Hyperaccumulator plants can accumulate high concentration of contaminants (especially metals) in their shoots without showing significant signs of toxicity (Ebbs et al., 1997; Thijs, Langill and Vangronsveld, 2017); the term was coined by Brooks and co (1977) to indicate plants that uptake large amounts of heavy metals from the soil, a behaviour contrary to that of excluder plants. In quantitative terms, the level of metal concentration achievable by hyperaccumulators is metal-dependent. A plant is classified as hyperaccumulator if it achieves: 10,000 mg/kg dry weight for Mn and Zn concentrations, 100 mg/kg dry weight for Cd, and 1,000 mg/kg dry weight for As, Cu, Co and Ni (Asad et al., 2019). Aside from the “high” metal concentration that these plants can achieve, another intrinsic feature is the ability to translocate the metals from their roots system to their shoots (Asad et al., 2019). The main characteristics of plant hyperaccumulators are detailed by Ernst (2005) as:
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a well branched root system;
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high transfer/efficient translocation from root to shoot;
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high capacity of metal accumulation in the aerial part of the plant without hindering growth;
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low transfer of the metals to the seeds of the plant.
These characteristics make hyperaccumulators the ideal candidates for phyto-remediation and even phyto-mining (Thijs, Langill and Vangronsveld, 2017). In particular, for phyto-mining, these plants remove metals from the abandoned substrates and concentrate them in the harvestable parts of plants. Overall, phyto-mining or phyto-extraction has been proposed as an environmentally friendly and low-cost technology for decreasing the heavy metal content of contaminated soils, creating an effective alternative to chemical/engineering based solutions (Ebbs et al., 1997; Lombi et al., 2003; Robinson et al., 2006; Asad et al., 2019). The hyperaccumulation capacity is considered selective, i.e. only one metal at a time can be hyperaccumulated by a specific plant hyperaccumulator. However, studies such as the one by Van Der Ent et al. (2018) indicated that some hyperaccumulators can intake high quantities of multiple metals simultaneously, with preference for one or the other depending on the pH of the soils.
This mechanism has been studied thoroughly for plants accumulating nickel, where approximately 350 taxa are known to accumulate between 1,000 and 38,000 mg/kg of dry leaf biomass (Reeves, 1992); Ni hyperaccumulators constitute 70% of the known hyperaccumulator species (Van Der Ent et al., 2018). However, not all metals have the same level of scientific interest and significantly fewer taxa have been identified for the hyperaccumulation of lead. Studies of herbaceous species growing in mining areas have indicated that lead accumulates 600 times more in some of the grass species (Yanquan et al., 2005). In comparison, studies showing the accumulation in bushe-like plants indicated a much lower accumulation ability (Yanqun et al., 2004). In Wales, UK, Agrostis tenuis has been recorded in mining areas as resistant to lead and zinc poisoning (Bradshaw, 1952; Gregory and Bradshaw, 1965), particularly at the Welsh sites of Goginan mine and Parys Mountain – where the relative concentration of lead was estimated at 3,250 and 1,600 ppm respectively, this is in comparison for instance, with the 6,000 ppm of the mines in Yunnan (Robinson et al., 2006). Agrostis fits well with the characteristics of an hyperaccumulator, however its accumulation ability is limited to the first few centimetres of soil.
In the UK, around 200,000 sites have been identified as potentially at risk of soil contamination (Crane et al., 2017), but the problem is also recognised worldwide with an extent of 3.5 million sites identified as being potentially at risk of contamination in the EU and half a million recognised as highly contaminated and requiring remediation (Mahar et al., 2015), hence the challenge is wide spread with the levels and combination of contaminants being highly variable.
Examples of the level of contamination present at ancient mining sites are given by the assessments of the ancient mining activities in Wales where a lead concentration of 4 wt.% in the Frongoch and 0.9 wt.% in the Parys Mountain mine (Crane et al., 2017) was discovered.
Environmental Agency data (McGrath and Zhao, 2006) indicates a maximum concentration of lead in fine loamy sediments in close proximity to ancient metal mines reaching 16,338 ppm and averaging 3,500 ppm in coarse and fine silty sediments, fundamentally evidencing extensive diffusion of lead contamination due to water percolation through open adits and leachate from tailings: enriching the loamy and silty sediments of waterbeds in proximity of the mines. However, as these sediments have polymetallic contaminants, the recovery of the metals are extremely difficult using present methods (Ernst, 2005).
The literature indicates that 14 species of hyperaccumulators have been identified for lead (Mahar et al., 2015), with the four main species being: Betula occidentalis (1,000 mg/kg d wt) (Koptsik, 2014), Brassica juncea (10,300 mg/kg d wt) (Ernst, 2005), Medicago sativa (43,300 mg/kg d wt) (Ernst, 2005) and Thlaspi rotundifolium (8,200 mg/kg d wt)(Wenzel and Jockwer, 1999); however, it is always best practice to evaluate the presence of autochthonous species in abandoned mining areas to ensure the avoidance of environmental issues arising due to the use of exotic species becoming invasive in the long term (Li, 2006). For this study, the correspondence of lead contamination and the presence of grass hyperaccumulators and in particular Agrostis in areas such as the discharges at Cwmystwyth mine (Ceredigion, Wales) shows a potential route for the use of this common taxon for the phytoextraction of metals. Agrostis is known for the multi-selective accumulation of Cd, Cu, Mn, Ni, As, Pb and Zn (Gregory and Bradshaw, 1965; Li, 2006), a summary of the types of Agrostis species and the metals accumulated is presented in Table 1. In particular, Agrostis grown on Pb-rich soil shows the preferential formation of chloropyromorphite (Pb5(PO4)3Cl) in the roots of the plant (Cotter-Howells, Champness and Charnock, 1999). The formation of this compound within the roots indicates a way forward for the stabilization of the metal contaminant in the soil and for this specific task Agrostis tenuis Sibth is already commercially available (Prasad and De Oliveira Freitas, 2003). Although other plants species like Thlaspi alpestre and Minuartia verna have been recorded as establishing successful populations on metal rich soils such as “the acidic [soils] in Central Wales and Snowdonia”, the almost consistent proliferation of Agrostis tenuis increases its attractiveness for use in lead bioremediation (Jowett, 1964). The prevalence of Agrostis tenuis and stolonifera was also observed near the metal refineries at Prescot, where heavy metal aerial pollution and a Cu concentration in the soil of 4,000 ppm was detected. The Agrostis species were shown to evolve increasing metal tolerance by selecting for metal tolerant genotypes that could thrive. It was observed that although a large number of plant species were present around Prescot before pollution, the Agrostis species were the only genus able to develop the genetic variability required to survive in such heavily polluted conditions within a relatively short period of time (sometimes within a single generation)(Wu, Bradshaw and Thurman, 1975).
Overall, Agrostis shows great capabilities to adapt and increase its accumulation capacity under stress from soil pollution, exhibiting a major advantage as a versatile hyperaccumulator in soils displaying different metal mixing (association of metals) and metal concentrations (ratio and absolute concentration of the different metals) (Austruy, et al., 2013).
Furthermore, the direct formation of lead salts as a way to store and effectively avoid the toxicity of the metal by Agrostis implies that a simple removal method of the lead compound from the harvested biomass is feasible, indicating a route for effective removal of the contaminant from the soils. Of course, this route would be viable only if the salts are present in highest concentration in the harvestable shoots of the plants. This is specifically the focus of this paper and the results below can be used to indicate the level of concentration of lead in the shoots of commercially available Agrostis tenuis (as used in this study) and their composition with the aim of extracting metal salts (from the soil) and stabilising them within the plant. This could be a method not only for remediating soils contaminated by industrial and mining activities, but also tap into a secondary raw material source that can lessen the demand for virgin metals and the environmentally damaging activities linked to their sourcing.
In summary, Agrostis offers strong benefits as a versatile hyperaccumulator and includes environmental benefits for the preservation of the scenic historic landscapes where often ancient mines and abandoned industrial sites are located. The height and type of plant (generic grass) are non-invasive and supports the idea of preservation of the landscape character. Furthermore, Agrostis grows fast and it is easy to harvest using routine agricultural machinery, while allowing for fast removal of the metal-rich biomass for further treatment/use.
Table 1
Reference to Agrostis spp. as hyperaccumulator in the literature, indicating the type of Agrostis, the metal/s targeted and the type of experimental setting. When “Literature” is indicated it means that the authors did not perform an experiment but they are reporting previous data from the literature themselves.
Agrostis type | Metal extracted | Reference | Type of trial |
Capillaris | Cd, Cu, Mn, Ni, Pb, Zn | (Ernst, 2005) | In situ |
Castellana; Tenerrima | As | (Asad et al., 2019) | Literature |
Tenuis; Stolonifera | Pb, Zn | (Li, 2006) | Literature |
Stolinifera; Capillaris | As, Cd, Cu, Pb, Zn | (Pérez-de-Mora et al., 2006) | In situ; Containers |
Spp. | As; Cd; Cu; Pb; Zn | (Boshoff et al., 2014) | In situ |
Capillaris | Pb | (Rodríguez-Seijo et al., 2016) | In situ |
Capillaris | As, Pb, Cu, Cd, Sb | (Austruy et al., 2013) | Containers |
Spp. | Cu; Zn; Pb | (Mahar et al., 2015) | Literature |
Tenuis | Zn; Pb | (Wenzel and Jockwer, 1999) | Literature |
Capillaris; Canina | As; Cu; Pb; Sb | (Bech et al., 2016) | Literature |
Durieui | Pb | (Fernández et al., 2017) | In-situ |
Capillaris | Pb | (Miransari, 2011) | Literature |
Capillaris | Pb | (Chaney et al., 1997) | In-situ |
Capillaris | Pb | (Tangahu et al., 2011) | Containers |
Capillaris; Gigantea | Cu | (Lange et al., 2017) | Literature |