot M-O, Vaughan J, Morel JL. Agromining: Farming for metals in the future. Environ Sci Technol. 2015;49:4773-80. https://doi.org/10.1021/es506031u
https://doi.org/10.1021/es506031u...
; Reeves et al., 2017)Reeves RD, Baker AJM, Jaffré T, Erskine PD, Echevarria G, van der Ent A. A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytol. 2017;218:407-11. https://doi.org/10.1111/nph.14907
https://doi.org/10.1111/nph.14907...
. Plants that reach such metal concentrations growing in hydroponics and spiked or chelator-treated soils are not considered hyperaccumulators. Currently, 746 plant species from 52 families and c. 130 genera are known to be hyperaccumulators of metals; Brassicaceae (83 species) and Phyllanthaceae (69 species) are the families most strongly represented (Reeves et al., 2017)Reeves RD, Baker AJM, Jaffré T, Erskine PD, Echevarria G, van der Ent A. A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytol. 2017;218:407-11. https://doi.org/10.1111/nph.14907
https://doi.org/10.1111/nph.14907...
. The vast majority of these species (532) are Ni-accumulators, followed by Cu (53), Co (42), Mn (42), Se (41), Zn (20) and Cd (7) (Corzo-Remigio et al., 2020)Corzo-Remigio A, Chaney RL, Baker AJM, Edraki M, Erskine PD, Echevarria G, van der Ent A. Phytoextraction of high value elements and contaminants from mining and mineral wastes: Opportunities and limitations. Plant Soil. 2020;449:11-37. https://doi.org/10.1007/s11104-020-04487-3
https://doi.org/10.1007/s11104-020-04487...
. Most field surveys for hyperaccumulators were carried out in ultramafic soils, mainly enriched in nickel. This fact and the market value for Ni are the likely reasons for the higher number of Ni hyperaccumulators discovered so far. Therefore, these species are the most studied and promising for commercial phytomining.

There is still a lack of systematic search for hyperaccumulators in several ultramafic regions, including Brazil, and new hyperaccumulators are certainly to be discovered in the coming years. For example, a recent systematic assessment of metal hyperaccumulators from New Caledonia using a portable XRF spectrometer (pXRF) revealed the existence of 34 new Ni-hyperaccumulators (Gei et al., 2020Gei V, Isnard S, Erskine PD, Echevarria G, Fogliani B, Jaffré T, van der Ent A. A systematic assessment of the occurrence of trace element hyperaccumulation in the flora of New Caledonia. Bot J Linn Soc. 2020;194:1-22. https://doi.org/10.1093/botlinnean/boaa029
https://doi.org/10.1093/botlinnean/boaa0...
). The pXRF screening of 7,300 herbarium specimens from Malaysia discovered 28 new Ni hyperaccumulators, 12 Co hyperaccumulators, and 51 Mn hyperaccumulators (van der Ent et al., 2019van der Ent A, Echevarria G, Pollard AJ, Erskine PD. X-ray fluorescence ionomics of herbarium collections. Sci Rep. 2019;9:4746. https://doi.org/10.1038/s41598-019-40050-6
https://doi.org/10.1038/s41598-019-40050...
). The tree species Blepharidium guatemalense was found to concentrate >4.0 % Ni in leaves when growing in soils of southeastern Mexico that are neither ultramafic nor Ni-contaminated through anthropogenic activities (Gutiérrez et al., 2021Gutiérrez DMN, Nkrumah PN, van der Ent A, Pollard J, Baker AJM, Torralba FN, Pons F, Sánchez MN, Hernández TG, Echevarria G. The potential of Blepharidium guatemalense for nickel agromining in Mexico and Central America. Int J Phytoremediat. 2021;23:1157-68. https://doi.org/10.1080/15226514.2021.1881039
https://doi.org/10.1080/15226514.2021.18...
). Such a surprisingly finding brought a new perspective for the search for hyperaccumulators beyond the ultramafic domains.

The potential of Brazil (and South America) for phytomining remains largely unexplored. The country is home to 33,951 native Angiosperms (18,793 endemics) and 26 native Gymnosperms (3 endemics), a plant species number greater than any other country (Jardim Botânico do Rio de Janeiro, 2021Jardim Botânico do Rio de Janeiro. Flora do Brasil 2020. Rio de Janeiro: Instituto de Pesquisas Jardim Botânico do Rio de Janeiro; 2021 [cited 2021 Jul 20]. Available from: http://floradobrasil.jbrj.gov.br/.
http://floradobrasil.jbrj.gov.br/...
). In addition, Brazil is one of the leaders in Ni production and third on the list of countries with the largest Ni reserves. Unfortunately, published systematic surveys of hyperaccumulators in Brazil are scarce and restricted to the ultramafic massifs of Macedo-Niquelândia and Barro Alto, Goiás State (Reeves et al., 2007Reeves RD, Baker AJM, Becquer T, Echevarria G, Miranda ZJG. The flora and biogeochemistry of the ultramafic soils of Goias state, Brazil. Plant Soil. 2007;293:107-19. https://doi.org/10.1007/s11104-007-9192-x
https://doi.org/10.1007/s11104-007-9192-...
; Pessoa-Filho et al., 2015Pessoa-Filho M, Barreto CC; Reis Junior FB, Fragoso RR, Costa FS, Mendes IC, Andrade LRM. Microbiological functioning, diversity, and structure of bacterial communities in ultramafic soils from a tropical savanna. A Van Leeuw J Microb. 2015;107:935-49. https://doi.org/10.1007/s10482-015-0386-6
https://doi.org/10.1007/s10482-015-0386-...
; Andrade et al., 2018Andrade LRM, Aquino FG, Miranda ZJG, Pereira CD, Reis Junior FB, Pessoa-Filho M, Oliveira-Filho EC, Nascimento CTC, Faleiro FG, Ramos AKB, Echevarria G. Native species of ultramafic massif of Barro Alto, GO, Brazil, can successfully be used to revegetate Ni mine spoil heaps. In: 21st World Congress of Soil Science, 12-14 August 2018; Rio de Janeiro. Viçosa, MG: Sociedade Brasileira de Ciência do Solo; 2018. Available from: https://ainfo.cnptia.embrapa.br/digital/bitstream/item/188857/1/Abstract-2561-final.pdf.
https://ainfo.cnptia.embrapa.br/digital/...
).

Reeves et al. (2007)Reeves RD, Baker AJM, Becquer T, Echevarria G, Miranda ZJG. The flora and biogeochemistry of the ultramafic soils of Goias state, Brazil. Plant Soil. 2007;293:107-19. https://doi.org/10.1007/s11104-007-9192-x
https://doi.org/10.1007/s11104-007-9192-...
collected 800 specimens from the ultramafic soils of Goiás, with more than 30 species showing Ni hyperaccumulation; some of them are shown in figure 4. Notable Ni-hyperaccumulators of this area include Pfaffia sarcophylla, Justicia lanstyakii, Heliotropium salicoides, and Lippia lupulina. However, the distribution of Ni concentrations in these species seems to be highly variable in the field. For example, we found Ni values measured by a pXRF in four specimens of P. sarcophylla growing in a hill nearby Niquelândia varying between 370 and 1,044 mg kg-1. Such a high variation among specimens is uncommon in other ultramafic plant surveys, in which the distinction between Ni hyperaccumulators and non-accumulators is clear (Reeves et al., 2007Reeves RD, Baker AJM, Becquer T, Echevarria G, Miranda ZJG. The flora and biogeochemistry of the ultramafic soils of Goias state, Brazil. Plant Soil. 2007;293:107-19. https://doi.org/10.1007/s11104-007-9192-x
https://doi.org/10.1007/s11104-007-9192-...
) and hence deserves studies. Nevertheless, field experiments are needed to assess Brazilian hyperaccumulators’ agronomical performance and profitability for phytomining programs.

Figure 4
Nickel hyperaccumulators growing on ultramafic soil in Niquelândia - GO, Brazil. From left to right: Lippia lupulina, Manihot sparsifolia, and Justicia lanstyakii. Photos by Clístenes Williams Araújo do Nascimento.

Agronomy of Ni phytomining

Although ultramafic soils can have high contents of other metals such as Cr, Mn, and Co, Ni phytomining has been the most promising approach so far because of the combination of good market value for Ni and a large number of Ni hyperaccumulators identified. Cobalt, for example, has higher value compared to Ni (Ni USD 18.7 kg-1 and Co USD 54.3 kg-1, London Metal Exchange, price for July 2021), but the foliar accumulation of Co and consequently the annual yield of the metal per hectare is much lower than Ni (van der Ent et al., 2018a; Nascimento et al., 2020Nascimento CWA, Hesterberg D, Tappero R, Nicholas S, Silva FBV. Citric acid-assisted accumulation of Ni and other metals by Odontarrhena muralis: Implications for phytoextraction and metal foliar distribution assessed by µ-SXRF. Environ Pollut. 2020;245:114025. https://doi.org/10.1016/j.envpol.2020.114025
https://doi.org/10.1016/j.envpol.2020.11...
). Despite that, the growing increase in the market price for metals, along with the discovery of new metal hyperaccumulators having enough high metal concentration in shoots and biomass yield, suggests that phytomining might be economically viable for other metals than Ni in the future. Case studies for other metals such as Co, Cu, Mn, Cd, and Zn can be found in van der Ent et al. (2018b).

Alyssum murale (syn Odontarrhena chalcidica), probably the most studied plant for phytomining to date (Tappero et al., 2007Tappero RV, Peltier E, Gräfe M, Heidel K, Ginder-Vogel M, Livi KJT, Rivers ML, Marcus MA, Chaney RL, Sparks DL. Hyperaccumulator Alyssum murale relies on a different metal storage mechanism for cobalt than for nickel. New Phytol. 2007;175:641-54. https://doi.org/10.1111/j.1469-8137.2007.02134.x.
https://doi.org/10.1111/j.1469-8137.2007...
; Chaney et al., 2007Chaney RL, Angle JS, Broadhurst CL, Peters CA, Tappero RV, Sparks DL. Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. J Environ Qual. 2007;36:1429-43. https://doi.org/10.2134/jeq2006.0514
https://doi.org/10.2134/jeq2006.0514...
; Bani et al., 2010Bani A, Pavlova D, Echevarria G, Mullaj A, Reeves RD, Morel JL, Sulce S. Nickel hyperaccumulation by species of Alyssum and Thlaspi (Brassicaceae) from the ultramafic soils of the Balkans. Botanica Servica. 2010;34:3-14., 2014Bani A, Echevarria G, Montargès-Pelletier E, Gjoka F, Sulçe S, Morel JL. Pedogenesis and nickel biogeochemistry in a typical Albanian ultramafic toposequence. Environ Monitor Assess. 2014;186:4431-44. https://doi.org/10.1007/s10661-014-3709-6
https://doi.org/10.1007/s10661-014-3709-...
; Nascimento et al., 2020Nascimento CWA, Hesterberg D, Tappero R, Nicholas S, Silva FBV. Citric acid-assisted accumulation of Ni and other metals by Odontarrhena muralis: Implications for phytoextraction and metal foliar distribution assessed by µ-SXRF. Environ Pollut. 2020;245:114025. https://doi.org/10.1016/j.envpol.2020.114025
https://doi.org/10.1016/j.envpol.2020.11...
), is regarded as the most promising Ni hyperaccumulator for temperate phytomining. This species has the ability to concentrate >1 % Ni in aerial tissues, high biomass and seeding rate, and ease of cropping (Bani et al., 2015a; Nkrumah et al., 2016Nkrumah PN, Baker AJM, Chaney RL, Erskine PD, Echevarria G, Morel JL, van der Ent A. Current status and challenges in developing nickel phytomining: An agronomic perspective. Plant Soil. 2016;406:55-69. https://doi.org/10.1007/s11104-016-2859-4
https://doi.org/10.1007/s11104-016-2859-...
; Cerdeira-Pérez et al., 2019)Cerdeira-Pérez A, Monterroso C, Rodríguez-Garrido B, Machinet G, Echevarria G, Prieto-Fernández A, Kidd PS. Implementing nickel phytomining in a serpentine quarry in NW Spain. J Geochem Explor. 2019;197:1-13. https://doi.org/10.1016/j.gexplo.2018.11.001
https://doi.org/10.1016/j.gexplo.2018.11...
. Because of these characteristics, technologies to potentially agromine ultramafic soils and clean up Ni-polluted soils using A. murale are economically feasible (Li et al., 2003Li YM, Chaney R, Brewer E, Rosenberg R, Angle JS, Baker A, Reeves R. Development of a technology for commercial phytoextraction of nickel: Economic and technical considerations. Plant Soil. 2003;249:107-15. https://doi.org/10.1023/A:1022527330401
https://doi.org/10.1023/A:1022527330401...
; Chaney et al., 2007Chaney RL, Angle JS, Broadhurst CL, Peters CA, Tappero RV, Sparks DL. Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. J Environ Qual. 2007;36:1429-43. https://doi.org/10.2134/jeq2006.0514
https://doi.org/10.2134/jeq2006.0514...
; Chaney and Baklanov, 2017)Chaney RL, Baklanov IA. Phytoremediation and phytomining: Status and promise. Adv Bot Res. 2017;83:189-221. https://doi.org/10.1016/bs.abr.2016.12.006
https://doi.org/10.1016/bs.abr.2016.12.0...
. In addition, a process for recovering Ni metal from A. murale biomass was developed (Barbaroux et al., 2011, 2Barbaroux R, Mercier G, Blais JF, Morel JL, Simonnot MO. A new method for obtaining nickel metal from the hyperaccumulator plant Alyssum Murale. Sep Purif Technol. 2011;83:57-65. https://doi.org/10.1016/j.seppur.2011.09.009
https://doi.org/10.1016/j.seppur.2011.09...
, 2012Barbaroux J, Plasari E, Mercier G, Simonnot MO, Morel JL, Blais JF. A new process for nickel ammonium disulfate production from ash of the hyperaccumulating plant Alyssum murale. Sci Total Environ. 2012;423:111-9. https://doi.org/10.1016/j.scitotenv.2012.01.063
https://doi.org/10.1016/j.scitotenv.2012...
).

Pioneering greenhouse and field studies to develop commercial phytomining were conducted in the USA using Streptanthus polygaloides, a Ni hyperaccumulator endemic to California (Nicks and Chamber, 1995) and Alyssum species (Li et al., 2003Li YM, Chaney R, Brewer E, Rosenberg R, Angle JS, Baker A, Reeves R. Development of a technology for commercial phytoextraction of nickel: Economic and technical considerations. Plant Soil. 2003;249:107-15. https://doi.org/10.1023/A:1022527330401
https://doi.org/10.1023/A:1022527330401...
; Chaney et al., 2007Chaney RL, Angle JS, Broadhurst CL, Peters CA, Tappero RV, Sparks DL. Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. J Environ Qual. 2007;36:1429-43. https://doi.org/10.2134/jeq2006.0514
https://doi.org/10.2134/jeq2006.0514...
). Nicks and Chamber (1995) found that S. polygaloides naturally growing on ultramafic soil containing 3,340 mg kg-1 of Ni produced biomass of 4.8 t ha-1 and averaged 5,300 mg kg-1 of Ni in shoots, with a Ni crop value of USD 476 ha-1. Phytomining would not be economically viable with this figure, so the Ni accumulation and biomass yield must be doubled. More promising results were reported by Li et al. (2003)Li YM, Chaney R, Brewer E, Rosenberg R, Angle JS, Baker A, Reeves R. Development of a technology for commercial phytoextraction of nickel: Economic and technical considerations. Plant Soil. 2003;249:107-15. https://doi.org/10.1023/A:1022527330401
https://doi.org/10.1023/A:1022527330401...
, who found that A. murale and Alyssum corsicum could accumulate over 20,000 mg kg-1 in shoots and yield biomass as high as 22 t ha-1, with up to two harvests per year. Under the price of Ni at the time this review was written, phytomining would have a crop value of approximately USD 7,480 ha-1 or BRL 38,715 (Brazilian reais) per harvest, making Ni phytomining a profitable phytotechnology. These values are far more than those attainable with commercial crops, especially on the Ni-toxic, unfertile ultramafic soils. By comparison, a corn crop yielding 5,500 kg ha-1(2020 average yield in Brazil) makes approximately USD 1,453 ha-1 (BRL 8,250) per harvest.

Commercial returns from phytomining decrease over time due to the gradual exhaustion of the Ni plant-available pool in the soil. However, the time frame for economic phytomining may be considerable (van der Ent et al., 2015van der Ent A, Baker AJM, Reeves RD, Chaney RL, Anderson CWN, Meech JA, Erskine PD, Simonnot M-O, Vaughan J, Morel JL. Agromining: Farming for metals in the future. Environ Sci Technol. 2015;49:4773-80. https://doi.org/10.1021/es506031u
https://doi.org/10.1021/es506031u...
). Considering that only 10 % of the 96 t ha-1 of the total Ni over 1 m depth of soil in Niquelândia (Table 2) will replenish the plant-available pool and a crop produces 100-200 kg ha-1 Ni, phytomining could be economically feasible for at least 48 years.

Although the high Ni accumulation and biomass yield of A. murale reported by Li et al. (2003)Li YM, Chaney R, Brewer E, Rosenberg R, Angle JS, Baker A, Reeves R. Development of a technology for commercial phytoextraction of nickel: Economic and technical considerations. Plant Soil. 2003;249:107-15. https://doi.org/10.1023/A:1022527330401
https://doi.org/10.1023/A:1022527330401...
have rarely been found in the literature, they are achievable with appropriated crop management. Liming, mineral and organic fertilization, weed control, bacteria inoculation, plant density, and improved cultivars can increase the Ni phytomining efficiency (Chaney et al., 2007Chaney RL, Angle JS, Broadhurst CL, Peters CA, Tappero RV, Sparks DL. Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. J Environ Qual. 2007;36:1429-43. https://doi.org/10.2134/jeq2006.0514
https://doi.org/10.2134/jeq2006.0514...
; Bani et al., 2015a,b; Hipfinger et al., 2021Hipfinger C, Rosenkranz T, Thüringer J, Puschenreiter M. Fertilization regimes affecting nickel phytomining efficiency on a serpentine soil in the temperate climate zone. Int J Phytoremediat. 2021;23:407-14. https://doi.org/10.1080/15226514.2020.1820446
https://doi.org/10.1080/15226514.2020.18...
) and should be considered in any commercial phytomining program and developed for the hyperaccumulator of interest. Also, combining A. murale cultivation with citric acid application to ultramafic soils increased Ni and other metals accumulation (Nascimento et al., 2020Nascimento CWA, Hesterberg D, Tappero R, Nicholas S, Silva FBV. Citric acid-assisted accumulation of Ni and other metals by Odontarrhena muralis: Implications for phytoextraction and metal foliar distribution assessed by µ-SXRF. Environ Pollut. 2020;245:114025. https://doi.org/10.1016/j.envpol.2020.114025
https://doi.org/10.1016/j.envpol.2020.11...
), but field studies are needed to confirm the potential observed in controlled conditions.

The first large-scale experiments assessing phytomining feasibility in Europe started in 2005 in Albania (Bani et al., 2007Bani A, Echevarria G, Sulce S, Morel JL, Mullai A. In-situ phytoextraction of Ni by a native population of Alyssum murale on an ultramafic site (Albania). Plant Soil. 2007;293:79-89. https://doi.org/10.1007/s11104-007-9245-1
https://doi.org/10.1007/s11104-007-9245-...
, 2018Bani A, Echevarria G, Pavlova D, Shallari S, Morel JL, Sulçe S. Element case studies: Nickel. In: van der Ent A, Echevarria G, Baker AJM, Morel JL, editors. Agromining: Farming for metals. Extracting unconventional resources using plants. Cham: Springer; 2018. p. 221-31.), a country with 11 % of its territory covered by ultramafic substrates (Lekaj et al., 2019Lekaj E, Teqja Z, Bani A. The dynamics of land cover changes and the impact of climate change on ultramafic areas of Albania. Period Mineral. 2019;88:69-80. https://doi.org/10.2451/2019PM849
https://doi.org/10.2451/2019PM849...
). These trials assessed the performance of A. murale growing on an ultramafic Vertisol during a five-year study in Pojske, Albania (Bani et al., 2015a). The crop value estimated for A. murale in Albania for a shoot Ni concentration of 11.5 mg kg-1 and a biomass yield of 9 t ha-1 (USD 1,055) was lower than obtained in the more intensive USA trials (Li et al., 2003Li YM, Chaney R, Brewer E, Rosenberg R, Angle JS, Baker A, Reeves R. Development of a technology for commercial phytoextraction of nickel: Economic and technical considerations. Plant Soil. 2003;249:107-15. https://doi.org/10.1023/A:1022527330401
https://doi.org/10.1023/A:1022527330401...
). However, Bani et al. (2015a) stated that such profit makes extensive commercial Ni phytomining feasible for the Balkans context owing to the low economic input and possibility of A. murale rotates with traditional crops.

Field studies on tropical Ni phytomining are scarce compared to those developed in the USA and Europe. However, the technology is potentially attractive as some of the top nickel-producing countries in 2020 (Indonesia, The Philippines, Brazil, New Caledonia, Cuba, and the Dominican Republic) are tropical. Nkrumah et al. (2019)Nkrumah PN, Tisserand R, Chaney RL, Baker AJM, Morel JL, Goudon R, Erskine PD, Echevarria G, van der Ent A. The first tropical ‘metal farm’: Some perspectives from field and pot experiments. J Geochem Explor. 2019;198:114-22. https://doi.org/10.1016/j.gexplo.2018.12.003
https://doi.org/10.1016/j.gexplo.2018.12...
carried out pot and field trials to establish the first ‘metal farm’ in the tropics, which took place in Sabah (Malaysia) using the hyperaccumulator Phyllanthus rufuschaneyi. The results of this large-scale demonstration of Ni phytomining were promising. The notably high Ni concentrations in leaves of P. rufuschaneyi grown in field conditions (up to 28,000 mg kg-1) and the high purity of the bio-ore generated show that phytomining can be economically attractive in Malaysia and other similar settings in the Asia-Pacific region. Countries in South America, the Caribbean, and Africa also hold untapped opportunities to develop commercial phytomining.

Transforming Ni hyperaccumulator biomass into valuable products

Nickel recovering from the dried biomass of hyperaccumulators is the final step in the phytomining chain. The extraction of Ni from the biomass is carried out by pyrometallurgical or hydrometallurgical processes. Pyrometallurgy includes three primary operations (calcination, prereduction, and smelting) followed by further raw material refining to remove impurities (Keskinkilic, 2019Keskinkilic E. Nickel laterite smelting processes and some examples of recent possible modifications to the conventional route. Metals. 2019;9:974. https://doi.org/10.3390/met9090974
https://doi.org/10.3390/met9090974...
). Hydrometallurgy, in turn, is the aqueous chemical processing of metals performed at relatively low temperatures through leaching, solution-phase upgrading, and purification of the recovered product (Simonnot et al., 2018Simonnot MO, Vaughan J, Laubie B. Processing of bio-ore to products. In: van der Ent A, Echevarria G, Baker AJM, Morel JL, editors. Agromining: Farming for metals. Extracting unconventional resources using plants. Cham: Springer; 2018. p. 39-52.). The raw material for these processes in the context of this review is the biomass of Ni hyperaccumulators, which can yield a bio-ore containing 10-25 % Ni, a figure much higher than the 1-2 % Ni in mined ores (Boominathan et al., 2004Boominathan R, Saha-Chaudhury NM, Sahajwalla V, Doran PM. Production of nickel bio-ore from hyperaccumulator plant biomass: Applications in phytomining. Biotechnol Bioeng. 2004;86:243-50. https://doi.org/10.1002/bit.10795.
https://doi.org/10.1002/bit.10795...
; van der Ent et al., 2015van der Ent A, Baker AJM, Reeves RD, Chaney RL, Anderson CWN, Meech JA, Erskine PD, Simonnot M-O, Vaughan J, Morel JL. Agromining: Farming for metals in the future. Environ Sci Technol. 2015;49:4773-80. https://doi.org/10.1021/es506031u
https://doi.org/10.1021/es506031u...
).

After drying and crushing of the plants, Ni can be thermally (with combustion) or chemically (without combustion) extracted from the biomass (Simonnot et al., 2018Simonnot MO, Vaughan J, Laubie B. Processing of bio-ore to products. In: van der Ent A, Echevarria G, Baker AJM, Morel JL, editors. Agromining: Farming for metals. Extracting unconventional resources using plants. Cham: Springer; 2018. p. 39-52.). The thermal approach can be performed by either feeding the plant ash into an existing smelter plant together with Ni sulfide and lateritic ores to produce ferronickel (Li et al., 2003Li YM, Chaney R, Brewer E, Rosenberg R, Angle JS, Baker A, Reeves R. Development of a technology for commercial phytoextraction of nickel: Economic and technical considerations. Plant Soil. 2003;249:107-15. https://doi.org/10.1023/A:1022527330401
https://doi.org/10.1023/A:1022527330401...
) or ashing the biomass in an electrical furnace followed by metal leaching (Barbaroux et al., 2011Barbaroux R, Mercier G, Blais JF, Morel JL, Simonnot MO. A new method for obtaining nickel metal from the hyperaccumulator plant Alyssum Murale. Sep Purif Technol. 2011;83:57-65. https://doi.org/10.1016/j.seppur.2011.09.009
https://doi.org/10.1016/j.seppur.2011.09...
), which seems more promising as the natural Ni purification made by plants is lost in the smelting process. In the chemical approach, dried and crushed biomass is directly acid leached to obtain a Ni-rich solution from where Ni is recovered (Barbaroux et al., 2011Barbaroux R, Mercier G, Blais JF, Morel JL, Simonnot MO. A new method for obtaining nickel metal from the hyperaccumulator plant Alyssum Murale. Sep Purif Technol. 2011;83:57-65. https://doi.org/10.1016/j.seppur.2011.09.009
https://doi.org/10.1016/j.seppur.2011.09...
, 2012Barbaroux J, Plasari E, Mercier G, Simonnot MO, Morel JL, Blais JF. A new process for nickel ammonium disulfate production from ash of the hyperaccumulating plant Alyssum murale. Sci Total Environ. 2012;423:111-9. https://doi.org/10.1016/j.scitotenv.2012.01.063
https://doi.org/10.1016/j.scitotenv.2012...
). However, leaching Ni from ashes is more efficient as Ni in the ash is 10 to 20 fold more concentrated than in plants (Zhang et al., 2016Zhang X, Laubie B, Houzelot V, Plasari E, Echevarria G, Simonnot MO. Increasing purity of ammonium nickel sulfate hexahydrate and production sustainability in a nickel phytomining process. Chem Eng Res Des. 2016;106:26-32. https://doi.org/10.1016/j.cherd.2015.12.009
https://doi.org/10.1016/j.cherd.2015.12....
).

Once in an aqueous solution at enough concentration and purity, Ni can be recovered as a pure metal or a compound by chemical or evaporative precipitation. For instance, Barbaroux et al. (2012)Barbaroux J, Plasari E, Mercier G, Simonnot MO, Morel JL, Blais JF. A new process for nickel ammonium disulfate production from ash of the hyperaccumulating plant Alyssum murale. Sci Total Environ. 2012;423:111-9. https://doi.org/10.1016/j.scitotenv.2012.01.063
https://doi.org/10.1016/j.scitotenv.2012...
produced an ammonium nickel sulfate hexahydrate (ANSH) salt (Ni(NH4)2(SO4)2.6H2O) containing 13.2 % of Ni. Briefly, the method consisted of the following steps: 1) washing the ashes of A. murale aboveground tissues with water; 2) leaching of Ni from the washed ash with H2SO4 1.9 mol L-1 heated to 100 °C for 2 h (150 g L-1 of ash) followed by filtration; 3) adjustment of the ash leachate to pH 5.0 with a NaOH 5 mol L-1 followed by evaporation; 4) selective recovery of Ni by crystallization of the ANSH salt; and, 5) purification of the ANSH salt through resolubilization, precipitation of MgF2 and recrystallization of the Ni salt. The same research group later improved this process by eliminating the number of steps to save water, chemicals, and energy (Zhang et al., 2016Zhang X, Laubie B, Houzelot V, Plasari E, Echevarria G, Simonnot MO. Increasing purity of ammonium nickel sulfate hexahydrate and production sustainability in a nickel phytomining process. Chem Eng Res Des. 2016;106:26-32. https://doi.org/10.1016/j.cherd.2015.12.009
https://doi.org/10.1016/j.cherd.2015.12....
). The method was then up-scaled from the lab to the pilot scale (Houzelot et al., 2017Houzelot V, Laubie B, Pontvianne S, Simonnot MO. Effect of up-scaling on the quality of ashes obtained from hyperaccumulator biomass to recover Ni by agromining. Chem Eng Res Design. 2017;20:26-33. https://doi.org/10.1016/j.cherd.2017.02.002
https://doi.org/10.1016/j.cherd.2017.02....
) using an industrial furnace to increase the production of nickel salts and develop a valuable method for the recovery of nickel. Further efforts are in place to improve the efficiency of these processes, and they will undoubtedly bring new options to recover metals in large-scale phytomining programs.

CONCLUSIONS AND PERSPECTIVES

The interest in the study of ultramafic soils has sharply increased in the last two decades in parallel with the research on metal phytoextraction, which seems to derive from the potential to use these soils as low-grade ores to be commercially exploited using metal hyperaccumulating plants. However, the ultramafic environment also has ecological value as a unique ecosystem that deserves protection from degradation by anthropic impacts. Thus, phytomining operations must consider the economic issues and the environmental and social consequences related to the use of ultramafic lands.

Despite the impressive outcomes of the phytomining research in the last years, anchored in discovering new Ni hyperaccumulators worldwide, the technology has not been tested on a large scale by the mining industry. These demonstrations are crucial to building a case with the mineral sector. Phytomining can also offer opportunities to farmers in developing countries to add an extra income to these low-productivity agricultural soils. Although this review focused on ultramafic soils, phytomining can also provide opportunities for sustainable reclamation of metal-polluted sites and mine site rehabilitation.

From the hyperaccumulators agronomy to the Ni recovery, the feasibility of the phytomining chain has been proven in temperate and tropical settings. However, especially for the tropics, there are untapped opportunities in places with large ultramafic outcrops and Ni production, such as Indonesia, The Philippines, Brazil, New Caledonia, and Cuba. It is likely that the progress made in the recent and future studies, along with a partnership with the mining industry, will enable phytomining to be converted into a sustainable technology to recover metals from low-grade ores that otherwise would not be economically viable.

REFERENCES

  • Alexander EB. Soil and vegetation differences from peridotite to serpentinite. Northeast Nat. 2009;16:178-92. https://doi.org/10.1656/045.016.0515
    » https://doi.org/10.1656/045.016.0515
  • Alexander EB, DuShey J. Topographic and soil differences from peridotite to serpentinite. Geomorphology. 2011;135:271-6. https://doi.org/10.1016/j.geomorph.2011.02.007
    » https://doi.org/10.1016/j.geomorph.2011.02.007
  • Alfaro MR, Montero A, Ugarte OM, Nascimento CWA, Accioly AMA, Biondi CM, Silva YJAB. Background concentrations and reference values for heavy metals in soils of Cuba. Environ Monit Assess. 2015;187:4198. https://doi.org/10.1007/s10661-014-4198-3
    » https://doi.org/10.1007/s10661-014-4198-3
  • Amir H, Lagrange A, Hassaïne N, Cavaloc Y. Arbuscular mycorrhizal fungi from New Caledonian ultramafic soils improve tolerance to nickel of endemic plant species. Mycorrhiza. 2013;23:585-95. https://doi.org/10.1007/s00572-013-0499-6
    » https://doi.org/10.1007/s00572-013-0499-6
  • Anacker BL. The nature of serpentine endemism. Am J Bot. 2014;101:219-24. https://doi.org/10.3732/ajb.1300349
    » https://doi.org/10.3732/ajb.1300349
  • Andrade LRM, Aquino FG, Miranda ZJG, Pereira CD, Reis Junior FB, Pessoa-Filho M, Oliveira-Filho EC, Nascimento CTC, Faleiro FG, Ramos AKB, Echevarria G. Native species of ultramafic massif of Barro Alto, GO, Brazil, can successfully be used to revegetate Ni mine spoil heaps. In: 21st World Congress of Soil Science, 12-14 August 2018; Rio de Janeiro. Viçosa, MG: Sociedade Brasileira de Ciência do Solo; 2018. Available from: https://ainfo.cnptia.embrapa.br/digital/bitstream/item/188857/1/Abstract-2561-final.pdf
    » https://ainfo.cnptia.embrapa.br/digital/bitstream/item/188857/1/Abstract-2561-final.pdf
  • Bani A, Echevarria G, Montargès-Pelletier E, Gjoka F, Sulçe S, Morel JL. Pedogenesis and nickel biogeochemistry in a typical Albanian ultramafic toposequence. Environ Monitor Assess. 2014;186:4431-44. https://doi.org/10.1007/s10661-014-3709-6
    » https://doi.org/10.1007/s10661-014-3709-6
  • Bani A, Echevarria G, Pavlova D, Shallari S, Morel JL, Sulçe S. Element case studies: Nickel. In: van der Ent A, Echevarria G, Baker AJM, Morel JL, editors. Agromining: Farming for metals. Extracting unconventional resources using plants. Cham: Springer; 2018. p. 221-31.
  • Bani A, Echevarria G, Sulce S, Morel JL, Mullai A. In-situ phytoextraction of Ni by a native population of Alyssum murale on an ultramafic site (Albania). Plant Soil. 2007;293:79-89. https://doi.org/10.1007/s11104-007-9245-1
    » https://doi.org/10.1007/s11104-007-9245-1
  • Bani A, Echevarria G, Sulçe S, Morel JL. Improving the agronomy of Alyssum murale for extensive phytomining: A five-year field study. Int J Phytoremediat. 2015a;17:117-27. https://doi.org/10.1080/15226514.2013.862204
    » https://doi.org/10.1080/15226514.2013.862204
  • Bani A, Echevarria G, Zhang X, Benizri E, Laubie B, Morel JL, Simonnot MO. The effect of plant density in nickel phytomining field experiments with Alyssum murale in Albania. Aust J Bot. 2015b;63:72-7. https://doi.org/10.1071/BT14285
    » https://doi.org/10.1071/BT14285
  • Bani A, Pavlova D, Echevarria G, Mullaj A, Reeves RD, Morel JL, Sulce S. Nickel hyperaccumulation by species of Alyssum and Thlaspi (Brassicaceae) from the ultramafic soils of the Balkans. Botanica Servica. 2010;34:3-14.
  • Barbaroux J, Plasari E, Mercier G, Simonnot MO, Morel JL, Blais JF. A new process for nickel ammonium disulfate production from ash of the hyperaccumulating plant Alyssum murale. Sci Total Environ. 2012;423:111-9. https://doi.org/10.1016/j.scitotenv.2012.01.063
    » https://doi.org/10.1016/j.scitotenv.2012.01.063
  • Barbaroux R, Mercier G, Blais JF, Morel JL, Simonnot MO. A new method for obtaining nickel metal from the hyperaccumulator plant Alyssum Murale. Sep Purif Technol. 2011;83:57-65. https://doi.org/10.1016/j.seppur.2011.09.009
    » https://doi.org/10.1016/j.seppur.2011.09.009
  • Becquer T, Quantin C, Boudot JP. Toxic levels of metals in Ferralsols under natural vegetation and crops in New Caledonia. Eur Soil Sci. 2010;61:994-1004. https://doi.org/10.1111/j.1365-2389.2010.01294
    » https://doi.org/10.1111/j.1365-2389.2010.01294
  • Berazaín R, de la Fuente V, Rufo L, Rodríguez N, Amils R, Díez-Garretas B, Sánchez-Mata D, Asensi A. Nickel localization in tissues of different hyperaccumulator species of Euphorbiaceae from ultramafic areas of Cuba. Plant Soil. 2007;293:99-106. https://doi.org/10.1007/s11104-007-9227-3
    » https://doi.org/10.1007/s11104-007-9227-3
  • Boominathan R, Saha-Chaudhury NM, Sahajwalla V, Doran PM. Production of nickel bio-ore from hyperaccumulator plant biomass: Applications in phytomining. Biotechnol Bioeng. 2004;86:243-50. https://doi.org/10.1002/bit.10795
    » https://doi.org/10.1002/bit.10795
  • Bourles A, Guentas L, Charvis C, Gensous S, Majorel C, Crossay T, Cavaloc Y, Burtet-Sarramegna V, Jourang P, Amir H. Co-inoculation with a bacterium and arbuscular mycorrhizal fungi improves root colonization, plant mineral nutrition, and plant growth of a Cyperaceae plant in an ultramafic soil. Mycorrhiza. 2020;30:121-31. https://doi.org/10.1007/s00572-019-00929-8
    » https://doi.org/10.1007/s00572-019-00929-8
  • Boyd RS, Martens SN. The significance of metal hyperaccumulation for biotic interactions. Chemoecology. 1998;8:1-7. https://doi.org/10.1007/s000490050002
    » https://doi.org/10.1007/s000490050002
  • Boyd RS. High-nickel insects and nickel hyperaccumulator plants: A review. Insect Sci. 2009;16:19-31. https://doi.org/10.1111/j.1744-7917.2009.00250.x
    » https://doi.org/10.1111/j.1744-7917.2009.00250.x
  • Burge DO, Barker WR. Evolution of nickel hyperaccumulation by Stackhousia tryonii (Celastraceae), a serpentine-endemic plant from Queensland, Australia. Aust Syst Bot. 2010;23:415-30. https://doi.org/10.1071/SB10029
    » https://doi.org/10.1071/SB10029
  • Cerdeira-Pérez A, Monterroso C, Rodríguez-Garrido B, Machinet G, Echevarria G, Prieto-Fernández A, Kidd PS. Implementing nickel phytomining in a serpentine quarry in NW Spain. J Geochem Explor. 2019;197:1-13. https://doi.org/10.1016/j.gexplo.2018.11.001
    » https://doi.org/10.1016/j.gexplo.2018.11.001
  • Chaney RL. Plant uptake of inorganic waste constituents. In: Parr JF, editor. Land treatment of hazardous wastes. Park Ridge: Noyes Data Corp; 1983. p. 50-76.
  • Chaney RL, Angle JS, Baker AJM, Li Y-M. Method for phytomining of nickel, cobalt and other metals from soil. US Patent 5,711,784. United States: IFI CLAIMS Patent Services; 1998.
  • Chaney RL, Angle JS, Broadhurst CL, Peters CA, Tappero RV, Sparks DL. Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. J Environ Qual. 2007;36:1429-43. https://doi.org/10.2134/jeq2006.0514
    » https://doi.org/10.2134/jeq2006.0514
  • Chaney RL, Baklanov IA. Phytoremediation and phytomining: Status and promise. Adv Bot Res. 2017;83:189-221. https://doi.org/10.1016/bs.abr.2016.12.006
    » https://doi.org/10.1016/bs.abr.2016.12.006
  • Clemens S. How metal hyperaccumulating plants can advance Zn biofortification. Plant Soil. 2017;411:111-20. https://doi.org/10.1007/s11104-016-2920-3
    » https://doi.org/10.1007/s11104-016-2920-3
  • Corzo-Remigio A, Chaney RL, Baker AJM, Edraki M, Erskine PD, Echevarria G, van der Ent A. Phytoextraction of high value elements and contaminants from mining and mineral wastes: Opportunities and limitations. Plant Soil. 2020;449:11-37. https://doi.org/10.1007/s11104-020-04487-3
    » https://doi.org/10.1007/s11104-020-04487-3
  • Doubková P, Vlasáková E, Sudová R. Arbuscular mycorrhizal symbiosis alleviates drought stress imposed on Knautia arvensis plants in serpentine soil. Plant Soil. 2013;370:149-61. https://doi.org/10.1007/s11104-013-1610-7
    » https://doi.org/10.1007/s11104-013-1610-7
  • Echevarria G. Genesis and behaviour of ultramafic soils and consequences for nickel biogeochemistry. In:van der Ent A, Echevarria G, Baker AJM, Morel JL, editors. Agromining: Farming for metals. Extracting unconventional resources using plants. Cham: Springer; 2018. p. 135-56.
  • Estrade N, Cloquet C, Echevarria G, Sterckeman T, Deng THB, Tang YT, Morel JL. Weathering and vegetation controls on nickel isotope fractionation in surface ultramafic environments (Albania). Earth Planet Sci Lett. 2015;423:24-5. https://doi.org/10.1016/j.epsl.2015.04.018
    » https://doi.org/10.1016/j.epsl.2015.04.018
  • Fantoni D, Brozzo G, Canepa M, Cipolli F, Marini L, Ottonello G, Zuccolini M. Natural hexavalent chromium in groundwaters interacting with ophiolitic rocks. Environ Geol. 2002;42:871-82. https://doi.org/10.1007/s00254-002-0605-0
    » https://doi.org/10.1007/s00254-002-0605-0
  • Jardim Botânico do Rio de Janeiro. Flora do Brasil 2020. Rio de Janeiro: Instituto de Pesquisas Jardim Botânico do Rio de Janeiro; 2021 [cited 2021 Jul 20]. Available from: http://floradobrasil.jbrj.gov.br/
    » http://floradobrasil.jbrj.gov.br/
  • Galey ML, van der Ent A, Iqbal MCM, Rajakaruna N. Ultramafic geoecology of South and Southeast Asia. Bot Stud. 2017;58:18. https://doi.org/10.1186/s40529-017-0167-9
    » https://doi.org/10.1186/s40529-017-0167-9
  • Garnier J, Quantin C, Guimarães E, Garg VK, Martins ES, Becquer T. Understanding the genesis of ultramafic soils and catena dynamics in Niquelândia, Brazil. Geoderma. 2009;151:204-14. https://doi.org/10.1016/j.geoderma.2009.04.020
    » https://doi.org/10.1016/j.geoderma.2009.04.020
  • Garnier J, Quantin C, Sophei R, Guimarães E, Becquer T. Field availability and mobility of metals in Ferralsols developed on ultramafic rock of Niquelândia, Brazil. Braz J Geol. 2021;51:e20200092. https://doi.org/10.1590/2317-4889202120200092
    » https://doi.org/10.1590/2317-4889202120200092
  • Gei V, Isnard S, Erskine PD, Echevarria G, Fogliani B, Jaffré T, van der Ent A. A systematic assessment of the occurrence of trace element hyperaccumulation in the flora of New Caledonia. Bot J Linn Soc. 2020;194:1-22. https://doi.org/10.1093/botlinnean/boaa029
    » https://doi.org/10.1093/botlinnean/boaa029
  • Guillot S, Hattori K. Serpentinites: Essential roles in geodynamics, arc volcanism, sustainable development, and the origin of life. Elements. 2013;9:95-8. https://doi.org/10.2113/gselements.9.2.95
    » https://doi.org/10.2113/gselements.9.2.95
  • Gutiérrez DMN, Nkrumah PN, van der Ent A, Pollard J, Baker AJM, Torralba FN, Pons F, Sánchez MN, Hernández TG, Echevarria G. The potential of Blepharidium guatemalense for nickel agromining in Mexico and Central America. Int J Phytoremediat. 2021;23:1157-68. https://doi.org/10.1080/15226514.2021.1881039
    » https://doi.org/10.1080/15226514.2021.1881039
  • Harrison SP, Damschen E, Going BM. Climate gradients, climate change, and special edaphic floras. Northeast Nat. 2009;16:121-30. https://doi.org/10.1656/045.016.0510
    » https://doi.org/10.1656/045.016.0510
  • Hipfinger C, Rosenkranz T, Thüringer J, Puschenreiter M. Fertilization regimes affecting nickel phytomining efficiency on a serpentine soil in the temperate climate zone. Int J Phytoremediat. 2021;23:407-14. https://doi.org/10.1080/15226514.2020.1820446
    » https://doi.org/10.1080/15226514.2020.1820446
  • Houzelot V, Laubie B, Pontvianne S, Simonnot MO. Effect of up-scaling on the quality of ashes obtained from hyperaccumulator biomass to recover Ni by agromining. Chem Eng Res Design. 2017;20:26-33. https://doi.org/10.1016/j.cherd.2017.02.002
    » https://doi.org/10.1016/j.cherd.2017.02.002
  • Isnard S, L’huillier L, Rigault F, Jaffré T. How did the ultramafic soils shape the flora of the New Caledonian hotspot? Plant Soil. 2016;403:53-76. https://doi.org/10.1007/s11104-016-2910-5
    » https://doi.org/10.1007/s11104-016-2910-5
  • Jacobi CM, Carmo FF, Campos IC. Soaring extinction threats to endemic plants in Brazilian metal-rich regions. Ambio. 2011;40:540-3. https://doi.org/10.1007/s13280-011-0151-7
    » https://doi.org/10.1007/s13280-011-0151-7
  • Jaffré T, Brooks RR, Lee J, Reeves RD. Sebertia acuminata: A hyperaccumulator of nickel from New Caledonia. Science. 1976;193:579-80. https://doi.org/10.1126/science.193.4253.579
    » https://doi.org/10.1126/science.193.4253.579
  • Jaffré T, Pillon Y, Thomine S, Merlot S. The metal hyperaccumulators from New Caledonia can broaden our understanding of nickel accumulation in plants. Front Plant Sci. 2013;4:279. https://doi.org/10.3389/fpls.2013.00279
    » https://doi.org/10.3389/fpls.2013.00279
  • Jaffré T, Reeves RD, Baker AJM, Schat H, van der Ent A. The discovery of nickel hyperaccumulation in the New Caledonian tree Pycnandra acuminata 40 years on: An introduction to a Virtual Issue. New Phytol. 2018;218:397-400. https://doi.org/10.1111/nph.15105
    » https://doi.org/10.1111/nph.15105
  • Kanellopoulos C. Influence of ultramafic rocks and hot springs with travertine depositions on geochemical composition and baseline of soils. Application to eastern central Greece. Geoderma 2020;380:1146-9. https://doi.org/10.1016/j.geoderma.2020.114649
    » https://doi.org/10.1016/j.geoderma.2020.114649
  • Kaprara E, Kazakis N, Simeonidis K, Coles S, Zouboulis AI, Samaras P, Mitrakas M. Occurrence of Cr(VI) in drinking water of Greece and relation to the geological background. J Hazard Mater. 2015;281:2-11. https://doi.org/10.1016/j.jhazmat.2014.06.084
    » https://doi.org/10.1016/j.jhazmat.2014.06.084
  • Kazakou E, Dimitrakopoulos PG, Baker AJM, Reeves RD, Troumbis AY. Hypotheses, mechanisms and trade-offs of tolerance and adaptation to ultramafic soils: From species to ecosystem level. Biol Rev. 2008;83:495-508. https://doi.org/10.1111/j.1469-185X.2008.00051.x
    » https://doi.org/10.1111/j.1469-185X.2008.00051.x
  • Keskinkilic E. Nickel laterite smelting processes and some examples of recent possible modifications to the conventional route. Metals. 2019;9:974. https://doi.org/10.3390/met9090974
    » https://doi.org/10.3390/met9090974
  • Kierczak J, Pedziwiatr A, Waroszewski J, Modelska M. Mobility of Ni, Cr and Co in serpentine soils derived on various ultrabasic bedrocks under temperate climate. Geoderma. 2016;268:78-91. https://doi.org/10.1016/j.geoderma.2016.01.025
    » https://doi.org/10.1016/j.geoderma.2016.01.025
  • Kierczak J, Pietranik A, Pędziwiatr A. Ultramafic geoecosystems as a natural source of Ni, Cr, and Co to the environment: A review. Sci Total Environ. 2021;755:142620. https://doi.org/10.1016/j.scitotenv.2020.142620
    » https://doi.org/10.1016/j.scitotenv.2020.142620
  • Kodolányi J, Pettke T, Spandler C, Kamber BS, Ling KG. Geochemistry of ocean floor and fore-arc serpentinites: Constraints on the ultramafic input to subduction zones. J Petrol. 2012;53:237-70. https://doi.org/10.1093/petrology/egr058
    » https://doi.org/10.1093/petrology/egr058
  • Lekaj E, Teqja Z, Bani A. The dynamics of land cover changes and the impact of climate change on ultramafic areas of Albania. Period Mineral. 2019;88:69-80. https://doi.org/10.2451/2019PM849
    » https://doi.org/10.2451/2019PM849
  • Li YM, Chaney R, Brewer E, Rosenberg R, Angle JS, Baker A, Reeves R. Development of a technology for commercial phytoextraction of nickel: Economic and technical considerations. Plant Soil. 2003;249:107-15. https://doi.org/10.1023/A:1022527330401
    » https://doi.org/10.1023/A:1022527330401
  • Lindsay WL, Norvell WA. Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J. 1978;42:421-8. https://doi.org/10.2136/sssaj1978.03615995004200030009x
    » https://doi.org/10.2136/sssaj1978.03615995004200030009x
  • McClain CN, Fendorf S, Webb SM, Maher K. Quantifying Cr(VI) production and export from serpentine soil of the California coast range. Environ Sci Technol. 2017;51:141-9. https://doi.org/10.1021/acs.est.6b03484
    » https://doi.org/10.1021/acs.est.6b03484
  • McClain CN, Maher K. Chromium fluxes and speciation in ultramafic catchments and global rivers. Chem Geol. 2016;426:135-57. https://doi.org/10.1016/j.chemgeo.2016.01.021
    » https://doi.org/10.1016/j.chemgeo.2016.01.021
  • Mengoni A, Barzanti R, Gonnelli C, Gabbrielli R, Bazzicalupo M. Characterization of nickel-resistant bacteria isolated from serpentine soil. Environ Microbiol. 2001;3:691-708. https://doi.org/10.1046/j.1462-2920.2001.00243.x
    » https://doi.org/10.1046/j.1462-2920.2001.00243.x
  • Mesjasz-Przybyłowicz J, Przybyłowicz WJ. Ecophysiology of nickel hyperaccumulating plants from South Africa – from ultramafic soil and mycorrhiza to plants and insects. Metallomics. 2020;12:1018-35. https://doi.org/10.1039/c9mt00282k
    » https://doi.org/10.1039/c9mt00282k
  • Morel JL. Agromining: A new concept. In: Echevarria G, Morel JL, Simonnot MO, leaders. Workshop 3 “Agromining: From soils to refined metal products”. Nancy: SGA Biennial Meeting; 2015. p. 24-7. Available from: https://e-sga.org/nc/publications/sga-biennial-meetings-abstract-volumes/2015-nancy/
    » https://e-sga.org/nc/publications/sga-biennial-meetings-abstract-volumes/2015-nancy/
  • Mouly A, Jeanson M. Specialization to ultramafic substrates and narrow endemism of Cyclophyllum (Rubiaceae) in New Caledonia: Contribution of novel species to the un- derstanding of these singular patterns. Acta Bot Gallica. 2015;162:173-89. https://doi.org/10.1080/12538078.2015.1062799
    » https://doi.org/10.1080/12538078.2015.1062799
  • Nascimento CWA, Biondi CM, Silva FBV, Lima LHV. Using plants to remediate or manage metal-polluted soils: An overview on the current state of phytotechnologies. Acta Sci-Agron. 2021;43:e58283. https://doi.org/10.4025/actasciagron.v43i1.58283
    » https://doi.org/10.4025/actasciagron.v43i1.58283
  • Nascimento CWA, Hesterberg D, Tappero R, Nicholas S, Silva FBV. Citric acid-assisted accumulation of Ni and other metals by Odontarrhena muralis: Implications for phytoextraction and metal foliar distribution assessed by µ-SXRF. Environ Pollut. 2020;245:114025. https://doi.org/10.1016/j.envpol.2020.114025
    » https://doi.org/10.1016/j.envpol.2020.114025
  • Nicks L, Chambers MF. Farming for metals. Mining Environ Manage. 1995;3:5-18.
  • Nkrumah PN, Baker AJM, Chaney RL, Erskine PD, Echevarria G, Morel JL, van der Ent A. Current status and challenges in developing nickel phytomining: An agronomic perspective. Plant Soil. 2016;406:55-69. https://doi.org/10.1007/s11104-016-2859-4
    » https://doi.org/10.1007/s11104-016-2859-4
  • Nkrumah PN, Tisserand R, Chaney RL, Baker AJM, Morel JL, Goudon R, Erskine PD, Echevarria G, van der Ent A. The first tropical ‘metal farm’: Some perspectives from field and pot experiments. J Geochem Explor. 2019;198:114-22. https://doi.org/10.1016/j.gexplo.2018.12.003
    » https://doi.org/10.1016/j.gexplo.2018.12.003
  • Pal A, Choudhuri P, Dutta S, Mukherjee PK, Paul AK. Isolation and characterization of nickel-resistant microflora from ultramafic soils of Andaman. World J Microbiol Biotechnol. 2004;20:881-6. https://doi.org/10.1007/s11274-004-2776-1
    » https://doi.org/10.1007/s11274-004-2776-1
  • Pal A, Dutta S, Mukherjee PK, Paul AK. Occurrence of heavy metal-resistance in microflora from ultramafic soil of Andaman. J Basic Microbiol. 2005;45:207-18. https://doi.org/10.1002/jobm.200410499
    » https://doi.org/10.1002/jobm.200410499
  • Palm ER, Van Volkenburgh E. Physiological adaptations of plants to serpentine soils. In: Rajakaruna N, Boyd RS, Harris TB, editors. Plant ecology and evolution in harsh environments. Hauppauge: Nova Science Publishers; 2014. p. 1-19.
  • Papazotos P, Vasileiou E, Perraki M. The synergistic role of agricultural activities in groundwater quality in ultramafic environments: The case of the Psachna basin, central Euboea, Greece. Environ Monit Assess. 2019;191:317. https://doi.org/10.1007/s10661-019-7430-3
    » https://doi.org/10.1007/s10661-019-7430-3
  • Rajapaksha AU, Vithanage M, Ok YS, Oze C. Cr(VI) formation related to Cr (III)-muscovite and birnessite interactions in ultramafic environments. Environ Sci Technol. 2013;47:9722-9. https://doi.org/10.1021/es4015025
    » https://doi.org/10.1021/es4015025
  • Pessoa-Filho M, Barreto CC; Reis Junior FB, Fragoso RR, Costa FS, Mendes IC, Andrade LRM. Microbiological functioning, diversity, and structure of bacterial communities in ultramafic soils from a tropical savanna. A Van Leeuw J Microb. 2015;107:935-49. https://doi.org/10.1007/s10482-015-0386-6
    » https://doi.org/10.1007/s10482-015-0386-6
  • Ratié G, Garnier J, Vieira LC, Araújo DF, Komárek M, Poitrasson F, Quantin C. Investigation of Fe isotope systematics for the complete sequence of natural and metallurgical processes of Ni lateritic ores: Implications for environmental source tracing. Appl Geochem. 2021;127:104930. https://doi.org/10.1016/j.apgeochem.2021.104930
    » https://doi.org/10.1016/j.apgeochem.2021.104930
  • Reeves RD, Adiguzel N. The nickel hyperaccumulating plants of Turkey and adjacent areas: A review with new data. Turk J Biol. 2008;32:143-53.
  • Reeves RD, Baker AJM, Becquer T, Echevarria G, Miranda ZJG. The flora and biogeochemistry of the ultramafic soils of Goias state, Brazil. Plant Soil. 2007;293:107-19. https://doi.org/10.1007/s11104-007-9192-x
    » https://doi.org/10.1007/s11104-007-9192-x
  • Reeves RD, Baker AJM, Borhidi A, Berasaín R. Nickel hyperaccumulation in the serpentine flora of Cuba. Ann Bot. 1999;83:29-38. https://doi.org/10.1006/anbo.1998.0786
    » https://doi.org/10.1006/anbo.1998.0786
  • Reeves RD, Baker AJM, Jaffré T, Erskine PD, Echevarria G, van der Ent A. A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytol. 2017;218:407-11. https://doi.org/10.1111/nph.14907
    » https://doi.org/10.1111/nph.14907
  • Robles-Camacho J, Armienta M. Natural chromium contamination of groundwater at Leon Valley, Mexico. J Geochem Explor. 2000;68:167-81. https://doi.org/10.1016/S0375-6742(99)00083-7
    » https://doi.org/10.1016/S0375-6742(99)00083-7
  • Russell MJ, Ponce A. Six ‘must-have’ minerals for life’s emergence: Olivine, pyrrhotite, bridgmanite, serpentine, fougerite and mackinawite. Life. 2020;10:291. https://doi.org/10.3390/life10110291
    » https://doi.org/10.3390/life10110291
  • Sachs J. Handbuch der Physiologischen Botanik. In: Hofmeister W, editor. Handbuch der Experimental-Physiologie der Pflanzen. Leipzig: Engelmann; 1865. v. IV. p. 153-4. https://www.biodiversitylibrary.org/item/197154#page/10/mode/1up
    » https://www.biodiversitylibrary.org/item/197154#page/10/mode/1up
  • Salles D, Carmo F, Jacobi C. Habitat loss challenges the conservation of endemic plants in mining-targeted brazilian mountains. Environ Conserv. 2019;46:140-6. https://doi.org/10.1017/S0376892918000401
    » https://doi.org/10.1017/S0376892918000401
  • Santos CA, Brito MFL, Pereira CS, Fernandes PR. Levantamento geológico e de potencial mineral de novas fronteiras: projeto Rio Capibaribe. Recife: Serviço Geológico do Brasil; 2020.
  • Schlegel HG, Cosson JP, Baker JM. Nickel hyperaccumulating plants provide a niche for nickel resistant bacteria. Bot Acta. 1991;104:18-25. https://doi.org/10.1111/j.1438-8677.1991.tb00189.x
    » https://doi.org/10.1111/j.1438-8677.1991.tb00189.x
  • Shuman LM. Fractionation method for soil microelements. Soil Sci. 1985:140;11-22. https://doi.org/10.1097/00010694-198507000-00003
    » https://doi.org/10.1097/00010694-198507000-00003
  • Silva JM, Ferreira Filho CF, Giustina MESD. The Limoeiro deposit: Ni-Cu-PGE sulfide mineralization hosted within an ultramafic tubular magma conduit in the Borborema Province, northeastern Brazil. Econ Geol. 2013;108:1753-71. https://doi.org/10.2113/econgeo.108.7.1753
    » https://doi.org/10.2113/econgeo.108.7.1753
  • Silva WR, Silva FBV, Araújo PRM, Nascimento CWA. Assessing human health risks and strategies for phytoremediation in soils contaminated with As, Cd, Pb, and Zn by slag disposal. Ecotox Environ Safe. 2017;144:522-30. https://doi.org/10.1016/j.ecoenv.2017.06.068
    » https://doi.org/10.1016/j.ecoenv.2017.06.068
  • Simonnot MO, Vaughan J, Laubie B. Processing of bio-ore to products. In: van der Ent A, Echevarria G, Baker AJM, Morel JL, editors. Agromining: Farming for metals. Extracting unconventional resources using plants. Cham: Springer; 2018. p. 39-52.
  • Strauss SY, Cacho NI. Nowhere to run, nowhere to hide: The importance of enemies and apparency in adaptation to harsh soil environments. Am Nat. 2013;182:E1-E14. https://doi.org/10.1086/670754
    » https://doi.org/10.1086/670754
  • Tappero RV, Peltier E, Gräfe M, Heidel K, Ginder-Vogel M, Livi KJT, Rivers ML, Marcus MA, Chaney RL, Sparks DL. Hyperaccumulator Alyssum murale relies on a different metal storage mechanism for cobalt than for nickel. New Phytol. 2007;175:641-54. https://doi.org/10.1111/j.1469-8137.2007.02134.x
    » https://doi.org/10.1111/j.1469-8137.2007.02134.x
  • Tashakor M, Hochwimmer B, Brearley FQ. Geochemical assessment of metal transfer from rock and soil to water in serpentine areas of Sabah (Malaysia). Environ Earth Sci. 2017;76:281. https://doi.org/10.1007/s12665-017-6585-x
    » https://doi.org/10.1007/s12665-017-6585-x
  • Tashakor M, Modabberi S, van der Ent A. Impacts of ultramafic outcrops in Peninsular Malaysia and Sabah on soil and water quality. Environ Monit Assess. 2018;190:333. https://doi.org/10.1007/s10661-018-6668-5
    » https://doi.org/10.1007/s10661-018-6668-5
  • van der Ent A, Baker AJM, Reeves RD, Chaney RL, Anderson CWN, Meech JA, Erskine PD, Simonnot M-O, Vaughan J, Morel JL. Agromining: Farming for metals in the future. Environ Sci Technol. 2015;49:4773-80. https://doi.org/10.1021/es506031u
    » https://doi.org/10.1021/es506031u
  • van der Ent A, Echevarria G, Pollard AJ, Erskine PD. X-ray fluorescence ionomics of herbarium collections. Sci Rep. 2019;9:4746. https://doi.org/10.1038/s41598-019-40050-6
    » https://doi.org/10.1038/s41598-019-40050-6
  • van der Ent A, Echevarria G, Tibbett M. Delimiting soil chemistry thresholds for nickel hyperaccumulator plants in Sabah (Malaysia). Chemoecology. 2016;26:67-82. https://doi.org/10.1007/s00049-016-0209-x
    » https://doi.org/10.1007/s00049-016-0209-x
  • van der Ent A, Mak R, de Jonge MD, Harris HH. Simultaneous hyperaccumulation of nickel and cobalt in the tree Glochidion cf. sericeum (Phyllanthaceae): Elemental distribution and chemical speciation. Sci Rep. 2018a;8:9683. https://doi.org/10.1038/s41598-018-26891-7
    » https://doi.org/10.1038/s41598-018-26891-7
  • van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H. Hyperaccumulators of metal and metalloid trace elements: Facts and fiction. Plant Soil. 2013;362:319-34. https://doi.org/10.1007/s11104-012-1287-3
    » https://doi.org/10.1007/s11104-012-1287-3
  • van der Ent A, Echevarria G, Baker AJM, Morel JL. Agromining: Farming for metals. Extracting unconventional resources using plants. Cham: Springer; 2018b.
  • Vidal-Torrado P, Macias F, Calvo R, Carvalho SG, Silva AC. Genese de solos derivados de rochas ultramaficas serpentinizadas no sudoeste de Minas Gerais. Rev Bras Geocienc. 2006;30:523-41. https://doi.org/10.1590/S0100-06832006000300013
    » https://doi.org/10.1590/S0100-06832006000300013
  • Vilela EF, Inda AV, Zinn YL. Soil genesis, mineralogy and chemical composition in a steatite outcrop under tropical humid climate in Brazil. Catena. 2019;183:104234. https://doi.org/10.1016/j.catena.2019.104234
    » https://doi.org/10.1016/j.catena.2019.104234
  • Vithanage M, Kumarathilaka P, Oze C, Karunatilake S, Seneviratne M, Hseu ZY, Gunarathne V, Dassanayake M, Ok YS, Rinklebe J. Occurrence and cycling of trace elements in ultramafic soils and their impacts on human health: A critical review. Environ Int. 2019;131:104974. https://doi.org/10.1016/j.envint.2019.104974
    » https://doi.org/10.1016/j.envint.2019.104974
  • Vithanage M, Rajapaksha AU, Oze C, Rajakaruna M, Dissanayake CB. Metal release from serpentine soils in Sri Lanka. Environ Monit Assess. 2014;186:3415-29. https://doi.org/10.1007/s10661-014-3626-8
    » https://doi.org/10.1007/s10661-014-3626-8
  • Von Wettberg EJ, Wright JW. Genomic approaches to understanding adaptation. In: Harrison SP, Rajakaruna N, editors. Serpentine: The evolution and ecology of a model system. Berkeley: University of California Press; 2011. https://doi.org/10.1525/california/9780520268357.003.0006
    » https://doi.org/10.1525/california/9780520268357.003.0006
  • Wall MA, Boyd RS. Nickel accumulation in serpentine arthropods from the Red Hills, California. Pan-Pac Entomol. 2002;78:168-76. https://archive.org/details/biostor-245415/mode/2up
    » https://archive.org/details/biostor-245415/mode/2up
  • Yan T, Wang X, Liu D, Chi Q, Zhou J, Xu J, Xu S, Zhang B, Nie L, Wang W. Continental-scale spatial distribution of chromium (Cr) in China and its relationship with ultramafic-mafic rocks and ophiolitic chromite deposit. Appl Geochem. 2021;126:104896. https://doi.org/10.1016/j.apgeochem.2021.104896
    » https://doi.org/10.1016/j.apgeochem.2021.104896
  • Zhang X, Laubie B, Houzelot V, Plasari E, Echevarria G, Simonnot MO. Increasing purity of ammonium nickel sulfate hexahydrate and production sustainability in a nickel phytomining process. Chem Eng Res Des. 2016;106:26-32. https://doi.org/10.1016/j.cherd.2015.12.009
    » https://doi.org/10.1016/j.cherd.2015.12.009

Edited by

Editors: José Miguel Reichert and Alberto Vasconcellos Indá Júnior.

Publication Dates

  • Publication in this collection
    20 Apr 2022
  • Date of issue
    2022

History

  • Received
    29 July 2021
  • Accepted
    22 Feb 2022
Sociedade Brasileira de Ciência do Solo Sociedade Brasileira de Ciência do Solo, Departamento de Solos - Edifício Silvio Brandão, s/n, Caixa Postal 231 - Campus da UFV, CEP 36570-900 - Viçosa-MG, Tel.: (31) 3612-4542 - Viçosa - MG - Brazil
E-mail: sbcs@sbcs.org.br