Environ Monit Assess (2014) 186:4591–4603 DOI 10.1007/s10661-014-3722-9
Assessment of the bioavailability of cadmium in Jamaican soils Adrian Spence & Richard E. Hanson & Charles N. Grant & Leslie Hoo Fung & Robin Rattray
Received: 30 September 2013 / Accepted: 6 March 2014 / Published online: 30 March 2014 # Springer International Publishing Switzerland 2014
Abstract Extraordinary geogenic concentrations of cadmium (Cd) have been reported for some Jamaican soils. However, the bioavailability of the metal in these soils remains unknown. Here, the bioavailability of Cd in selected Jamaican soils was investigated through the determination of total and sequentially extractable concentrations in paired soil–plant (yam; Dioscorea sp.) samples (n=24), using neutron activation analysis and atomic absorption spectroscopy as primary analytical techniques. Our results indicate that total soil Cd varied widely (2.2–148.7 mg kg−1), and on average, total extractable Cd accounted for ~55 % of the total soil Cd. The exchangeable and oxidizable species averaged 1.5 and 6.4 % of the total Cd, respectively, and, based on Spearman analysis, are the best predictors of yam Cd. There is also good evidence to suggest that variation in the bioavailability of the metal is in part controlled by the geochemical characteristics of the soils analyzed and is best explained by pH, cation exchange capacity (CEC) and organic matter content (% LOI).
Keywords Bioavailability . Cadmium . Correlation . Geochemical characteristics . Jamaican soils . Yam
A. Spence (*) : R. E. Hanson : C. N. Grant : L. Hoo Fung International Centre for Environmental and Nuclear Sciences, University of the West Indies, Mona, Kingston 7, Jamaica e-mail: [email protected] R. Rattray Department of Chemistry, University of the West Indies, Mona, Kingston 7, Jamaica
Introduction The accumulation of high levels of trace metals in the surface of agricultural soils is an issue of paramount importance due to the potential adverse influence on soil health, crop quality and the environment (McLaughlin et al. 2000; Gray et al. 2003). Recent island wide surveys of Jamaican soils revealed that there are several locations where geogenic concentrations of cadmium (Cd), a persistent pollutant, are of increasing concern to environmental and ecosystem health (Lalor 2008). For example, in Manchester Parish, soils overlying limestone have been determined to contain some of the highest Cd concentrations with a mean of 54 mg kg−1 and a maximum of over 900 mg kg−1 from a residential district (Lalor 2008). These concentrations are unusual for unpolluted soils, and the highest values are comparable to those of Cd levels of industrially polluted soils found close to some smelters (Waldron 1980). However, when assessing the bioavailability and risks associated with metal-contaminated soils, it is now generally accepted that chemical speciation—the relative existence of a metal in different chemical forms under different physico-chemical conditions (Shadid et al. 2012), rather than total metal content—is a more accurate descriptor (Xie et al. 2012). In soils, Cd exists in several chemical forms with varying degrees of solubility and bioavailability and may be defined as follows: water soluble (in soil solution), readily exchangeable, acid soluble (bound to carbonates), oxidizable [bound to organic matter (OM)], reducible (bound to hydrous oxides of Fe and Mn) and residual (occluded by mineral structures) (Kabata-Pendias 2011).
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Except for residual Cd, all other fractions are usually considered bioavailable (Pueyo et al. 2004). In general, the bioavailability of Cd in soils is influenced by adsorption–desorption phenomena (Violante et al. 2010; Krishnamurti et al. 2004), which are inextricably linked to a complex variety of biotic and abiotic factors. These include pH; OM content; cation exchange capacity (CEC); quantity and type of clay minerals; hydrous metal oxides of Fe, Al and Mn; and redox potential (Aydinalp and Marinova 2003). Taken in total, it is essential to delineate the chemical forms of Cd in soils if we are to better understand and predict its mobility, bioavailability, and toxicity while informing effective soil management practices to attenuate the impact of Cd toxicity in the environment. In the recent years, analytical techniques using stable and radioactive isotope dilution (ID) have been applied to determine the ‘labile’ (available) pool of Cd (and other metals) in soils (e.g. Stacey et al. 2001; Sterckeman et al. 2009). In particular, ID using stable isotopes is considered by some geochemists to be the ‘gold standard’ of defining available metal pools in soils. However, despite the distinction of providing a relatively unambiguous assessment of the available metal pool, ID is time-consuming, requires specific and expensive instruments, and, in the case of radioactive ID, requires scrupulous and expensive radiation protection protocols (Sterckeman et al. 2009). Alternatively, the chemical partitioning of Cd (and other metals) in soils has been studied using single reagent and sequential extraction approaches (Nolan et al. 2003). Sequential extraction procedures use a series of suitable reagents applied in a given order to a soil sample to target the different operationally defined species of the metal and release them into solution where they can be measured quantitatively (Okoro et al. 2012). Extractions normally follow the sequence of most mobile to least mobile species by progressively increasing the leachant strength of the extractant (Okoro et al. 2012). Numerous adaptations of the sequential extraction protocol, first worked on by Gupta and Chen (1975) and Tessier et al. (1979) and later modified by the Community Bureau of Reference (BCR), have been used to investigate the operationally defined extractable metal fractions of soils (e.g. Ure et al. 1993). However, only a limited number of studies have focused on paired soil–plant scenarios to provide an empirical understanding of metal bioavailability. Moreover, despite
Environ Monit Assess (2014) 186:4591–4603
significant improvements in our knowledge on the global and regional distributions of trace metal pools, speciation of Cd (and other metals) remains a critical area of research, needed to facilitate further advances in our understanding of its bioavailability. For instance, although recent geochemical surveys have provided a comprehensive overview of the spatial distribution of Cd (total and dissolved content) in Jamaican soils, research defining its speciation has been virtually ignored, leaving unknown information regarding its bioavailability. Additionally, there is a need for continual monitoring of these high natural values of Cd in Jamaican soils in order to (i) understand and quantify long-term changes in Cd bioavailability, (ii) the possible effects of remediation processes on Cd bioavailability in these soils and (iii) the possible effects of changes in crop variety or crop type on Cd uptake. Here, we employ a paired soil–plant study to better understand the biogeochemistry of Cd in Jamaican soils. The specific objectives of this study were (i) to quantify the chemical forms of Cd in bulk soils collected across Central Jamaica, (ii) to determine the relationship between the various forms of soil Cd and the Cd content of the edible portions of yams (Dioscorea sp.) grown in the same soils and (iii) to determine the influence of simple geochemical properties on the bioavailability of Cd. In Jamaica, yams are an important staple with an estimated local annual consumption of 120 million kg. Additionally, yams are fundamental to the welfare of many small farmers (not just a few large producers) and are an important foreign exchange earner for the local economy with an annual export value of approximately US$17 million (JAMPRO 2011).
Methods Sample collection Twenty-four bulk soil samples (0–30 cm) representing different soil types (typically terra rossa and bauxitic soils), Cd origins (data not shown) and contents were collected from multiple field sites across an area (~314 km2) encompassing the northern and southwestern sections of Manchester and St. Ann parishes (respectively) in Jamaica (Fig. 1). Each field site sampled had been under production of various species of the herbaceous root tubers, Dioscorea sp. Traditionally,
Environ Monit Assess (2014) 186:4591–4603
4593
Fig. 1 Distribution of paired soil–plant sample collection sites (soil sample numbers in Table 1) in North Manchester and south-western St. Ann parishes in Central Jamaica
yam tubers are cultivated in mounds prepared from soils that have been tilled to depths of up to 30 cm. Therefore, by collecting soil samples at up to 30 cm, it is likely to capture a more representative geochemical profile of the immediate growing environment of the root tubers. The sampling regime (at each sampling point) involved the use of an Edelman hand auger to collect five soil cores at the four corners and centre of a square with dimensions of 5 m×5 m. The soil cores were combined in a doublestrength polyethylene bag to yield a bulk sample of ~0.5 kg, and the bag was sealed at the collection site. Samples were transported to the laboratory under ambient conditions and processed within 24 h of collection. Previously, at each sampling site (5 m×5 m), the samples were collected but, critically, without mixing of the five sub-samples. The rationale was to assess the geochemical variability within each sampling site so as to avoid the mixing of geochemical dissimilar sub-samples. Composite samples of mature yam tubers were also collected within each soil sampling location (5 m×5 m) by carefully harvesting them from soil mounds. The
tubers were brushed to remove adhering soils, placed in labelled polyethylene bags and transported to the laboratory. Preparation and analysis of soil samples General geochemical characteristics After the removal of debris including plant material and stones, the samples were air-dried, disaggregated, and filtered through a nylon sieve with a 2-mm aperture. A small sub-sample of the
Assessment of the bioavailability of cadmium in Jamaican soils Adrian Spence & Richard E. Hanson & Charles N. Grant & Leslie Hoo Fung & Robin Rattray
Received: 30 September 2013 / Accepted: 6 March 2014 / Published online: 30 March 2014 # Springer International Publishing Switzerland 2014
Abstract Extraordinary geogenic concentrations of cadmium (Cd) have been reported for some Jamaican soils. However, the bioavailability of the metal in these soils remains unknown. Here, the bioavailability of Cd in selected Jamaican soils was investigated through the determination of total and sequentially extractable concentrations in paired soil–plant (yam; Dioscorea sp.) samples (n=24), using neutron activation analysis and atomic absorption spectroscopy as primary analytical techniques. Our results indicate that total soil Cd varied widely (2.2–148.7 mg kg−1), and on average, total extractable Cd accounted for ~55 % of the total soil Cd. The exchangeable and oxidizable species averaged 1.5 and 6.4 % of the total Cd, respectively, and, based on Spearman analysis, are the best predictors of yam Cd. There is also good evidence to suggest that variation in the bioavailability of the metal is in part controlled by the geochemical characteristics of the soils analyzed and is best explained by pH, cation exchange capacity (CEC) and organic matter content (% LOI).
Keywords Bioavailability . Cadmium . Correlation . Geochemical characteristics . Jamaican soils . Yam
A. Spence (*) : R. E. Hanson : C. N. Grant : L. Hoo Fung International Centre for Environmental and Nuclear Sciences, University of the West Indies, Mona, Kingston 7, Jamaica e-mail: [email protected] R. Rattray Department of Chemistry, University of the West Indies, Mona, Kingston 7, Jamaica
Introduction The accumulation of high levels of trace metals in the surface of agricultural soils is an issue of paramount importance due to the potential adverse influence on soil health, crop quality and the environment (McLaughlin et al. 2000; Gray et al. 2003). Recent island wide surveys of Jamaican soils revealed that there are several locations where geogenic concentrations of cadmium (Cd), a persistent pollutant, are of increasing concern to environmental and ecosystem health (Lalor 2008). For example, in Manchester Parish, soils overlying limestone have been determined to contain some of the highest Cd concentrations with a mean of 54 mg kg−1 and a maximum of over 900 mg kg−1 from a residential district (Lalor 2008). These concentrations are unusual for unpolluted soils, and the highest values are comparable to those of Cd levels of industrially polluted soils found close to some smelters (Waldron 1980). However, when assessing the bioavailability and risks associated with metal-contaminated soils, it is now generally accepted that chemical speciation—the relative existence of a metal in different chemical forms under different physico-chemical conditions (Shadid et al. 2012), rather than total metal content—is a more accurate descriptor (Xie et al. 2012). In soils, Cd exists in several chemical forms with varying degrees of solubility and bioavailability and may be defined as follows: water soluble (in soil solution), readily exchangeable, acid soluble (bound to carbonates), oxidizable [bound to organic matter (OM)], reducible (bound to hydrous oxides of Fe and Mn) and residual (occluded by mineral structures) (Kabata-Pendias 2011).
4592
Except for residual Cd, all other fractions are usually considered bioavailable (Pueyo et al. 2004). In general, the bioavailability of Cd in soils is influenced by adsorption–desorption phenomena (Violante et al. 2010; Krishnamurti et al. 2004), which are inextricably linked to a complex variety of biotic and abiotic factors. These include pH; OM content; cation exchange capacity (CEC); quantity and type of clay minerals; hydrous metal oxides of Fe, Al and Mn; and redox potential (Aydinalp and Marinova 2003). Taken in total, it is essential to delineate the chemical forms of Cd in soils if we are to better understand and predict its mobility, bioavailability, and toxicity while informing effective soil management practices to attenuate the impact of Cd toxicity in the environment. In the recent years, analytical techniques using stable and radioactive isotope dilution (ID) have been applied to determine the ‘labile’ (available) pool of Cd (and other metals) in soils (e.g. Stacey et al. 2001; Sterckeman et al. 2009). In particular, ID using stable isotopes is considered by some geochemists to be the ‘gold standard’ of defining available metal pools in soils. However, despite the distinction of providing a relatively unambiguous assessment of the available metal pool, ID is time-consuming, requires specific and expensive instruments, and, in the case of radioactive ID, requires scrupulous and expensive radiation protection protocols (Sterckeman et al. 2009). Alternatively, the chemical partitioning of Cd (and other metals) in soils has been studied using single reagent and sequential extraction approaches (Nolan et al. 2003). Sequential extraction procedures use a series of suitable reagents applied in a given order to a soil sample to target the different operationally defined species of the metal and release them into solution where they can be measured quantitatively (Okoro et al. 2012). Extractions normally follow the sequence of most mobile to least mobile species by progressively increasing the leachant strength of the extractant (Okoro et al. 2012). Numerous adaptations of the sequential extraction protocol, first worked on by Gupta and Chen (1975) and Tessier et al. (1979) and later modified by the Community Bureau of Reference (BCR), have been used to investigate the operationally defined extractable metal fractions of soils (e.g. Ure et al. 1993). However, only a limited number of studies have focused on paired soil–plant scenarios to provide an empirical understanding of metal bioavailability. Moreover, despite
Environ Monit Assess (2014) 186:4591–4603
significant improvements in our knowledge on the global and regional distributions of trace metal pools, speciation of Cd (and other metals) remains a critical area of research, needed to facilitate further advances in our understanding of its bioavailability. For instance, although recent geochemical surveys have provided a comprehensive overview of the spatial distribution of Cd (total and dissolved content) in Jamaican soils, research defining its speciation has been virtually ignored, leaving unknown information regarding its bioavailability. Additionally, there is a need for continual monitoring of these high natural values of Cd in Jamaican soils in order to (i) understand and quantify long-term changes in Cd bioavailability, (ii) the possible effects of remediation processes on Cd bioavailability in these soils and (iii) the possible effects of changes in crop variety or crop type on Cd uptake. Here, we employ a paired soil–plant study to better understand the biogeochemistry of Cd in Jamaican soils. The specific objectives of this study were (i) to quantify the chemical forms of Cd in bulk soils collected across Central Jamaica, (ii) to determine the relationship between the various forms of soil Cd and the Cd content of the edible portions of yams (Dioscorea sp.) grown in the same soils and (iii) to determine the influence of simple geochemical properties on the bioavailability of Cd. In Jamaica, yams are an important staple with an estimated local annual consumption of 120 million kg. Additionally, yams are fundamental to the welfare of many small farmers (not just a few large producers) and are an important foreign exchange earner for the local economy with an annual export value of approximately US$17 million (JAMPRO 2011).
Methods Sample collection Twenty-four bulk soil samples (0–30 cm) representing different soil types (typically terra rossa and bauxitic soils), Cd origins (data not shown) and contents were collected from multiple field sites across an area (~314 km2) encompassing the northern and southwestern sections of Manchester and St. Ann parishes (respectively) in Jamaica (Fig. 1). Each field site sampled had been under production of various species of the herbaceous root tubers, Dioscorea sp. Traditionally,
Environ Monit Assess (2014) 186:4591–4603
4593
Fig. 1 Distribution of paired soil–plant sample collection sites (soil sample numbers in Table 1) in North Manchester and south-western St. Ann parishes in Central Jamaica
yam tubers are cultivated in mounds prepared from soils that have been tilled to depths of up to 30 cm. Therefore, by collecting soil samples at up to 30 cm, it is likely to capture a more representative geochemical profile of the immediate growing environment of the root tubers. The sampling regime (at each sampling point) involved the use of an Edelman hand auger to collect five soil cores at the four corners and centre of a square with dimensions of 5 m×5 m. The soil cores were combined in a doublestrength polyethylene bag to yield a bulk sample of ~0.5 kg, and the bag was sealed at the collection site. Samples were transported to the laboratory under ambient conditions and processed within 24 h of collection. Previously, at each sampling site (5 m×5 m), the samples were collected but, critically, without mixing of the five sub-samples. The rationale was to assess the geochemical variability within each sampling site so as to avoid the mixing of geochemical dissimilar sub-samples. Composite samples of mature yam tubers were also collected within each soil sampling location (5 m×5 m) by carefully harvesting them from soil mounds. The
tubers were brushed to remove adhering soils, placed in labelled polyethylene bags and transported to the laboratory. Preparation and analysis of soil samples General geochemical characteristics After the removal of debris including plant material and stones, the samples were air-dried, disaggregated, and filtered through a nylon sieve with a 2-mm aperture. A small sub-sample of the
