Abstract
Background and Aims
Indonesia is one of the most biodiverse regions in the world, but only a few metal hyperaccumulator plants have been reported from this vast country. This study aimed to discover rare earth element (REE) hyperaccumulator plants on Bangka Island, an area known to have REE enriched soils associated with tin placer deposits.
Methods
Prior to this study, herbarium specimens at the Universitas Bangka Belitung Herbarium were screened using non-destructive X-ray Fluorescence (XRF) scanning to detect specimens with anomalous REE concentrations. Fieldwork was subsequently conducted to collect samples from plant species suspected to be (hyper)accumulators based on the earlier XRF survey. Scanning electron microscopy and micro-XRF were used to verify the possibility of surface contamination by soil particles in plant specimens, and inductively coupled plasma atomic emission spectroscopy (ICP-AES) was used to determine total elemental concentrations in the plant material.
Results
Blechnopsis orientalis was found to hyperaccumulate REEs up to 3000 µg g−1 as well as arsenic up to 2100 µg g−1. The non-destructive analysis found no dust or soil contamination on B. orientalis specimens, confirming it as a genuine REE and arsenic hyperaccumulator. Additionally, the known REE hyperaccumulator Dicranopteris linearis was confirmed to be a REE hyperaccumulator on Bangka Island.
Conclusion
Blechnopsis orientalis is a REE hyperaccumulator with high potential for phytoextraction as it is a faster growing and larger species than D. linearis. As B. orientalis and D. linearis are native to Bangka Island, both should be studied further for their application in rehabilitating and extracting REEs from the (abandoned) tin mine areas.
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Introduction
Hyperaccumulators are plants that can attain high concentrations of specific metals and metalloids in their living tissues without any symptoms of physiological stress (van der Ent et al. 2013). Among this group of plants, rare earth elements (REE) hyperaccumulators have attracted recent attention because these plants could potentially be used to locate REE-enriched soils and deposits or for extracting REEs in phytomining from soil and industrial by-products and wastes, such as coal ash, red muds, mine tailings (Gaustad et al. 2021). Despite the growing importance of discovering new species of REE hyperaccumulator plants, of 721 identified hyperaccumulator plants, only two species are currently known to hyperaccumulate REEs with potential for phytomining (Reeves et al. 2017). Furthermore, most studies focused on Dicranopteris linearis (Burm.f.) Underw. (Gleicheniaceae) from China where it hyperaccumulates REEs when growing on REE mine waste soils and surrounding areas (Liu et al. 2018). REE hyperaccumulation is defined as a plant with more than 1000 µg g−1 in its leaves/fronds (Baker and Brooks 1989). The low number of identified REE hyperaccumulators is partly because REEs are present in relatively low concentrations (Tyler 2004) as well as their low bioavailability (Khan et al. 2017) in most soils. As REEs are not essential nutrients for plants, the mechanisms of REE uptake and accumulation in plants are poorly understood (Yuan et al. 2017). The roots of plants generate exudates that can strongly influence the mobility and bioavailability of REEs in soils (Khan et al. 2017). In Phytolacca americana, an REE hyperaccumulator, the roots absorb REEs via aluminium transporters and calcium channels (Yuan et al. 2017) which aligns with a study on 49 fern species that showed a postive correlation between REE and aluminium and calcium (Grosjean et al. 2019).
Discovery of REE hyperaccumulator plants elsewhere in the World requires extensive screening of plant taxa, for example, two more REE hyperaccumulators were recently discovered (van der Ent et al. 2022) after scanning 27,000 herbarium specimens originating from Australia, Papua New Guinea, New Caledonia and Malaysia (Purwadi et al. 2023). A follow-up study confirmed that these new REE hyperaccumulators (from the genus Helicia of the Proteaceae family) occur on REE-bearing rock formations in Queensland in Australia (van der Ent et al. 2022). As was previously shown, screening plants occurring on REE-rich soils will increase the likelihood of encountering REE hyperaccumulators (Purwadi et al. 2021a). Analysing herbarium specimens also assists in the endeavour to locate REEs hyperaccumulators (and/or other hyperaccumulator plant taxa) by saving time and cost to collect new samples in the field, often from remote locales (van der Ent et al. 2019a). An ideal case would be to focus on herbarium specimens originating from metal-enriched soils. However, in reality, herbarium specimens are often collected without those considerations. Furthermore, searching through millions of herbarium collections based on their location data is more challenging than simply X-ray fluorescence (XRF) scanning entire selected genera, which is the common strategy in herbarium XRF scanning campaigns undertaken thus far (Nkrumah et al. 2018; van der Ent et al. 2019b; Do et al. 2020).
Bangka Island, off the coast of Sumatra in Indonesia, has high potential for discovery of new REE hyperaccumulator plant species because the parent granitic rocks were altered during metasomatic and hydrothermal processes resulting in the enrichment of tin (Sn) and REEs bearing minerals (Schwartz and Surjono 1991), which have been weathered very intensively producing placer, off- and on-shore deposits (Schwartz et al. 1995). Since the early eighteenth century, Bangka Island has been mined for Sn (Ko 1986). In total, 1.2 million tons of Sn tailings are produced annually (Szamałek et al. 2013). REEs are not recovered and therefore the Sn mine tailings contain REEs largely as monazite and xenotime, which in turn are weathered, leading to the enrichment of REEs in the soil profile (Setiawan 2018; Zglinicki et al. 2021) with up 181 µg g−1 tREEs in soils (Syafrizal et al. 2021). These types of REE deposits and weathered REE tailings represent potential untapped REE resources (Binnemansa et al. 2013; Golev et al. 2014; Binnemans et al. 2015; Mudd and Jowitt 2016).
Given the potential of Bangka Island for discovery of REE hyperaccumulator plants, this study aimed to first screen herbarium specimens at Herbarium Bangka Belitungense to detect taxa with anomalous REE concentrations, followed by fieldwork on Bangka Island to collect plant material samples (and associated soil samples) of target species identified as having anomalous REE concentrations from the XRF survey.
Materials and methods
Study area and soil and plant sample collection
Bangka Island is located in the Southeast Asian tin belt, which stretches from Myanmar, Thailand to Malaysia and ends in West Kalimantan, Indonesia. Bangka Island and Belitung Island are often called “tin islands” because these island have made Indonesia the peak Sn producing country (United States Geological Survey 2023). Herbarium Bangka Belitungense is based at a public university on Bangka Island and was established in 2007. The date on which the herbarium specimens were collected is a crucial factor in revisiting where they were collected because old specimens collected decades or centuries ago tend to have a problem with locational accuracy. In total, 1006 specimens kept at Herbarium Bangka Belitungense were measured using XRF analysis. Each specimen was measured at least two times, one time at a young and an old leaf/frond depending on their size. For specimens with elemental anomalies, additional measurements were conducted on different parts. The raw spectra from the instrument were exported as a CSV file, and then imported into GeoPIXE software, a software package incorporating dynamic analysis used to fit and process XRF data. Then the background spectrum and elemental XRF peaks were fitted and converted into elemental concentration data as described in Purwadi et al. (2022). During this study, the XRF instrument was not fully calibrated and the output of the pipeline produced relative concentrations. Due to instrumental limitations, only the concentrations of yttrium (Y) are reported, and this was sufficient to detect specimens with anomalous REE and trace elemental concentrations as illustrated in previous studies (van der Ent et al. 2022; Purwadi et al. 2023). From the results of XRF scanning, it was found that Blechnopsis orientalis showed Y concentration anomalies. Subsequently, fieldwork sample collection focussed on B. orientalis species with anomalies from across Bangka Island. Dicranopteris linearis was also collected to compare REE concentrations in D. linearis from Bangka Island to other localities. The fieldwork location was refined based on the specimen location of B. orientalis. No roots of B. orientalis could be collected, and only young and old lamina and rachis were collected, whilst for D. linearis young and old D. linearis was taken randomly from each colony. Soil samples (250 g) were collected down to depth of 20 cm from where each D. linearis specimen was taken, but for B. orientalis, the soil sample was taken within a 1 m distance, if possible. Each plant material sample was thoroughly washed with water, then air-dried, and finally oven-dried (48 h at 60 °C). Figure 1 shows the sampling locations, and Fig. 2 shows the target species D. linearis and B. orientalis field. Upon importation into Australia, all of the soil and plant samples were gamma irradiated (50 kGy) at Steritech Pty. Ltd. in Brisbane following Australian Quarantine Regulations.
Soil and plant elemental analysis
All of the dried soil samples were sieved through a 2 mm screen and sub-samples were weighed to 100 ± 5 mg in quartz digestion vessels, and 5 mL HNO3 (70%) and 2 mL HCl (37%) was added (Wang and Brindle 2014; Han et al. 2021). Each sample was then digested for 15 min. at 80% power using a ColdBlock system (CB15S 15 channel system, ColdBlock Technologies Inc). The digestates were transferred to 50 mL tubes and made to volume (40 mL) with ultra-pure water (Millipore 18.2 MΩ·cm at 25 °C) and filtered (Whatman® Grade 1 filter paper) before analysis with inductively coupled plasma atomic emission spectroscopy (ICP-AES, as described below). The plant material samples were manually ground to a fine powder using a mortar and pestle and weighed to 100 ± 5 mg in 6 mL polypropylene tubes. Then 2 mL HNO3 (70%) was added to each sample and left for 24 h before being digested in a block heater (Thermo Scientific™ digital dry bath) for a 2-h program (1 h at 70 °C followed by 1 h at 125 °C) and brough to volume (40 mL) with ultrapure water before analysis with ICP-AES. The acid digestates were analysed with a Thermo Scientific iCAP 7400 instrument for macro-elements (Ca, K, Mg, Na, P), trace-elements (Al, As, Co, Cr, Cu, Fe, Ga, In, Mn, Ni, Pb, Ti, Zn), and REEs (Ce, Dy, Er, Eu, Gd, Ho, La, Lu, Nd, Pr, Sm, Tb, Tm, Y, Yb), in radial and axial mode depending on the element and expected analyte concentration. Quality controls included matrix blanks, certified reference material (Sigma-Aldrich Periodic table mix 1 for ICP TraceCERT®, 33 elements, 10 mg L−1 in HNO3) and Standard Reference Material NIST 1570a Trace Elements in Spinach Leaves digested as described above for the plant and soil materials.
Laboratory micro-X-ray fluorescence elemental mapping (micro-XRF)
Several B. orientalis frond samples were selected based on their REEs and As concentrations measured using portable XRF instrument. These selected specimens were mounted between sheets of 6 μm Ultralene thin film on a micro-XRF motion stage and scanned in a modified ATLAS X instrument (IXRF, Inc.) at the Centre for Microscopy and Microanalysis, the University of Queensland, Australia. The instrument is a custom-built system which incorporates two 50 kV–1000 μA sources fitted with polycapillary focussing optics. An XOS microfocus Mo-target tube producing 17.4 keV X-rays (flux of 2.2 × 108 ph s−1) focussed to 25 μm was used here. The micro-XRF spectra were acquired in mapping mode controlled using Iridium (IXRF, Inc.) software and the data processed in GeoPIXE software (Ryan 2000; Ryan et al. 2005) post hoc.
Scanning electron microscopy with energy‑dispersive spectroscopy (SEM–EDS)
One of the B. orientalis frond samples was freeze-dried (Thermoline), mounted on an Al-stub, sputter-coated with carbon and imaged using scanning electron microscopy with energy-dispersive X-ray spectroscopy (Hitachi SU3500) with 100–1000-fold magnification and 5 and 15 kV electron voltage. The lower accelerator energies were used for imaging using only secondary electron returns and higher accelerator energies for backscatter mode imaging and EDS point analyses. The data were analysed with AZtecEnergy Microanalysis software.
Statistical analysis
The distribution of REEs follows the Oddo-Harkins rule which represents a zigzag pattern in which even atomic numbers of REEs are more abundant than those with odd atomic numbers (Ramos et al. 2016). Anomalous REE concentrations are normalised to chondritic abundance, a theoretical abundance of an element when the universe is formed (O’Neill 2016) and here we use the values provided in Taylor and McLennan (1995) to interpret soil REE concentrations.
Results
Herbarium XRF scanning for REE detection
In the herbarium XRF scanning 1006 specimenskept in Herbarium Bangka Belitungense were analysed, and 617 species were identified and after processing the raw XRF spectra, Y concentration anomalies (>50 µg g−1) were detected in two species, namely, Dicranopteris linearis and Blechnopsis orientalis.
Rare earth element concentrations in Blechnopsis orientalis and Dicranopteris linearis and associated soils
The XRF scanning of herbarium specimens at Herbarium Bangka Belitungense led to the discovery of specimens with 1000 µg g−1 > REE concentrations in B. orientalis (L.) C.Presl. This taxon was previously known as Blechnum orientale (L.) and is widespread in Southeast Asia (de Gasper et al. 2016, 2017; Schuettpelz et al. 2016). The fieldwork then focussing on B. orientalis. In addition, D. linearis was also collected to evaluate the hyperaccumulation traits of this species in Bangka Islands compared to elsewhere. Compared to upper continental crust abundance, the average concentration of Sc, Y, Eu, Ho, Er, and Lu in soils showed negative anomalies, while positive anomalies were observed in La, Ce, Pr, Nd, Sm, Gd, Tb, Dy, Tm, and Yb Fig. 3. Scatter plots of total REEs concentrations in soils and in B. orientalis and D. linearis (Fig. 4) reveal that there are no clear correlations between total REEs concentrations in soils and the old rachis, old pinna, young rachis, and young pinna of both fern species. In Figures S1 and S2, soil samples were grouped into two clusters based on their elemental composition after principal component analysis, and each plant was assigned to the same group as its corresponding soil sample, but no significant correlation between soil total REE concentrations and shoot concentrations was observed. Several samples of B. orientalis and D. linearis contained total REEs concentrations > 1000 µg g−1 whereas the soil had a total REE concentration < 10 µg g−1. When comparing the mean and maximum REEs concentrations, the old pinna of B. orientalis had higher concentrations of all REEs than D. linearis (Table 1). For example, up to 930 µg g−1 Y in B. orientalis and 350 µg g−1 Y in D. linearis (Table 1). On average, the translocation of REEs in both B. orientalis and D. linearis follows a pattern with higher concentrations in the old pinna, followed by young pinna, young rachises/petioles, but the magnitude of translocation differs (Fig. 5). Blechnopsis orientalis tends to translocate REE more to old pinna compared to D. linearis, but the translocation rate of D. linearis from old rachis to young pinna is higher than that in B. orientalis. The REE concentrations are shown in Fig. 6 and old pinnae of B. orientalis exceeds the REE hyperaccumulator threshold (1000 µg g−1), confirming that it is an REE hyperaccumulator as previously reported (Liu et al. 2018). In addition to REE concentrations, macronutrients and trace elements are given in Table 2 which shows that B. orientalis has higher macronutrient concentrations compared to D. linearis with on average B. orientalis have at least twice the P, K, Mg and Ca concentrations in that of D. linearis. Aluminium, which is toxic to most plants, was accumulated by some D. linearis up to 8000 µg g−1, while some B. orientalis up to 790 µg g−1. It was also found that the old pinna of a B. orientalis sample contain As up to 2100 µg g−1 whilst D. linearis has < 10 µg g−1 As in (Table 3). The As concentrations in soils, had an average and maximum of 34 µg g−1 and 273 µg g−1 respectively. Three B. orientalis samples taken from the same vicinity had As concentrations up to to 2100 µg g−1 while the mean soil As concentration was 34 µg g−1.
Elemental distribution in Blechnopsis orientalis pinnules and contamination
Blechnopsis orientalis pinnae were screened with portable XRF and samples with REE anomalies were selected for subsequent micro-XRF and SEM-EDS analysis. Of the REEs, only La could be analysed, as the micro-XRF cannot excite any K-lines of elements Z > La, whilst the L-lines of the REEs suffer from line-overlaps with the first-row transition metals. As can be seen in Fig. 7, La concentrates at the edge of the pinnules. Across different pinnules of B. orientalis, the sample at the right side has an As anomaly, and ICP-AES results confirmed that this pinna had 2100 µg g−1 As. Field collected plant material samples are often prone to surficial contamination by soil particulates (Gei et al. 2018), and the pinnules of B. orientalis were subjected to surface examination using SEM-EDS analysis. Figure 8 shows that no discernible surface contamination can be observed on the B. orientalis pinnule surface and no signals from REEs or As could be detected.
Discussion
This study used portable XRF analysis to screen herbarium collections at Herbarium Bangka Belitungense leading to the discovery of B. orientalis as a hyperaccumulator of REEs. Field collected samples revealed that B. orientalis can also hyperaccumulate As. In a recent XRF screening study conducted at the herbarium of Muséum national d'Histoire naturelle (MNHN, Paris, France) B. orientalis from other localities in Southeast Asia were found to hyperaccumulate REEs up to 4200 µg g−1 (Gourdard et al. 2024). In this study, B. orientalis had total REEs up to 2900 µg g−1, which is almost three times the REE hyperaccumulator threshold of 1000 µg g−1 and As up to 2100 µg g−1, which is twice the As hyperaccumulator threshold of 1000 µg g−1. The fractionation of REEs in B. orientalis follows the same trend as found in a recently reported REE hyperaccumulator, Helicia glabriflora, in which old fronds contain more REEs than young fronds, indicating strong translocation and distribution limitation of REEs from mature to young fronds (van der Ent et al. 2022). Lanthanum, one of REEs, accumulates at the margins of B. orientalis pinnules. Compared to D. linearis, REEs were highest at necrotic lesions (Liu et al. 2020, 2021). In addition to accumulating in the pinnule margin, As also accumulated in midveins, and K had a similar pattern. A study of As hyperaccumulators reported that As can induce increased K in fronds (Tu and Ma 2005). Arsenic hyperaccumulation is known from ferns, such as Pityrogramma calomelanos and Pteris vittata (Ma et al. 2001; Visoottiviseth et al. 2002), and a study suggested that other ferns species may hyperaccumulate As (Zhao et al. 2002). In, B. orientalis we record the first fern species to hyperaccumulate As outside the Pteridaceae, Pteris and Pityrogramma genera. Compared to the two previously known As hyperaccumulator plants, B. orientalis has relatively higher biomass. Pteris vittate is the first reported As hyperaccumulators, and together with other species from Pteridaceae, they hyperaccumulate and tolerate As (Gumaelius et al. 2004; Xie et al. 2009). In P. vittata, arsenate is taken up by phosphate transporters (Indriolo et al. 2010; Ditusa et al. 2016), and B. orientalis may also have a similar behaviour as shown in Fig. 7, in which the sample shows high intensities of P and As. The regression analysis of total REEs concentration in soil and ferns revealed no significant (positive) correlations. The ferns can attain > 1000 µg g−1 when growing in soils with < 10 µg g−1. This phenomenon aligns with a broader study's proposition (Stein et al. 2017), suggesting that the accumulation of metals in plants is not solely dictated by soil type. This implies that, even within similar soil environments, the accumulation of metals can exhibit divergence, a phenomenon highlighted by the existence of within-population variation. This variation underscores the intricate nature of ecological adaptation in response to metal presence, potentially indicating an adaptive response to the distinct challenges posed by these metals. Compared to D. linearis, B. orientalis is large and fast-growing and a stronger REE hyperaccumulator. In addition, D. linearis tends to colonize open barren areas and whereas B. orientalis grows in wetter shaded areas. This differential habitat preference contributes to these fern species ecological diversity and specialization. Given the high growth and REE hyperaccumulation characteristics of B. orientalis, it has a potential for phytomining (agromining), but further research and exploration are necessary to determine the full potential and suitability for this purpose.
To date, most of the research on D. linearis and REE hyperaccumulation has been undertaken in China where this species grows on REE mine sites. This study revealed similar concentration patterns in which the fern hyperaccumulates aluminium and REEs (Liu et al. 2019). This result further supports the suggestion that REE hyperaccumulation is a constitutive trait of D. linearis (Koyama et al. 1987; Zhenggui et al. 2001; Purwadi et al. 2021b), with the hyperaccumulator trait of D. linearis a common characteristic across its distribution range, beyond China.
Data Availability
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.
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Acknowledgements
We would like to express our sincere gratitude and appreciation to the Ministry of Energy and Mineral Resources, Indonesia, and PT Timah Tbk for their invaluable support throughout our fieldwork activities and their permission for analysing the collected samples in our lab. We would like to extend special thanks to Mr. Firmansyah Adi Prianto from the Ministry for his guidance and help from the early stage of fieldwork to the presentation of this study. We would like to express our gratitude to Mr Angga Widya Yogatama from PT Timah Tbk for his invaluable insights and recommendations that greatly contributed to refining the selection of my fieldwork area. We are grateful to the Herbarium Bangka Belitungense for allowing examination and sampling of its herbarium specimens. Additionally, we extend our heartfelt thanks to Mr. Tegar Dwi Santoso for his assistance during the fieldwork. Also, we thank Mr. Vinod Nath for his help during lab work, and Dr Amelia Corzo-Remigio for her help during SEM analysis. We also acknowledge the expertise and support provided by Dr Lachlan W. Casey and Microscopy Australia at the Centre for Microscopy and Microanalysis, at the University of Queensland for the micro-XRF analysis.
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Open Access funding enabled and organized by CAUL and its Member Institutions. Imam Purwadi was the recipient of an Australian Government Research Training Program Scholarship at The University of Queensland, Australia.
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IP, AVDE, and PDE conceived the presented idea. EN prepared and measured herbarium specimens and identified local plant species. ACR performed SEM analysis. IP, BPH, and TRW conducted fieldwork. All authors discussed and wrote the manuscript.
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Purwadi, I., Erskine, P.D., Hutahaean, B.P. et al. Rare earth elements (REEs) in soils and plants of Bangka Island (Indonesia) focussing on (hyper)accumulation. Plant Soil (2024). https://doi.org/10.1007/s11104-024-06735-2
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DOI: https://doi.org/10.1007/s11104-024-06735-2