Assessment of metal(loid)s phytoavailability in intensive agricultural soils by the application of single extractions to rhizosphere soil
Graphical abstract
Introduction
Metals and metalloids, from now on referred to as metal(loid)s, are ubiquitous components of the lithosphere. Metal(loid)s are distributed in both the solid and aqueous phases of the soil and may be involved in a panoply of interactions ranging from weak electrostatic sorption up to irreversible binding (Fedotov et al., 2012).
According to ISO (2008a), environmental bioavailability is defined as the fraction of an element that can be either available or potentially available to living organisms. This definition includes both the actual available fraction (i.e., the sum of dissolved free ions/molecules plus dissolved complexes) and the potentially available fraction (i.e., ions/molecules that can be released from stable organo-mineral soil complexes). When this definition is specifically applied to plants, it is commonly referred as phytoavailability (Meers et al., 2007).
The uptake of an element by plant can lead to its depletion at the rhizosphere zone, which usually induces a response from the surrounding soil. When the element uptake is slow, depletion at the root surface is insignificant and the concentration can be expected to be proportional to the dissolved free ions in solution. In this case, the Free Ion Activity Model (FIAM) can be applied (Lofts et al., 2013). However, when the rate of removal of the element by the plant at the soil–root interface exceeds its diffusional supply, its concentration in the rhizosphere can become depleted. This can lead to resupply of elements from dissociation of complexes in the solution and/or release of elements from the soil particles in contact with the confined zone where depletion in solution occurs. In this case, the dynamic process of (re)supply of elements to a plant is likely to be determined by the concentration of total labile element in solution, its diffusional supply, the concentration of labile element available from solid phase and the rate at which it is released from solid phase to solution (Lehto et al., 2006).
The use of a single well-defined extraction procedure is one of the most common approaches used to assess the phytoavailable fraction of elements in soil. In the last years, single extraction methods have being widely applied to study particular solid-phase associations of metal(loid)s in soils (Feng et al., 2005, Gupta and Sinha, 2007, Hass and Fine, 2010, Meers et al., 2007, Menzies et al., 2007, Minca and Basta, 2013, Pueyo et al., 2004). Several extractants are used and can be classified according to the intrinsic mechanism involved in the release of elements from soil. For instance, salt solutions such as NH4NO3 and CaCl2 can only extract elements from the water-soluble and exchangeable phases. However, the DTPA extractant is also able to attack organically-bound elements (Rao et al., 2008). The data generated in these studies are particularly useful for understanding the physicochemical processes that take place in the soil since they allow the elucidation of the mechanisms involved in metal(loid)s binding, transformation and/or release from soil. However, until now, no extraction procedure proved to be suitable to accurately predict the phytoavailability of metal(loid)s (Fedotov et al., 2012). One of the major challenges in field studies has been how to correlate the results from single extraction assays with metal(loid)s uptake and accumulation by plants.
As mentioned before, the actual and potential phytoavailable fractions of metal(loid)s can be considered as the fraction of the total amount of an element present in a specific environmental compartment that, within a defined time period, is either available or can be made available for uptake by plants (Rao et al., 2008). Therefore, the plant metal(loid)s content should closely reflect the metal(loid)s phytoavailability in the rhizosphere zone. Several factors are known to control the phytoavailability of metal(loid)s in the soil, and ultimately, their soil–plant–human transfer and accumulation (Pauget et al., 2012). The soil properties pH, cation exchange capacity (CEC), organic matter (OM) content, electrical conductivity (EC), particle size distribution and oxides content are generally regarded as the main parameters that control the distribution of metal(loid)s between the phytoavailable and non-phytoavailable fractions (Frierdich and Catalano, 2012, Hernandez-Soriano and Jimenez-Lopez, 2012, Luo et al., 2011, Pinto et al., 2014). Moreover, the phytoavailability of soil metal(loid)s is also the result of root–rhizosphere interactions. Reactions that take place at this interface strongly determine the metal(loid)s speciation and uptake by plants, ultimately affecting the accumulation and overall content of these elements in plants (Cheng, 2009, Rajkumar et al., 2012).
Modern agricultural practices largely rely on the application of high amounts of chemical fertilizers, which can be contaminated with several toxic metal(loid)s (Jiao et al., 2012). In this context, studies on the potential transfer of toxic metal(loid)s to the food chain are of major importance. Lettuce (Lactuca sativa) is one of the most consumed vegetables worldwide, representing about 6.5% of the total dietary intake of vegetables by humans (WHO, 2003). Besides, lettuce is recommended by the US Environmental Protection Agency (EPA) as a suitable test plant to determine uptake and translocation of toxic substances (USEPA, 2012).
Based on the above background, and in order to contribute for a better understanding of the soil–plant relationship regarding metal(loid)s, the aim of this study was to assess the influence of soil properties on the availability of metal(loid)s to lettuce during its normal growth period and the differences in phytoavailability results obtained by using different extraction methods. To accomplish this, a four-step approach was used: (1) the physicochemical properties of three different soils and the soil metal(loid)s extractable content (as assessed by four different extraction methods) were determined; (2) the metal(loid)s content in the plant shoot at five time points of lettuce growth was measured; (3) the correlation between the metal(loid)s extractable content in the soil and the plant shoot content was performed; and (4) multiple regression analysis was used to identify the most suitable extraction method in order to estimate the metal(loid)s phytoavailability to lettuce and to predict the metal(loid)s content in lettuce shoot.
Section snippets
Plant cultivation, sampling and sample preparation
Lettuce (Lactuca sativa L.) plants (n=100) were cultivated in three greenhouse experimental fields: A1 (41° 26.991 N, 8° 46.335 W), A2 (41° 25.249 N, 8° 44.936 W) and A3 (41° 27.435 N, 8° 45.377 W). These fields were chosen because intensive agriculture practices, relying on the use of high amount of chemical fertilizers, have been adopted during the last decade in the growing of high-yield crops. Plants were submitted to similar sunlight exposure (a total of 334 h; photoperiod on average 11.16
Soil properties and extraction method efficiency
The main physicochemical properties (pH, CEC, OM, EC, salinity, oxides and particle size distribution) of bulk soils collected from the three experimental fields (A1, A2 and A3) are shown in Table 1. No significant differences were observed for each physicochemical property along the 5 time points (data not shown). Thus, results in Table 1 are the mean and standard deviation of triplicate measurements performed at each of the 5 time points (T1, T2, T3, T4 and T5). Significant differences were
Conclusion
The analysis of rhizosphere soil proved to be a reliable approach to estimate metal(loid)s phytoavailability. Several significant correlations between lettuce shoots and extractable metal(loid)s content in soil were obtained for Cr, V, Ni, As, Pb, Co, Cd and Sb. From the four extraction methods used, the NH4NO3 method showed strong positive correlations for almost all the metal(loid)s studied and is the most suitable method to estimate metal(loid)s phytoavailability. Soil properties (pH, OM,
Acknowledgements
Edgar Pinto thanks to Fundação para a Ciência e a Tecnologia (Portuguese Foundation for Science and Technology) for his Ph.D. Grant (SFRH/BD/67042/2009). This work received financial support from the European Union (FEDER funds through COMPETE) and National Funds (Fundação para a Ciência e a Tecnologia) through project Pest-C/EQB/LA0006/2013. The work also received financial support from the European Union (FEDER funds) under the framework of QREN through Project NORTE-07-0124-FEDER-000069. To
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