Substratum influences uptake of radium-226 by plants
Graphical abstract
Introduction
The Critical Zone (CZ), which is the domain between the top of the aquifer and the top of the canopy, is the part of the Earth's surface sustaining life. One fundamental issue currently is to assess the fluxes of energy and matter between the various compartments of the CZ and their vulnerability (Brantley et al., 2007; Lin, 2010). Soil, a key compartment at the boundary between the lithosphere, biosphere, and atmosphere, sensitive to natural and unnatural forcing and essential for mankind, often appears as the most polluted part of the CZ (Abrahams, 2002; Banwart, 2011). Various pollutants, harmful to the biosphere, have been detected in soil, including heavy metals and radionuclides (e.g., He and Walling, 1996; Manta et al., 2002; Douay et al., 2009; Li et al., 2014; Girault et al., 2016). Vegetation growing on top of this soil is directly capable of capturing naturally occurring elements as well as pollutants in its roots, tissues, flowers, and fruits (e.g., Sheppard and Evenden, 1988b; Carini, 1999; Ehlken and Kirchner, 2002). This uptake of tracer elements can also be a way to constrain the biogeochemical cycle of elements from the pedosphere to the biosphere in the CZ.
Ubiquitous in the environment, the alkaline earth element radium is present in all CZ compartments including water, rock, soil, and vegetation. The radium-226 isotope belongs to the uranium-238 decay chain and is an alpha emitter with a half-life of 1600 ± 7 years (Duchemin et al., 1994). Several studies have focused on the uptake of 226Ra by plants, quantifying a transfer factor (or concentration ratio) of 226Ra from the soil to the plant tissues (Simon and Ibrahim, 1990; Sheppard et al., 2006; Vandenhove et al., 2009; Uchida et al., 2009). Predominantly, because of the need to assess the radium content of agricultural products and the risk to the population, researches on the 226Ra uptake by plants have been carried out in 226Ra-contaminated areas (e.g., Simon and Ibrahim, 1990 and references herein), such as former or operating uranium mining and milling sites (Marple, 1980; Vasconcellos et al., 1987; Bettencourt et al., 1988; Ibrahim and Whicker, 1992; Markose et al., 1993; Madruga et al., 2001; Blanco Rodríguez et al., 2002, Blanco Rodríguez et al., 2010; Vera Tomé et al., 2002, Vera Tomé et al., 2003; Chen et al., 2005; Ryan et al., 2005; Soudek et al., 2007a, Soudek et al., 2007b, Soudek et al., 2010; Carvalho et al., 2009; Černe et al., 2011; Medley et al., 2013; Hu et al., 2014; Medley and Bollhöfer, 2016; Yan and Luo, 2016), phosphate fertilizer processing complexes (Paul and Pillai, 1986; Martínez-Aguirre and Periáñez, 1998), radium salt factories (Bettencourt et al., 1988), depleted uranium ammunition sites (Popovic et al., 2008), and other industrial units (Paul and Pillai, 1986). These studies have been complemented by experiments on artificially 226Ra-enhanced soils at the laboratory scale in pots or at larger scale in lysimeter and field experiments (Gerzabek et al., 1998; Bunzl and Trautmannsheimer, 1999; Vandenhove et al., 2005; Vandenhove and Van Hees, 2007; Nezami et al., 2016), providing valuable insights for phytoremediation of contaminated areas (Thiry and Van Hees, 2008; Vera Tomé et al., 2008, Vera Tomé et al., 2009; Abreu et al., 2014). By contrast, fewer studies have focused on 226Ra uptake by plants in non-contaminated areas or control sites (Sam and Eriksson, 1995; Ham et al., 2001; Karunakara et al., 2003; Pulhani et al., 2005; Popovic et al., 2008; Uchida and Tagami, 2007; da Conceição et al., 2009; Lauria et al., 2009; Dragović et al., 2010; James et al., 2011; Medley et al., 2013; Asaduzzaman et al., 2014; Al-Hamarneh et al., 2016; Mrdakovic Popic et al., 2020). Despite these efforts, the uptake of 226Ra by plants thus remains insufficiently well understood.
The first mechanism of uptake of elements by plants is passive and results from element concentration in groundwater and evapotranspiration. In this mechanism, 226Ra accumulates in leaves and can also be excreted (e.g., Weis and Weis, 2004). In addition, uptake of elements by a living plant is part of the metabolic cycle. In vascular plants, 226Ra uptake takes place through the various steps of the biological processes (e.g., Simon and Ibrahim, 1990): mobility of Ra2+ ions including release and diffusion from the solid phase to the soil solution, exchange of available Ra2+ ions by sorption/desorption onto the surfaces of roots, transport of Ra2+ ions across membranes in the roots, and diffusion and translocation of 226Ra into plant tissues. Among other factors, it has been recognized that radium uptake depends on the presence of other alkaline earth elements of smaller ionic radius such as barium, strontium, calcium, and magnesium. This suggests that the radium uptake by plants decreases as the concentration of other alkaline earth elements in soil increases, and that incorporation by roots can saturate (Nathwani and Phillips, 1979; Marple, 1980; Simon and Ibrahim, 1987). Generally, a bottom-to-top decreasing gradient (i.e., acropetal) of radium concentration has been observed in plant tissues, from roots to stems and from stems to shoots (e.g., Simon and Ibrahim, 1990). As a testing hypothesis, we could consider that the variability in 226Ra uptake by plants may be due to different types of soil (substrate) and substratum, in particular in non-contaminated areas. However, surprisingly, only small differences or no change at all have been evidenced (e.g., Simon and Ibrahim, 1987, Simon and Ibrahim, 1990; Vera Tomé et al., 2003; Pulhani et al., 2005).
Several methods, such as gamma-ray spectrometry, alpha-particle spectrometry, liquid scintillation counting, and mass spectrometry, are commonly used to measure high 226Ra levels of numerous materials. However, for low 226Ra levels in soil and for plant samples of relatively small mass, such methods generally give large analytical uncertainty and data have remained limited. Thus, to study 226Ra uptake by plants in non-contaminated areas, an alternative technique is desired, able to reach low 226Ra levels for a large amount of samples, in a cost-effective manner. A candidate high-sensitivity technique with well-constrained leakage effects and relatively small uncertainty for low 226Ra levels is available; it is based on radon-222 emanation, as already suggested thirty years ago (Simon and Ibrahim, 1990). Radon-222 is a radioactive gas (half-life 3.8 days) produced by the alpha decay of 226Ra. The probability that a 226Ra atom decays into a 222Rn atom able to escape from a medium is the emanation coefficient E (Tanner, 1964; Nazaroff, 1992). We define the 222Rn emanating power of a given material by the effective 226Ra concentration (ECRa), i.e. the product of E by the bulk 226Ra concentration (CRa), expressed in Bq kg−1 (Stoulos et al., 2004). Based on the accumulation method, ECRa has been measured in various materials including soils (e.g., Markkanen and Arvela, 1992; Girault et al., 2011; Perrier et al., 2016b), rocks and building materials (e.g., Przylibski, 2000; Righi and Bruzzi, 2006; Hassan et al., 2011; Girault et al., 2012), and more recently plants (Perrier et al., 2018). Lately, this method has been updated with a significantly higher sensitivity, allowing ECRa measurement of material with small mass (<5 g) and low 226Ra levels (<10−14 g g−1) (Girault et al., 2017a; Girault and Perrier, 2019). Measuring ECRa of plants using this high-sensitivity method is particularly suited in areas characterized by low 226Ra levels.
In this paper, to test the hypothesis of a possible effect of the substratum on the 226Ra uptake by plants in non-contaminated areas, we present results of effective 226Ra concentration (ECRa) in a total of 108 plants collected at several non-contaminated sites in France that belong to two geological subsets: granitic and metamorphic context, and calcareous and sedimentary context. Using measured ECRa of plants and of the nearby soil as well as representative 222Rn emanation coefficients for plants and soils, we infer the 226Ra soil-to-plant transfer ratio (RSP). We show that, by contrast with the results available previously in contaminated areas, RSP values strongly depend on the substratum. We then discuss our results in terms of plant type, species, and compartment, and of the 226Ra concentration of soil–plant pairs. Consequences for the assessment of element fluxes in the CZ are discussed in the conclusion.
Section snippets
Plant and soil samples
A total of 108 plant samples and their associated nearby local soil samples were collected at different sites in France (Fig. 1). The plants mainly include deciduous trees (Quercus robur, Fagus sylvatica, Castanea sativa, Tilia ×europaea, Prunus cerasus, Ficus carica, Fraxinus excelsior, Corylus avellana, Aesculus hippocastanum), evergreen trees (Quercus ilex, Pinus pinaster, Abies alba), shrubs (Buxus sempervirens, Phillyrea latifolia, Spartium junceum, Cytisus oromediterraneus), and ferns (
Effective 226Ra concentrations in plants and their nearby local soils
Effective 226Ra concentration (ECRa) values of plant samples (n = 108) range over about five orders of magnitude (Fig. 3c), from 0.020 ± 0.001 to 113 ± 7 Bq kg−1, and with a mean of 1.66 ± 0.03 Bq kg−1 (Table 1). The two largest values, 113 ± 7 and 44 ± 2 Bq kg−1, are measured for a moss and roots of Fagus sylvatica, respectively, both from the granitic area near Ambazac. The two smallest values, 0.020 ± 0.001 and 0.09 ± 0.07 Bq kg−1, are measured for chestnuts of Aesculus hippocastanum and
Updated status on the understanding of radium uptake by plants
Our soil-to-plant transfer ratio (RSP) data, although they are inferred from the measurement of effective 226Ra concentration (ECRa) and emanation coefficient (E) of both soil and plant samples, give compatible values with the transfer factors deduced from the direct measurement of bulk 226Ra concentrations as reported in the literature. Indeed, our mean RSP value, 0.0188 ± 0.0004, thus about 2%, is consistent with mean 226Ra transfer factors reported in the literature for all plants, ranging
Conclusion
We have shown that measuring effective 226Ra concentration (ECRa) can be useful to quantify the 226Ra uptake by the biosphere from soil or water in various environments. We have found that, in non-contaminated areas, RSP values are heterogeneous but reveal an important influence by the substratum, with about an order of magnitude larger RSP values in granitic and metamorphic context than in calcareous and sedimentary context. This difference may likely be due to the competition between calcium
CRediT authorship contribution statement
Frédéric Girault: Conceptualization, Methodology, Formal analysis, Investigation, Resources, Data curation, Writing - original draft, Writing - review & editing, Visualization. Frédéric Perrier: Conceptualization, Methodology, Investigation, Resources, Writing - original draft, Writing - review & editing. Jean-Marc Ourcival: Investigation, Resources. Roxane Ferry: Investigation. Yves Gaudemer: Visualization. François Bourges: Investigation, Resources. Jean-François Didon-Lescot: Investigation,
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We thank Jean Bouillaguet for his help in plant and soil sampling around Saint-Yrieix-la-Perche, Haute-Vienne department, Hélène Bouquerel and Aude Isambert for their help in plant and soil sampling around the Pech Merle cave, Lot department, and Benoit Heumez, Eric Parmentier, and Xavier Lalanne for their help in the sampling of soils in the compound of the National Magnetic Observatory at Chambon-La-Forêt, Loiret department. Dominique Genty and Bruno Lartiges are thanked for their
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