# Relationship between the distribution of rare earth elements in soil pools with plant uptake: a sequential extraction study

Kaisa Forsyth, Aline Dia, Rosa Marques, Maria Isabel Prudêncio, Cynthia Obregón-Castro, Catarina Diamantino, Edgar Carvalho, Maxime Pattier, Mélanie Davranche, Mathieu Pédrot

► To cite this version:

Kaisa Forsyth, Aline Dia, Rosa Marques, Maria Isabel Prudêncio, Cynthia Obregón-Castro, et al. Relationship between the distribution of rare earth elements in soil pools with plant uptake: a sequential extraction study. Plant and Soil, 2025, 512, pp.1137-1152. 10.1007/s11104-024-07135-2. insu-04866127

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# Relationship between the distribution of rare earth elements in soil pools with plant uptake: a sequential extraction study

Kaisa Forsyth · Aline Dia · Rosa Marques · Maria Isabel Prudêncio · Cynthia Obregón-Castro · Catarina Diamantino · Edgar Carvalho · Maxime Pattier · Mélanie Davranche · Mathieu Pédrot

Received: 26 July 2024 / Accepted: 4 December 2024
© The Author(s) 2024

## Abstract

*Background and Aims* Many studies have considered whether all forms of rare earth elements (REEs) in the soil are potentially bioavailable. The general consensus is that the exchangeable and carbonate-bound mineral pool is bioavailable. However, within the rhizosphere, site-specific geochemical conditions and biological weathering (due to plants, animals and

microbes) may cause insoluble pools of REEs in the soil to become plant bioavailable.

*Methods* This study categorized soil into four fractions using the Community Bureau of Reference (BCR) sequential extraction method. The geochemical associations of REEs with soil fractions were assessed to determine which mineral and organic pools were most bioavailable by comparing the similarity of REE fractionation patterns in local plant tissues with the BCR extraction results for compatible soils.

*Results* The results showed that the residual or more recalcitrant fraction of the soil displays a convex REE pattern with distinct depletion of middle REEs (MREEs) compared with light REEs (LREEs) and heavy REEs (HREEs). Some evidence suggested that Eu may be excluded by plants, as anomalous Eu concentrations were observed when the belowground plant tissue concentrations were normalized to the BCR extraction data.

*Conclusions* This study demonstrates that the REEs in belowground plant tissue are closely related, not only to exchangeable and carbonate-bound phases, but also to reducible and oxidizable soil fractions. According to the REE patterns, MREEs are more mobile than LREEs and HREEs, indicating enhanced bioavailability of MREEs.

**Keywords** Sequential extraction · Rare Earth elements · Plant · Soil · Water · Bioaccumulation

**Supplementary Information** The online version contains supplementary material available at https://doi.org/10.1007/s11104-024-07135-2.

Responsible Editor: Antony Van der Ent.

K. Forsyth (✉) · A. Dia · M. Pattier · M. Davranche · M. Pédrot
Géosciences Rennes, UMR 6118 CNRS, Univ. Rennes, Rennes 35000, France
e-mail: kaisa.forsyth@gmail.com

R. Marques · M. I. Prudêncio · C. Obregón-Castro
Centro de Ciências e Tecnologias Nucleares, Instituto Superior Técnico, Universidade de Lisboa, Bobadela 2695-066, Portugal

R. Marques · M. I. Prudêncio
Departamento de Engenharia e Ciências Nucleares (DECN), Instituto Superior Técnico, Universidade de Lisboa, Bobadela 2695-066, Portugal

C. Diamantino · E. Carvalho
EDM - Empresa de Desenvolvimento Mineiro, S.A., Lisboa 1070-050, Portugal
Introduction

Rare earth elements (REEs) are technology-critical
elements (Van Gosen et al. 2017). Increasing evi-
dence of their toxicity and prevalence in the biosphere
indicates that they pose a risk to human and environ-
mental health (Gong et al. 2021; Li et al. 2013; Mer-
schel and Bau 1995; Pagano et al. 2015; Rim et al.
2013; Wakabayashi et al. 2016). These 14 elements of
the lanthanide series typically adapt to a +3 oxidation
state, with the exception of Ce, which can be oxidized
to +4 and Eu, which can be reduced to +2. Another
common attribute is the filling of the 4f electron shell,
which results in insufficient shielding of the nucleus
and ultimately a contraction of the atomic radius. Due
to this lanthanide contraction phenomenon, REEs are
accepted in isomorphic substitution with similarly
sized elements such as Ca (Shannon 1976). Minor
differences in how these elements interact with sur-
faces and compatible ligands contribute to their par-
titioning and fractionation behavior in the soil. It is
therefore convenient to categorize REEs as light
REEs (LREEs) (La to Nd), middle REEs (MREEs)
(Sm to Tb), and heavy REEs (HREEs) (Dy to Lu).

As lithophilic elements, REEs typically have lim-
ited solubility. Exceptions to this trend are found in
environmental conditions where a low pH develops
and metal solubility increases (Baker et al. 1990;
Pérez-López et al. 2010; Prudêncio et al. 2015; Soyol-
Erdene et al. 2018). The contributions of different
mineral pools to total REEs in the soil are described
in Migaszewski and Gałuszka (2015), who estimated
that 43% of all REEs are associated with silicate min-
erals, 23% with carbonates, 14% with oxides, and
14% with phosphates and oxyhydroxides. Although
the contribution of REEs from soil organic matter
was not quantified by Migaszewski and Gałuszka
(2015), other studies have shown that the organic
pool contributes between 1.84 and 26.5% of the REEs
in soil (Pang et al. 2002).

Given that these complex biogeochemical inter-
actions dictate the bioavailability of not only REEs,
but all elements in rhizosphere, predicting the origin
of elements found in plants is a challenge. Brioschi
et al. (2013) theorized that the preferential uptake of
LREEs can be summarized as follows: (1) preferen-
tial precipitation of HREEs over LREEs into Fe-oxy-
hydroxide minerals (suggesting that Fe-oxyhydroxide
mineral-associated fraction is fixed and generally not

bioavailable) and (2) preferential uptake of free and
non-complexed cations (LREEs) by plants. Although
there is a general consensus that the dissolved pool
and easily exchangeable cations are bioavailable and
pose the greatest threat to local ecology (Liang et.
2005; Pérez-López et al. 2008), this pool is often
minimal in comparison with the sum of elements
found in plant tissue (Liang et al. 2005).

A possible explanation for this disparity is that
plants affect nutrient solubility and further weather
the surrounding soil matrix (Stille et al. 2006) by
altering pH and redox potential and producing bio-
genic exudates (Liang et al. 2008; Wyttenbach et al.
1998b). Manipulation of rhizosphere conditions
can even extend outside the plant, with symbiotic
microbes playing a major role in nutrient extrac-
tion and limiting the impacts of metal toxicity for
plants (Kong and Glick 2017; Sessitsch et al. 2013).
In particular, the literature describing the solubiliza-
tion of REEs by low-molecular-weight organic acids
(LMWOA) and humic/fulvic acids (Dia et al. 2000;
Pourret et al. 2007; Tang and Johannesson 2003;
Tyler 2004; Wiche and Pourret 2023) suggests that
the bioavailable pool should be expanded to include
REEs associated with other pools of soil minerals and
organic matter, which are classically considered less
labile.

The Community Bureau of Reference (BCR)
sequential extraction is typically used for environ-
mental risk assessment and for predicting the origin
and fate of polyvalent cations in soil (Ure et al. 1993).
Selective partitioning of the soil enables the identi-
fication of metals associated with the (1) exchange-
able and carbonate-bound, (2) oxidizable, (3) reduc-
ible, and (4) residual soil fractions. Knowledge of the
distribution of REEs within these phases provides
insight into their behavior and fate. Many studies
have attempted to use BCR and other soil extraction
methods to predict the toxicity and bioavailability of
REEs and other trace metal contaminants (Kubová
et al. 2008; Liang et al. 2005; Pang et al. 2002; Shan
et al. 2003; Wang et al. 2001a, b; Wyttenbach et al.
1998a; Zhang and Shan 2001). Kubová et al. (2008)
used BCR extraction to compare the bioavailability
of nine different elements in plants. Ultimately, they
concluded that the results of sequential extraction
alone are not a pertinent predictor of bioavailability,
but this method could be used to qualitatively deter-
mine the relative amounts of plant-available elements.
Although the geochemical fractionation of REEs is not a good predictor of bioavailability on its own, this approach can be used to predict which soil REE fractions are vulnerable to solubilization. Solubility is a major barrier to bioavailability in the rhizosphere, thus this potentially soluble pool can approximate a bioavailable pool. Based on previous studies, REEs are likely geochemically partitioned before entering plant tissues (Brioschi et al. 2013; Forsyth et al. 2023; Gonzalez et al. 2014; Tyler 2004). Rare earth elements are a physicochemically uniform group of elements that should undergo similar biogeochemical reactions (Gonzalez et al. 2014). Slight differences in their interactions with compatible ligands, their redox chemistries, and their atomic radii lead to the fractionation of individual elements into different soil phases. Therefore, a sequential extraction scheme can be useful to compare the lability and recalcitrance of different REEs against each other. This information can then be used to determine which elements exhibit the highest potential for phytoavailability and the conditions that promote this.

The current literature relating REE chemical fractionation within soils to plant phytoavailability is limited. Many studies have quantified only a subset of REEs, instead of the entire series (Shan et al. 2003; Wang et al. 2001b; Wyttenbach et al. 1998b; Xinde et al. 2000; Zhang and Shan 2001), and often, these studies focus on aboveground plant tissue rather than belowground tissue (Wang et al. 2001b; Wyttenbach et al. 1998b; Xinde et al. 2000). However, the biological partitioning of REEs from belowground to above ground tissues has been well documented (Forsyth et al. 2023; Liang et al. 2008; Tyler 2004). The partitioning of REEs into aboveground tissue, while not observed across all specimens, seems to be related to plant species endogeny rather than the bioavailability of the REEs (Liang et al. 2008; Tyler 2004). For this reason, the current study focuses on relating the chemical fractionation of REEs in soils to the REE contents in belowground tissue rather than aboveground tissue, with further studies planned to assess the mechanisms and effects of biological partitioning of REEs in plants.

This study uses a BCR sequential extraction scheme to investigate the sources of REEs in plant tissues collected from three distinct legacy mining sites in Portugal. Study sites were selected based on their geochemical background. Generally, the

environmental conditions of these sites promote the dissolution of polyvalent cation-bearing minerals. As REEs are ubiquitous elements in the Earth's crust (Taylor and McLennan 1985), incidental release of geogenic REEs can be promoted by the Acid Mine Drainage (AMD) conditions formed in mining sites, like those selected (Ferreira da Silva et al. 2009; Pérez-López et al. 2010; Prudêncio et al. 2015; Soyol-Erdene et al. 2018). Many studies having demonstrated that REE solubility is high in such areas (Grawunder et al. 2014; Pérez-López et al. 2010). Soils and sediments sequentially extracted in this experiment correspond to samples reported by Forsyth et al. (2023), which published a survey of total REE concentrations in water, soil, and plant samples from the three legacy mining sites selected for this study. The BCR sequential extractions are contextualized using the total concentration of REE in plants and soils/sediments presented in Forsyth et al. (2023).

## Materials and methods

### Site description

Samples were collected in November 2020 from three mining sites: Lousal, São Domingos, and Quinta do Bispo (Portugal). A detailed description of the sample collection and processing procedures can be found in Forsyth et al. (2023), which presents a comprehensive survey of the concentrations of REEs and their associations in surface waters, soils/sediments, and belowground and aboveground plant tissues. The following section details the current knowledge on the mineralogy of these sites and describes the procedures used to determine the chemical fractionation of soils/sediments.

### Lousal

Lousal mining operations occurred along the Sado Valley Fault, an area of volcanic deposition with major hydrothermal alteration (Morais et al. 2020) that resulted in volcanic sedimentary complexes (VSCs) emblematic of the Iberian Pyrite Belt (IPB). The area features bimodal volcanic rocks with massive sulfide lenses (predominantly composed of pyrite with lesser amounts of chalcopyrite, galena, sphalerite, pyrrhotite, marcasite, bournonite, tetrahedrite,
arsenopyrite, cobaltite, magnetite, and gold; Luís
et al. 2011) and carbonate veins. Mantle melting
is assumed to be responsible for the characteristic
enrichment of Eu and Tb and the depletion of Sc,
Al, and Ti in the felsic and intermediate geology
(Morais et al. 2020). Devonian shales and quartzites
from the Corona Formation (Luís et al. 2011; Matos
et al. 2014) and other post-Mesozoic materials over-
lie a Paleozoic basement (Oliveira et al. 2001) in the
area surrounding the mine's passive treatment system.
This treatment system is located near the confined
waste piles, which produces AMD, and successfully
treats effluents for sulfates, arsenic, aluminum, iron,
copper, and chromium before confluence with the
nearby Corona River (Empresa de Desenvolvimento
Mineiro [EDM] and Direcção Geral de Energia e
Geologia [DGEG], 2011). Metal-enriched effluents
progress through the 17-basin treatment system,
where the pH slowly increases along the reach, caus-
ing the precipitation of secondary minerals with fur-
ther stabilization of metals supported by the aerobic
wetland system. Lousal was the only study site that
contained a passive treatment system for AMD efflu-
ent in the sampling period.

Two aquatic sediment samples were collected from the Lousal site: L-01, which corresponds to sediment collected from a stock pond outside the mining area, i.e. in the fresh water from the Albufeira da Barragem da Tapada reservoir; and L-02, which is aquatic sediment collected from the 6th treatment basin, where the aerobic wetland basins begin.

São Domingos

Similar to Lousal, São Domingos is hosted in the IPB
of southern Portugal. The exploitation of iron-sulfide
ores along with in copper, lead, zinc, and sulfur over
time has led to the continual generation of AMD at
this site (Álvarez-Valero et al. 2008). Although the
dominant ore composition is pyrite, with heterogene-
ous arrangements of chalcopyrite, galena, and sphal-
erite (Durães et al. 2017), long-term usage of this
site has led to the development of many secondary
minerals along the São Domingos river valley. Sec-
ondary minerals are typically formed from the super-
saturation of various metal species associated with
AMD. They include Fe-oxide gossans (goethite and
hematite) along with sulfate salts such as alunogens,
as well as calcite, clinochlore, gypsum, jarosite, and

schwertmannite (Durães et al. 2017; Ferreira et al. 2021). Much of the mining waste materials have been characterized previously by Álvarez-Valero et al. (2008), who focus on the mineralogical and chemical composition, and Pérez-López et al. (2008), who performed a sequential extraction on the materials characterized by Álvarez-Valero et al. (2008) to identify the risks posed by various trace and major elements. Neither paper described the REE contents.

Three soil samples were collected from the São
Domingos River Valley: SD-01, SD-02, and SD-03.
The soil corresponding to SD-01 was retrieved from
outside the mining area, close to the Albufeira da
Tapada Grande dam. The soil around this reservoir
represents the background lithology (Quental et al.
2002) and is weathered from shales of the Represa
Formation, felsic and mafic volcanic rocks, and
black shales (Pereira et al. 2008). Soils SD-02 and
SD-03 were collected along the São Domingos river
valley in areas previously identified by Pérez-López
et al. (2008) as being landfilled with heavily sili-
ceous and inert material. Despite the use of a rela-
tively inert material (up to 90% quartz according to
Pérez-López et al. 2008), vegetation in the area is
still sparse, presumably due to the presence of sec-
ondary precipitates on the soil surface after runoff
(Ferreira et al. 2021).

Quinta do Bispo

Unlike São Domingos and Lousal, Quinta do Bispo is
hosted in Variscan granites and pre-Cambrian meta-
sediments (Ramalho et al. 2009). Previous studies
have characterized the granitic rocks of Quinta do
Bispo as (1) coarse-grained, (2) medium-grained, and
(3) medium-fine-grained monzonitic two-mica gran-
ites (Matos-Dias and Costa 1972; Barbosa 2012 and
references therein). Deposits of uranium oxides and
uranium phosphates are associated with hydrothermal
deposition into stockworks (Barbosa 2012). Meta-
somatic albitization of felspars and chloritization of
biotite are evident in cores taken from the area (Bar-
bosa 2012). Previous studies of the area have attrib-
uted Eu anomalies to the albitization of plagioclase
minerals (Cardenas et al. 2023; Forsyth et al. 2023),
where Ca²⁺ and Eu²⁺ incorporated in plagioclases
are metasomatically displaced, resulting in positive
Eu anomalies corresponding to uranium ores and negative Eu anomalies corresponding to the altered material.

Although manganese oxides, pyrite, and arsenopyrite have been associated with the mineralogy of Quinta do Bispo, the dominant ore mineralogy comprises autunite and torbernite (Cardenas et al. 2023). Uranium was extracted from these ores between 1979 and 1987. The original ores were exploited at the Quinta do Bispo site and processed in Urgeiriça (Pereira et al. 2014). However, after 1992, the open pit at Quinta do Bispo was used for in situ leaching (ISL) of low-grade ores; thus, the site is impacted by acidic wastewaters that are isolated in an open pit awaiting treatment.

Seven soil samples corresponding to three distinct geological units were collected from the Quinta do Bispo site. Samples QB-01 and QB-01b represent soils collected from outside the mining area, with similarly medium-grain granite as in mining area. Samples QB-02 and QB-02b represent a large waste rock pile on site and thus should reflect uranium enrichment consistent with the exploited material. Samples QB-03, QB-04, and QB-04b correspond to the alluvium formed by an ephemeral stream, reflecting weathering from materials in the surrounding drainage basin. Samples QB-01b, QB-02b, and QB-04b are distinct from the other samples collected at Quinta do Bispo because they represent bulk material that was not collected from a plant rhizosphere. These samples were collected to compare the rhizosphere environment to that of the bulk soil.

## BCR extraction procedure

Chemical fractionation was determined using the standard three-step BCR extraction scheme established by the Standard Measurements and Testing Program of the European Community (Ure et al. 1993). BCR extraction partitions soil into three fractions defined as the “easily exchangeable and carbonate-bound” (exchangeable), “reducible mineral” (reducible), and “oxidizable mineral and organic matter” (oxidizable) soil fractions. The soil fraction that remains can then be calculated using Eq. 1, where the sum of the elements associated with the three sequential extraction fractions is subtracted from the total concentration of elements in the soil to determine the remaining amounts, including

REEs, in the residual fraction, which corresponds to a more recalcitrant pool of REEs.

$$REE_{\text{Resid.}} = REE_{\text{soil/aquatic sediment}} - (REE_{\text{exchangeable}} + REE_{\text{reducible}} + REE_{\text{oxidizable}}) \quad (1)$$

All materials were prepared in a clean room and decontaminated using nitric acid (1.5 M HNO₃) washing for 24 h at 45 °C, followed by 24 h washing with ultrapure water (18 MΩ-cm) at 45 °C. Approximately 0.5 g of soil was added to a decontaminated 50 mL centrifuge tube, with the reagents and agitation times are reported in Table 1. The supernatant resulting from each extraction step was separated by centrifugation and filtered through a 0.2 µm polyethersulfone (PES) filter before analysis. Carbon from the reagents used in each of the sequential extraction steps was digested in preparation for inductively coupled plasma–mass spectrometry (ICP–MS) analysis. Concentrated HNO₃ was used to digest the carbon associated with the “exchangeable and carbonate-bound” and “oxidizable minerals and organic material” extracts, while a combination of HCl and HNO₃ was used to digest the carbon in the “reducible mineral” extracts.

## Plant tissue data

The soils studied by sequential extraction were collected as part of a campaign to catalog REE concentrations in plants, soils, sediments, and waters of mining sites. A large amount of background information pertaining to these samples is published in Forsyth

<table><caption>**Table 1** Modified sequential extraction procedure (Ure et al. 1993)</caption><thead><tr><td>Target Fraction</td><td>Reagent</td><td>Time</td></tr></thead><tbody><tr><td>BCR 1: exchangeable</td><td>40 mL of 0.11 M acetic acid solution</td><td>16 h</td></tr><tr><td>BCR 2: reducible</td><td>40 mL of 0.5 M hydroxylamine hydrochloride adjusted to pH 1.5</td><td>16 h</td></tr><tr><td>BCR 3: oxidizable</td><td>Predigestion at 85 °C using 20 mL 8.8 M hydrogen peroxide 50 mL of 1 M ammonium acetate adjusted to pH 2</td><td>N/A<br>16 h</td></tr></tbody></table>

<footnote>*N/A indicates a time that was determined by the rate of sediment digestion and was not confined to any particular time window</footnote>
et al. (2023). The soils tested matched to plant samples, which included the species: *Cistus ladanifer*, *Typha latifolia*, *Juncus acutus*, *Pteridium aquilinum*, *Retama sphaerocarpa*, and *Salix sp*. Biota varied among sites, none of the plants grew in all three collection sites. Plants were collected from within a 1 m grid in the locations detailed in each site description. For this study only the belowground plant tissue data was used to determine the uptake of REE from BCR fractions, aboveground tissue was excluded as partitioning of REE occurs between uptake and assimilation into aboveground tissues. The belowground tissue mass includes: roots, rhizomes, and any transition material from roots to stem that were beneath the soil. Belowground tissue was processed using multiple washes with deionized water (18 MΩ-cm) followed by drying at 50 °C in an oven for 4 days and grinding using a zircon ball-mill. Belowground plant samples were then digested using a microwave (Anton Paar Multiwave 7000) digestion method. Tomato leaves standard 1573a (NIST® SRM®) was used as a reference material and digestions were performed in triplicate. Though there is no certified reference values for REEs in 1573a NIST, there are values without approximated errors reported for La, Ce, Gd, and Sm. Recovery rates for the reported REE were within 17% and all of the REE concentrations recorded for the triplicates were within 5% of eachother.

## Rare earth element analysis

The REE concentrations in the sequential extraction solutions and digestions were measured using a quadrupole ICP-MS (Agilent Technologies 7700×). The matrix of each sequential extract was acidified to match a 0.37 M HNO₃ concentration. The instrument was tuned to account for oxide and double-charged ion formation, normal plasma conditions were used (no gas mode). The concentrations were determined using a conventional 7-point external calibration procedure using multielemental solutions acidified in a 0.37 M HNO₃ matrix with online introduction of a Rh internal standard. Rhodium was introduced to correct for instrumental drift and possible matrix effects. The international geostandard SLRS-6 was used to check the validity and reproducibility of the results (Yéghicheyan et al. 2019). The typical uncertainties, including all error sources, were below ±5% for all the REEs.

The detection limits were calculated following the AFNOR protocol, and values of <0.25 ppt (ng L⁻¹) were obtained for all REEs. Interference from Ba-oxides and REE-oxides were accounted for using the methods reported in Aries et al. (2000), and corrections were applied to REEs with a mass greater than that of Sm. The above procedures are standard in analyses at the University of Rennes analytical platform, and similar protocols were employed by Davranche et al. (2004), Pédrot et al. (2009), and Forsyth et al. (2023) to obtain REE concentrations in waters, soils, sediments, and plant tissues.

Elements were categorized as LREEs (La-Pm), MREEs (Sm-Tb), and HREEs (Dy-Lu). Since both Ce and Eu can exhibit fractionation and anomalous concentrations due to their additional oxidation states, their behavior was described using linear extrapolation of the soil-normalized REE data (Eqs. 2 and 3, respectively), where Ce/Ce* represents the cerium anomaly and Eu/Eu* represents the europium anomaly; the greater this value varies from 1, the more anomalous the concentration is.

$$Ce/Ce^* = \frac{2(Ce)}{La + Pr} \qquad (2)$$

$$Eu/Eu^* = \frac{2(Eu)}{Sm + Gd} \qquad (3)$$

## Results

### REE fractionation in legacy mining sites

The concentration in µg kg⁻¹ of the REE associated with each BCR fraction can be found in Table S1 of the supplementary materials. The REE fractionation, expressed as a percentage of the total soil REEs, is shown in Table S2 which is provided in the supplementary materials. Figure 1a and c demonstrate the REE fractionation for each soil sample (the data are normalized to the total soil REEs and are plotted on a log scale). These figures can be used to interpret the fractionation of individual REEs in soil. For all samples, the majority of the REEs are associated with the residual fraction, demonstrating the relatively recalcitrant and conservative behavior
**Fig. 1** Log-scale plots of the relative contents of individual REEs in the (a) exchangeable (b) reducible, and (c) oxidizable fractions after normalization to the total soil/sediment content. Plot (d) expresses the contents of REEs in the residual fraction as percentages and is not log scaled. Dashed lines correspond to samples taken from outside the mining areas. Samples from São Domingos are indicated by triangles, samples from Quinta do Bispo are indicated by circles, and samples from Lousal are indicated by squares

<figure><img src="image_2.png" /></figure>

of these elements. Middle REEs are enriched in the exchangeable (Fig. 1a), reducible (Fig. 1b), and oxidizable (Fig. 1c) soil fractions. This enrichment is complemented by the slight depletion of MREEs plotted in Fig. 1d, which plots the soil-normalized residual REE content.

## Lousal

Figure 2a displays the contents of REEs associated with sediments collected from inside and outside the passive treatment system at Lousal. The aquatic sediment collected from Lousal had the least amount of REEs associated with the residual fraction. The fractionation of REEs was compared between sediment samples collected from outside the treatment system and inside the treatment system. The results verified that the processes inside the treatment system modified the initial sediment profile; LREEs were preferentially incorporated into the exchangeable,

reducible, and oxidizable fractions of the sediments collected from inside the treatment basin. This trend is most notable in the reducible phase, in which the LREE content increased from 9% outside to 33% inside the treatment system. The exchangeable, reducible, and oxidizable fractions also exhibited a slightly positive Ce/Ce*, ranging from 1.19 to 1.29, which was accompanied by a slightly negative Ce/Ce* in the residual fraction (0.88).

## São Domingos

Similar to Lousal, the residual fraction accounted for the largest REE pool (Fig. 2b). Again, there was significant variation in the REE-bearing soil fractions outside and inside the mining area. The percentage of REEs associated with the reducible and oxidizable phases was greater in the samples collected outside the mining area than in the samples collected inside the mining area. Soil samples collected from São
<figure><img src="image_3.png" /><figcaption>**Fig. 2** REE fractionation in samples collected (a) inside and outside the Lousal passive treatment system, (b) inside and outside the São Domingos River Valley, and (c) from a tailing pile, outside the mine, and weathered material near the mine at Quinta do Bispo</figcaption></figure>

Domingos river valley exhibited similar REE fractionation across all the BCR steps, with a skewed concave pattern of MREE > HREE > LREE. This finding contrasted to the samples collected outside the mining area, which displayed MREE enrichment in the oxidizable soil fraction, but a LREE > MREE > HREE pattern in the reducible fraction was verified.

For samples collected outside the mining area, Ce/Ce* and Eu/Eu* seemed to be predominantly related to the residual soil fraction (Fig. 1), which showed enrichment of Ce (Ce/Ce*=1.22) and Eu (Eu/Eu*=1.26) relative to their total contents in the soil. Slightly negative Eu/Eu* values were associated with the exchangeable, reducible, and oxidizable BCR fractions. Cerium was depleted in the oxidizable fraction, which had a significantly negative Ce/Ce* of 0.55. The soil sample collected in the mining area

showed positive Ce/Ce*, associated with both reducible and oxidizable solid phases.

## Quinta do Bispo

Samples were collected from three distinct soil environments at the Quinta do Bispo site: a low-grade ore pile, weathered materials collected in an ephemeral stream below Quinta do Bispo, and the surrounding lithology outside the mining area (for comparison). Figure 2c displays the distributions of LREEs, MREEs, and HREEs in the bulk soil collected from these three different sampling points. Although the total concentrations of LREEs, MREEs, and HREEs in the soils collected from Quinta do Bispo were not significantly different (Forsyth et al. 2023), the geochemical associations of these REE groups
varied among the three sampling points. As mentioned before, the surrounding area is a granite with metasomatic deposits of uranium. The sample collected from outside the mining area appears to reflect the surrounding lithology, with the residual fraction accounting for 89–98% of the REEs. Across all Quinta do Bispo sites, the residual fraction contained the largest proportion of REEs. The samples collected from the alluvium and the waste rock pile contained similar proportions of residual REEs. However, the alluvium contained a lower proportion of REEs associated with the reducible fraction when compared to the waste rock pile (9% instead of 15%) and a slightly higher relative proportion of oxidizable REEs (9%, instead of 6%).

Strong positive Eu/Eu\* values were observed in all of the Quinta do Bispo soils throughout all sequential extraction steps, showing that Eu²⁺ is preferentially assimilated into more labile minerals rather than the recalcitrant residual fraction. However, because the residual fraction represents such a large pool of REEs, the soils collected from the area surrounding the ore body have a net negative Eu/Eu\* (Forsyth et al. 2023); samples collected from QB-02 and QB-02b, which resemble the ore body, were enriched in hydrothermally deposited Eu.

REE fractionation influenced by plants

Bulk and rhizosphere soils at Quinta do Bispo were compared. For both the bulk and rhizosphere soils, the residual fraction was the dominant fraction, accounting for 62–98% of individual REEs. Forsyth et al. (2023) reported no significant differences among rhizosphere and bulk soil REE concentrations. However, the BCR extraction results in the current study showed slight differences between the rhizosphere and bulk soil fractions, as displayed in Fig. 3. The rhizosphere samples showed a 0.77–1.94% increase in the amount of REEs associated with the exchangeable fraction; this increase corresponded to a 1.69 µg kg⁻¹ increase in the total soil REE concentration in relation to bulk soil. Since the exchangeable fraction represents such a small proportion of soil REE, this increase is not very significant. An increase of 4.02% and 4.24% in the reducible fraction were observed for MREEs and HREEs, respectively. However, the amount of LREEs associated with the reducible fraction increased by only 0.12%, which corresponded to

0.28 µg kg⁻¹ increase in total rhizosphere soil REE concentrations.

When the REE concentrations in the belowground plant tissues (REE<sub>BG</sub>) were normalized to the BCR extraction data for soils and sediments collected from the rhizosphere (Fig. 4a and d), the patterns were relatively smooth, and negative Eu/Eu\* values were identified in samples from Quinta do Bispo. This finding, paired with the positive Eu/Eu\* in Fig. 1a and d, demonstrates that the mobility of Eu in these soils was high, but that the plant uptake of Eu was relatively low.

Discussion

Influence of mining conditions in REE fractionation

Pang et al. (2002) reported that the average amount of REEs associated with the residual soil fraction was between 45.2% and 94.7%, and many authors

<figure><img src="image_4.png" /><figcaption>**Fig. 3** REE fractionation in rhizosphere soils (Rhiz. soil) and bulk soils collected from Quinta do Bispo</figcaption></figure>
<figure><img src="image_5.png" /><figcaption>**Fig. 4** Relative contents of REEs associated with the (a) exchangeable, (b) reducible, (c) oxidizable, and (d) residual soil fractions in belowground plant tissue. Samples from São</figcaption></figure>

Domingos are indicated by triangles, samples from Quinta do Bispo are indicated by circles, and samples from Lousal are indicated by squares

have reported that in natural soils, the majority of soil REEs are bound to the residual fraction (Cao et al. 2022; Pang et al. 2002; Pédrot et al. 2009; Xinde et al. 2000; Zhang et al. 2023), with the exception of soils associated with certain mining waste streams (Khorasanipour and Rashidi 2020). Presumably, the lower proportions of REEs associated with the exchangeable, reducible, and oxidizable soil fractions in samples collected inside the mining site can be attributed to alteration of exchange surfaces and the dissolution of REE-bearing minerals due to the generation of AMD, leaving only recalcitrant or residual REE fractions. Compared with the samples taken from inside the mining sites, the samples collected from

the passive treatment system at Lousal had the highest proportion of non-recalcitrant REEs. The sediment collected from the Lousal treatment system was a composite of plant growth media, eroded material from the surroundings, and newly formed precipitates, which explains the differences in REE fractionation observed across these systems.

The sediment samples collected in this study exhibited distinct depletion of MREEs in the recalcitrant phase. This could be interpreted as evidence of the greater lability of MREEs over LREEs and HREEs in these systems. Both Grawunder et al. (2014) and Pérez-López et al. (2010) made similar observations but attributed the mobility of REE
to alteration of sulfide minerals, resulting in soluble MREE-sulfate complexes. In this study, both oxidizable and reducible fractions show MREE enrichment and could contribute to the observed MREE enrichment in AMD. This was in agreement with an article published by Khorasanipour and Rashidi (2020) who found the reducible minerals could play a significant role in controlling REE release from mining sites. Inside the treatment system at Lousal, REE fractionation shifted, and the relative content in the reducible fraction grew significantly. This change was accompanied by a larger proportion of LREEs associated with the reducible fraction. The relative proportions of LREEs and MREEs were comparable in the reducible (33% LREEs, 30% MREEs) and residual (61% LREEs, 62% MREEs) fractions. Similarly, a study of another passive treatment system installed by EDM in Jales, Portugal, revealed an association between REEs and Fe-oxide ochre precipitates formed in the limestone treatment basins (Prudêncio et al. 2015). It was concluded that the ochre precipitates scavenged more LREEs, causing an increase in the observed LREE/MREE ratio. These ochre precipitates were vulnerable to changes in hydrology and chemistry, leading to seasonal similarities in LREE/MREE ratios between effluents and precipitates (Prudêncio et al. 2015). Obregón-Castro et al. (2023) investigated similar samples from Lousal and found that most of the materials were Fe-oxyhydroxides with a large proportion of jarosite. Medium REEs with slight enrichment of LREEs over HREEs have been recorded in jarosite minerals (Obregón-Castro et al. 2023; Welch et al. 2009). Therefore, in this study, we attribute the increased percentage of REEs associated with the exchangeable fraction to the formation of jarosite in sample L-02, which is supported by the characteristic increases in the LREE/MREE ratios reported by Obregón-Castro et al. (2023) and Welch et al. (2009).

The Ce/Ce\* and Eu/Eu\* results revealed common themes across the REE patterns for the mining sites. The oxidizable fraction of the mining soils and sediments in this study is dominated by volcanogenic sulfide minerals and lower contents in organic matter. Similar positive Ce/Ce\* values have been observed in sulfides, which may originate in oceanic waters and sediments enriched in Ce (Otake et al. 2021). The geology could therefore account for the positive Ce/Ce\* in the oxidizable fraction. The negative Ce/Ce\* in the oxidizable fraction for the soil collected from

outside São Domingos was also reported for soils and surface waters in this area by Forsyth et al. (2023). The negative Ce/Ce\* in the oxidizable fraction may indicate preferential oxidation of Ce and subsequent Ce depletion in the reduced minerals. The negative Ce/Ce\* could also result from the formation of stable Ce complexes with microbially mediated organic acids, which has been shown to produce a negative Ce/Ce\* for mineral surfaces and increase Ce mobility (Kraemer et al. 2017).

For the soils collected inside the mining-impacted areas, the highly oxidizing nature of AMD waste may promote Ce oxidation, leading to the depletion of Ce in the oxidizable fraction and enrichment of Ce in surface complexes (exchangeable) and in the matrix of secondary minerals such as Fe-oxides (reducible). In this study, some samples had a slightly positive Ce/Ce\* in the reducible fraction. One such sample was collected from the treatment system at Lousal, and there are multiple possible explanations for the observed Ce/Ce\* value. As the passive treatment system is based on a wetland system, soil organic matter (SOM) may be responsible for trapping Ce. However, Pédrot et al. (2015) examined the combined effects of SOM and Fe-oxides on the behavior of REEs and found that Ce/Ce\* was mainly controlled by the Fe-oxide phase. Congruent with Pédrot et al. (2015), secondary mineral precipitates in the Lousal treatment system could scavenge any oxidized Ce, thereby producing a positive Ce/Ce\* in the reducible fraction.

The geochemical conditions in which soil phases were formed and weathered are important background information when making comparisons across studies and sites. As indicated in the materials and methods section, the soils collected from inside and outside the mining area differ in origin and pedogenesis. These differences are highlighted by the BCR extraction results. Although these soils are not directly comparable, the results provide valuable insight into the REE patterns established inside and outside the mining areas.

## Bioavailability fingerprinting

As exemplified by a study of Vermeire et al. (2016), abiotic and biotic weathering of soils, sediments, and host rocks can change the fractionation and the amounts of bioavailable REEs in topsoil horizons. The following section explains the observed
partitioning of REEs in the context of biological weathering processes and defines a bioavailable pool.

The increase in the exchangeable REE pool in rhizosphere soils vs. bulk soils may be caused by carboxylic acids affecting the solubility of REEs in the rhizosphere, as theorized by Wiche and Pourret (2023). This mechanism may also explain some of the patterns observed in the soil-normalized REE<sub>BG</sub> data. Typically, a MREE enrichment is associated with the monodentate complexation, while a HREE preference has been reported for stronger binding sites. Although simple carboxylic acid groups tend to form weaker monodentate complexes in high REE saturated environments, the function of stronger binding sites, associated with multidentate complexation or other anionic functional groups, is more pronounced at lower REE concentrations (Marsac et al. 2010). Europium also has a particular affinity for carboxylic and phosphate functional groups, limiting the solubility of Eu in plant tissue by sorption onto microbial biomass or other surfaces in the rhizosphere (Texier et al. 2000; Tyler 2004). Interestingly, the plants collected from Quinta do Bispo had large negative Eu/Eu* when

REE<sub>BG</sub> was normalized to the REE liberated through sequential extraction. This would mean that in relation to the other REE, the amount of Eu liberated by sequential extraction is lower than what would be expected based on the REE patterns in plants. Since this was isolated to the Quinta do Bispo samples it may indicate an interaction between the specific geological setting of Quinta do Bispo and the physiology of the plants collected there. In particular, the Quinta do Bispo site is dominated by granitic material instead of sulphide minerals and the soil pH was generally higher at the Quinta do Bispo site (ranging from pH 5.4–6.0) than in the other two sites (ranging from 3.3 to 5.8). Both of these factors distinguish Quinta do Bispo and may explain the differences observed in Eu uptake.

In the context of AMD, geochemical observations suggest that (1) a substantial portion of the exchangeable REE fractions are mobilized by changes in surface charge caused by lower pH, (2) reducible REEs can be released through acid-driven dissolution of reducible minerals, and (3) oxidation processes during AMD evolution can lead to oxidizable REE

<figure><img src="image_6.png" /><figcaption>**Fig. 5** (a) Data taken from Forsyth et al. (2023). The below-ground tissue contents are normalized to the total soil/sediment REE contents; (b) belowground tissue contents normalized to the sum of the contents of the three soil fractions identified by</figcaption></figure>

sequential extraction. Samples from São Domingos are indicated by triangles, samples from Quinta do Bispo are indicated by circles, and samples from Lousal are indicated by squares

<figure><img src="image_7.png" /></figure>
solubilization. Based on these assumptions, a labile pool of REEs could be operationally defined. Figure 5a and b compare the REE<sub>BG</sub> concentrations normalized to the total soil REE contents (Fig. 5a) with the REE<sub>BG</sub> concentrations normalized to the operationally defined labile REEs (Fig. 5b). Normalization of the belowground tissue data to the BCR extraction data changed the scale of the observations, with the values for all but one of the plant samples falling within one order of magnitude of 1.00. Moreover, the trend in the BCR extraction-normalized REE<sub>BG</sub> data exhibited little to no slope or concavity (Fig. 5b), in contrast to the total soil REE-normalized REE<sub>BG</sub> data (Fig. 5a), except for samples collected from Quinta do Bispo, which had a negative Eu/Eu* and slight depletion in HREEs. These trends can be taken as qualitative evidence that the BCR extraction results reflect REE uptake by the investigated plants fairly well.

Conclusions

Soil is a complex medium, and it is difficult to predict
the bioavailability of an element based on chemical
extractions alone. Some studies have tried to address
this topic by comparing different chemical extraction
methods and determining which extracts best cor-
relate with plant uptake of REEs. While sequential
selective extractions provide valuable information on
the behavior of elements, particularly their mobility,
they do not accurately reflect their phytoavailability.
This study related REE patterns for soil and sediment
fractions to belowground plant tissue to determine the
potential sources of REE in spontaneous vegetation
around mining sites. These mining sites are charac-
terized by the dissolution of oxidizable and reducible
fractions. Rare earth elements in the soil were mainly
associated with the residual fraction, which was
depleted in MREEs. Accordingly, MREE enrichment
was observed in the “exchangeable and carbonate-
bound”, “reducible mineral”, and “oxidizable mineral
and organic” fractions, which were more vulnerable
to desorption and dissolution promoted by the geo-
chemical conditions accrued from mining activity. As
a result, the fractions from all three sequential extrac-
tion steps were operationally defined as the plant-
available fraction in this system.

The concentrations of REEs in belowground
plant tissue were in good agreement with the sum

of the REEs associated with the three sequential
extraction steps. This was demonstrated by the nor-
malization of the belowground tissue contents to
the operationally defined available REEs, which
showed that the shape and scale of the REE patterns
were smoother than the soil-normalized data and
distributed around 1.00. However, the Eu data devi-
ated from this trend, as there was a distinct nega-
tive Eu/Eu* for the Quinta do Bispo samples. There
was a negative Eu/Eu* in the tissue coupled with a
positive Eu/Eu* for the defined labile pools, indicat-
ing the exclusion of Eu from plant tissue despite the
abundance of Eu in less recalcitrant soil fractions.

Although the insight provided here is valuable for
determining the controlling factors of REE uptake in
plant roots in mining environments, further studies
should consider a variety of geological contexts and
pH conditions. Additionally, further studies should
be planned to determine the biological factors con-
trolling or limiting plant uptake of REEs. To focus
on phytoextraction, a more thorough assessment of
the element's physical and chemical speciation is
required. Such studies could include the investigation
of plant nutrient acquisition and how it relates to the
plant availability of REEs.

**Acknowledgements** The authors are grateful for support from the GeOHeLiS analytical platform of Rennes. This publication is also supported by the European Union through the European Regional Development Fund (FEDER), the French Ministry of Higher Education and Research, and the French Region of Brittany and Rennes Métropole.

**Author contributions** Kaisa Forsyth: Writing – Original Draft, Investigation, Data Curation; Aline Dia: Conceptualization, Supervision, Writing – Review & Editing, Funding acquisition; Rosa Marques: Conceptualization, Writing – Review & Editing, Resources; Maria Isabel Prudêncio: Conceptualization, Writing – Review & Editing; Cynthia Obregón-Castro: Writing – Review & Editing, Data Curation; Catarina Diamantino: Writing – Review & Editing, Resources; Edgar Carvalho: Writing – Review & Editing, Resources; Maxime Pattier: Formal analysis; Mélanie Davranche: Conceptualization, Funding acquisition; Mathieu Pédrot: Conceptualization, Supervision, Writing – Review & Editing.

**Funding** This project received funding from the European Union's Horizon 2020 Research and Innovation Program under the Marie Skłodowska-Curie Grant Agreement No. 857989 (PANORAMA project).

**Data availability** The datasets generated and/or analyzed during the current study are available from the corresponding author upon request.
Declarations

**Competing interests** The authors have no relevant financial or nonfinancial interests to disclose.

**Open Access** This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.

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