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Article
Effect of atmospheric mercury deposition on selenium accumulation in rice (Oryza sativa L.) at a mercury mining region in Southwestern China Chao Zhang, Guangle Qiu, Christopher William Noel Anderson, Hua Zhang, Bo Meng, Liang Liang, and Xinbin Feng Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/es505827d • Publication Date (Web): 17 Feb 2015 Downloaded from http://pubs.acs.org on February 18, 2015
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Effect of atmospheric mercury deposition on selenium accumulation
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in rice (Oryza sativa L.) at a mercury mining region in Southwestern
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China
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Chao Zhang1, 2, Guangle Qiu1,*, Christopher W. N. Anderson3, Hua Zhang4, Bo Meng1, Liang Liang1, 2, Xinbin Feng1,* 1
State Key Laboratory of Environmental Geochemistry, Institute of Geochemistry, Chinese Academy of Sciences,
Guiyang 550002, P.R. China 2
Graduate University of Chinese Academy of Sciences, Beijing 100049, P.R. China
3
Soil and Earth Sciences, Institute of Agriculture and Environment, Massey University, Palmerston North, New
Zealand 4
Contaminants in Aquatic Environments, Norwegian Institute for Water Research (NIVA), Gaustadalleen 21, Oslo
0349, Norway
*Corresponding Author: Xinbin Feng Phone: +86-851-5895728 Fax: +86-851-5891721 Email: [email protected]
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Abstract: Selenium (Se) is an important trace element for human nutrition, and has an interactive effect on mercury (Hg) uptake by plants and Hg toxicity in animals. Rice (Oryza sativa L) is the dominant source of dietary Se in China, however the effect of soil Hg contamination on the Se concentration in rice is unknown. We collected 29 whole rice plant samples and corresponding soils from across an active artisanal mercury mining area and an abandoned commercial mercury mining area. The soil Se concentration was similar across the two mining areas and greater than the background concentration for China. However, the Se concentration in rice grain was dramatically different (artisanal area 51±3 ng g-1; abandoned area 235±99 ng g-1). The total gaseous mercury (TGM) concentration in ambient air at the artisanal mining site was significantly greater than at the abandoned area (231 ng m-3 and 34 ng m-3 respectively) and we found a negative correlation between TGM and the Se concentration in grain for the artisanal area. Principal component analysis (PCA) indicated that the source of Se in rice was the atmosphere for the artisanal area (no contribution from soil), and both the atmosphere and soil for the abandoned area. We propose that TGM falls to soil and reacts with Se, inhibiting the translocation of Se to rice grain. Our data suggests that Se intake by the artisanal mining community is insufficient to meet Se dietary requirements, predisposing this community to greater risk from Hg poisoning.
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1. Introduction: Selenium (Se) is an essential trace element for mammalian physiology. However symptoms
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of deficiency or toxicity are apparent outside of the narrow concentration range that is considered
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adequate for physiological function.1 Selenium is recognized to have specific function in cellular
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defense against reactive oxygen species, to protect against carcinogenesis, and to maintain the
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activity of the thyroid hormone.2-3 Selenium is also thought to protect against infection with the
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HIV virus and to inhibit the progression of this virus to AIDS.1, 4
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Human exposure to Se occurs through the diet. Cereals, vegetables and meat have potential to
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deliver adequate levels of dietary intake, however this will depend on the Se concentration in food
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and the amount consumed.5-6 The concentration of Se in food is primarily dependent on the
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concentration and speciation of Se in soil, and the ability of plants to accumulate Se from the soil
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into edible tissues. 7 Consumption of foods that contain less than 0.1 µg g-1 Se will generally lead
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to Se-deficiency, while a concentration greater than 1.0 µg g-1 will result in toxicity.7 The
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recommended dietary allowance (RDA) of Se for humans in the USA and countries of the
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European Commission is 55 µg day-1 for both men and women, while an upper tolerable nutrient
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level (UL) for adults is 400 µg day-1.8-9 China has a maximum food standard limit of 300 ng g-1 Se
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in cereal grains such as rice, and the concentration of Se in rice is regularly assessed as this cereal
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is considered to the staple food for the majority of the Chinese population. Therefore, for much of
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China, daily Se intake is dependent on the Se concentration in rice.10
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Selenium is a rare element in our planet. The mean concentration of Se in igneous bedrock
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(50 ng g-1) is less than any other essential nutrient element.11The provenance of rocks that weather
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to form soil therefore leads to a varied distribution of the Se concentration in soil, and this, in turn,
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affects the concentration of Se in rice (See Supporting Information for details). The global 3
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background concentration of Se in soil is 200 ng g-1, while the background concentration of Se in
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rice is 95 ng g-1.12-13 However, the Se concentration in rice shows large variations across China,
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especially when known areas of seleniferous soil are compared to non-seleniferous areas (See
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Supporting Information for details).
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Plant uptake of Se is dependent on the speciation of Se in the soil. Two species of Se can be
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present under ambient environmental conditions; selenite which is strongly retained to soil
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colloids through the mechanism of specific adsorption, and selenate, which is weakly retained to
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soil colloids due to electrostatic repulsion.14 Selenate is therefore generally more available to
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plants than selenite and is the predominant form of Se in soil under alkaline or well-oxidized
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conditions. However, in highly anoxic and reduced soil, selenite can become the principle species
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of soil Se and this is poorly available to plants.15 Selenate competes with sulfate for uptake by
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plants because of the chemical similarity between selenate and sulfate, and it has been proposed
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that uptake of both species occurs by way of a sulfate transporter in the root plasma membrane.16
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The translocation of Se from root to stem is also highly dependent on the speciation of Se with
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selenate being much more easily transported than selenite or organic Se.17 Plants can also
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accumulate (absorb) Se from the atmosphere via leaf surfaces.16 In the Yangtze River Delta of
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China, a foliage spray of sodium selenite is regularly used to rectify the problem of low Se content
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of rice grains.18
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To protect against an excessive Se concentration in crop plants such as rice, maximum
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guidelines exist for Se in soil. In China the maximum allowable limit for Se in agricultural soil is
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290 ng g-1, a concentration that is coincidental with the soil Se background concentration for all of
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China.19 However, at contaminated locations, total soil Se concentrations can exceed this limit. 4
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The Wanshan Hg mining area of eastern Guizhou Province is one area that has been contaminated
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with Se. Mercury has been recovered from cinnabar ore in the Wanshan area since the Qin
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Dynasty (211 B.C.). Selenium is present at high concentration in the ore20 and has historically
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been released into the environment during ore processing. The background level of Se in soil
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across all of Guizhou Province is 390 ng g-1, 21 higher than the soil Se background value for all of
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China (290 ng g-1)22 and the world (200 ng g-1).23 Commercial-scale mining was closed in 2001,
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but some artisanal and small scale mercury mining is ongoing in the Wanshan mining area
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releasing mercury into the atmosphere today. However, the greatest legacy of mercury pollution is
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from historical and now abandoned large-scale smelting activities. Within the Wanshan area it is
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therefore possible to differentiate between lands that has been subject to historically high Se (and
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Hg) input, and land that is subject to current day Se (and Hg) flux from artisanal and small-scale
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mining. Paddy rice is the dominant crop species grown throughout the Wanshan region and
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monitoring the Se and Hg concentration in rice grains is important to protect public health.24-25
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Few studies have investigated the uptake and translocation of Se in cereal crop plants
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growing in mining areas with high flux of Hg and Se. These two elements are known to have an
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interactive effect on uptake and the subsequent concentration of these elements in cereal
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grains.25-26 In the current study we have investigated the influence of the nature of Se and Hg
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contamination (i.e. historic soil contamination or current day atmospheric contamination) on the
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concentration of Se in tissues of paddy rice (Oryza sativa L). Specifically, we have investigated
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the influence of Hg concentration and flux on the uptake and translocation of Se in rice. This work
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has been carried out in order to provide mechanistic insight into the process of Se uptake by paddy
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rice growing in Hg-contaminated soil. 5
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2. Materials & Methods
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2.1 Study area
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Formal Hg mining in the Wanshan area ceased at the end of 2001. However, illegal artisanal
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mining and smelting activities have continued to produce Hg to the current day. During the
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retorting of cinnabar ore (from both industrial and artisanal activity), mercury and other elements
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present within the ore, including Se (0.02 – 0.87% of the ore), 20 are released into the environment.
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During the current study, rice and soil at a current-day artisanal mining area (sixteen sites), and a
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now-abandoned industrial-scale mining area (thirteen sites) were sampled. All sampling was
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conducted during the rice growing season of 2009. Small-scale smelting was ongoing throughout
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the sampling period, with the consequential released of mercury to the atmosphere. Mining at the
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industrial area ceased in 2001, however, historical large-scale Hg smelting released serious Hg
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contamination to the ambient air, water, soil, sediment, and biota. Wanshan has a subtropical
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monsoon humid climate with an average annual rainfall of 1200-1400 mm and the annual mean
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temperature of 17°C. The altitude of this area ranges from 205 to 1149 m above sea level.
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2.2 Sampling
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Twenty- nine samples of whole rice plant (Oryza sativa L) and corresponding soil samples (from
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10-20 cm depth) were collected by hand from across the study area (Figure 1). The whole rice
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plant samples were washed in the field with tap water to remove soil particles that had adhered to
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the plants’ surface. All rice and soil samples were then sealed in clean polyethylene bags and
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stored in a cooler before being carried to the laboratory.
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In the laboratory, the whole rice plant samples were carefully washed with deionized water 6
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three times, and divided into root, stem, leaf, and seed components with Teflon scissors, then
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freeze dried (EYELA FDU-1100, Tokyo Rikakikai Co. LTD, Japan). The mass of root, stem, leaf,
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and seed was recorded, and these components accounted for 3%, 31%, 10%, and 56% (average) of
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total plant biomass, respectively. The seed was separated into husk and brown rice using a huller.
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A rice milling machine was then used to separate the bran from the brown rice to yield white rice.
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Rice grain, white rice, bran, and husk accounted for 57%, 12% and 31%, respectively of seed
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biomass. All samples were ground to 150 mesh (IKA-A11 basic, IKA, Germany). The grinder and
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huller were thoroughly cleaned before/after processing each sample with ethanol to avoid
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cross-contamination during sample preparation. The powdered samples were kept in sealed
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polyethylene bags.
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Soil samples were freeze-dried (EYELA FDU-1100) and ground to pass through a 200 mesh sieve using an agate mortar and pestle.
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2.3 Analysis
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The experimental protocol employed for plant digestion and soil digestion, the analysis of Se
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concentration in rice plant tissues and soil, the analysis of the total Hg concentration in plants, and
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the analysis of total gaseous mercury (TGM) concentration are described in the Supporting
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Information.
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2.4 Quality assurance and quality control
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Quality assurance and quality control were validated by using duplicates, method blanks, matrix
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spikes, and certified reference materials (CRMs). Details of the protocols employed are presented 7
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in the Supporting Information.
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3. Results and discussion
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3.1 Se in the soil
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The mean concentration of total Se in soil was two-fold greater for the abandoned mining area
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(2,200 ng g-1) than for the current-day artisanal mining area (990 ng g-1)(Table 1). These
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concentrations are 2.6 and 5.6 fold greater than the soil background level of 390 ng g-1 Se for
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Guizhou province, 21 but lower than the soil Se concentration recorded for seleniferous areas such
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as Enshi in Hubei of China (See Supporting Information for details). The higher concentration of
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Se in soil for the abandoned mining area can be attributed to the extent of historical large-scale Hg
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smelting activities in this area. The cumulative release of elements to soil at the abandoned mining
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areas exceeds that at the current-day artisanal mining area.27
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3.2 Se in rice tissues
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The Se concentration varied between the tissues of rice plants collected from the two areas (Table
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2 and Figure 2). For plants collected from the artisanal area, the highest concentration of Se was
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found in roots (average 220 ng g-1), whereas the lowest concentration was found in the polished
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grain (40 ng g-1). In rice plants collected from the abandoned area the Se concentration in root
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ranged from 80 to 1700 ng g-1, with a mean of 520 ng g-1, whereas the concentration in grain
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ranged from 27 to 970 ng g-1 with a mean of 240 ng g-1. Figure 2 shows that the concentration of
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Se in rice tissues collected from both the artisanal and abandoned areas follows the trend root >
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leaf > stem >grain, an observation that is in agreement with the recent findings of Qin et al who 8
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investigated the distribution of Se in rice at Enshi in Hubei Province.28
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There are also differences in the concentration of Se in the various parts of the rice grain,
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with plants from the abandoned area exhibiting a higher concentration of Se in all parts of the
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cereal. The highest concentration of Se in the different components of rice grain was recorded for
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the bran at both areas. The Se concentration of the bran was 3.2- and 2.1-fold higher than the Se
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concentration in white rice and husk for the artisanal area, and 4.3- and 3.5-fold higher than the Se
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in white rice and husk for the abandoned area. Our results are in agreement with those of a
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previous investigation in the Wanshan area which showed that the Se concentration in whole rice
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grain ranged from 20 to 670 ng g-1 with an average of less than 100 ng g-1.26 When compared to
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the global average concentration of Se in white rice 95 ng g-1,13 rice from the abandoned areas
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exceeds the global average, but rice from the artisanal areas is lower (40 and 160 ng g-1 for the
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artisanal and abandoned areas respectively). However, the Se concentrations in the polished rice
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samples collected in this work were much lower than those recorded from the Enshi seleniferous
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region (range: 160 to 10200 ng g-1).28
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According to the mass proportion of root, stem, leaf, and grain in a whole rice plant, and the
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mass proportion of polished rice, bran, and husk in a whole grain, we calculated the relative mass
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distribution of Se throughout rice plants collected from the two areas (Figure 4). Selenium was
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predominantly accumulated in the above-ground parts of rice plants. For the artisanal area, 10% of
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accumulated Se was stored in roots, while 90% was stored in the aerial tissues. These values were
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5% and 95% for the abandoned area. For both areas, the greatest sink of plant Se was in the grain,
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with Se in the grain predominantly accumulated in the polished rice, followed by bran and husk.
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The relative distribution of Se between plant components was similar, despite the large difference 9
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in Se concentration for rice plants collected from the two areas. This indicates that the plant
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actively distributes accumulated Se throughout the various organs.
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The bioaccumulation factors (BAF) of Se in the various tissues of the rice plant are presented
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in Table 2. The BAF of Se in root for both areas was similar. However there was a significant
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difference in the BAF of Se in stem and grain for plants collected from the two areas. In particular,
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the BAF for Se in grain from the abandoned area was double that for the artisanal area (Table 2).
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For both areas the highest BAF was observed in root, followed by leaf, stem and grain, with the
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BAF in all the rice tissues greater at the abandoned area than at the artisanal area.
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3.3 Investigating the source of Se in rice plants
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Principal component analysis (PCA) is a multivariate statistical technique that reduces a large
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number of variables to a small number of factors (principal components or PCs) that can be used
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to explain the relationships and associations among objects and variables.29-31 For example, Shan
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et al.32 applied PCA to extract hidden subsets from a dataset in order to detect possible sources of
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heavy metals in agricultural soils (see Supporting Information). In order to identify the likely
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origin of Se in the plants sampled from the two mining areas, we analyzed the Se concentration of
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soil and the various tissues of rice plants collected from the two areas using PCA statistical
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software (SPSS 18.0).
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Principal Component Analysis of Se concentrations at the artisanal area defines three
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components (PC1, PC2 and PC3) which account for 84% of the variance in the data set (Table 3).
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PC1 expressed high positive loadings on leaf and grain and we interpret the inclusion of these two
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variables in one component to indicate a common origin of Se. Selenium can be accumulated as a 10
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function of stomata uptake of gas phase Se or foliar absorption from particulate material. 33-35 We
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therefore propose that PC1 can be used to infer that the source of Se in the aerial tissues of rice
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plants collected from artisanal area is the ambient air. There is precedent for this inference in
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previous studies that have investigated how atmospheric Se flux can affect plants. Component
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PC2 expressed a high positive loading for stem and a highly negative loading for soil. We interpret
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this to represent an internal phytophysiological transfer process for Se absorbed from the
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atmosphere. PC 3 expressed high positive loadings for all components: root, grain, stem and soil.
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As the stem is the transport channel connecting the root to the grain, we propose that PC3 for the
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artisanal area is an indicator for soil derived Se. The lower total variance described by PC3
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indicates that soil is a minor source for Se uptake by rice plants at the artisanal area.
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Principle Component Analysis of the Se concentrations for the abandoned area defined two
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components which together accounted for 98% of total variance in the data set (PC1 58% and PC2
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40%) (Table 4). Due to high loadings on grain, stem and leaf, but relatively low loading on root,
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we infer that PC1 again describes ambient air as the source of Se. However, the positive loading
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on soil for PC1 indicates that soil has an influence on PC1 for the abandoned area. We propose
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that this influence may be Se volatilized from soil that is subsequently adsorbed by the aerial plant
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tissues; however, the validity of this assumption must be further tested. PC2 has a high loading on
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soil, root and leaf. As these are the two plant components with the highest BAF (Table 2) we infer
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that soil is again the source of Se for PC2. PCA of Se for the abandoned area suggests that there is
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no clear distinction between soil and air as the primary source of this element in rice and describes
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an apparent interaction between these two sources that is not observed for the artisanal area.
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Artisanal smelting of cinnabar ore was ongoing during the rice growing season in 2009 and 11
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therefore there was release of Hg into the atmosphere throughout this period. Monitoring of the
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total gaseous mercury (TGM) concentration in air recorded a mean concentration of 231 ng m-3
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which was significantly higher than the mean concentration recorded for the abandoned area (34
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ng m-3). During smelting other volatile components of the ore will also have been released into the
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atmosphere, including Se. The elevated TGM concentration for the artisanal area relative to the
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abandoned area therefore suggests a differential concentration of Se in the atmosphere between the
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two areas and supports the PCA modeled differential primary origin of Se in rice between the two
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areas. Further research is needed to substantiate this interpretation of the PCA data. Measurement
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of the total gaseous selenium concentration at the two areas and isotopic fingerprinting would
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achieve this aim.
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3.4 Wanshan daily dietary Se intake via rice consumption
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Dumont et al.7 indicated that if the concentration of Se in food is less than 100 ng g-1, symptoms
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of deficiency can be expected in human populations. Across the sampling sites in this study, the Se
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concentration of polished rice exceeded 100 ng g-1 for only 17% of the 29 locations. The potential
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magnitude of this problem can be further considered through analysis of rice consumption habits.
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According to the National Bureau of Statistics of China, the daily per capita consumption of
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rice in 2010 in China was 200 g dry weight per day for adults with an average weight of 60 kg.
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Assuming that 100% of the ingested Se is absorbed in the body, we can approximately calculate
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the adult daily intake of Se via rice consumption in each of the two study areas. For an adult,
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consuming 200 g rice per day containing an average Se concentration of 40 and 160 ng g-1 for the
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artisanal and abandoned mining areas respectively, total daily Se intake will be 8 and 32 µg 12
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respectively (intake will be lower if absorption is not 100%; these values are therefore
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conservative). Based on these calculations, Se intake from rice in the abandoned mining area will
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exceed the WHO/FAO/IAEA guideline level of 30 µg day-1 for women and is close the guideline
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level for men (40 µg day-1).4 However, Se intake from rice in the artisanal mining area is
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considerably lower than the guideline level for both men and women.
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The soil Se concentration at both areas exceeded the Chinese guideline concentration for Se
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in soil. Therefore, the low concentration of Se in rice at the artisanal site cannot be attributed to a
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low soil Se concentration. Instead, we believe the high concentration of Hg in the atmosphere is
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inhibiting Se uptake from soil. Zhang et al.24 , proposed a new criterion for Se and Hg exposure
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assessment, based on their understanding of the interaction between Se and Hg; the physiology
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and toxicology of Se; and the toxicology of Hg. According to Zhang et al., daily dietary Se intake
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can have an important mitigating impact on the toxicity of Hg exposure. However, assessment of
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Se intake alone without considering the potential for interactions with Hg may inadequately reflect
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the Se status of individuals. Applying Zhang et al.’s criterion, the low Se intake predicted for the
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artisanal mining area may lead to both a deficiency of Se and increased risk of Hg toxicity in the
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population.
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3.5 Conceptual model to explain the effect of atmospheric Hg on Se uptake by rice
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According to the Principle Component Analysis, the source of Se in rice across the artisanal
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area is the atmosphere, with little to no accumulation of Se from soil, despite the presence of a
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significant concentration of soil Se. However, across the abandoned area, PCA indicates that rice
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accumulates Se from both the atmosphere and the soil. We believe that the factor controlling the
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uptake of Se from soil is the total gaseous mercury (TGM) concentration in ambient air. Where the 13
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TGM concentration in ambient air is low, rice plants are able to accumulate Se from the soil and to
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translocate this to grain. However, where the TGM concentration in ambient air is high, uptake of
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Se from soil and translocation is restricted. Supporting this hypothesis is a negative correlation
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(R2=0.242, P=0.074) between TGM concentration in ambient air and the concentration of Se in
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grain for the artisanal area only (Figure 3). No similar correlation was found for the abandoned
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area. The rationale for using the correlation between TGM concentration in ambient air and Se
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concentration in grain to qualify the effect of TGM concentration in ambient air is further
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explained in the supporting information.
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Previous work has shown that a high TGM concentration in ambient air due to artisanal and
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small-scale mining will lead to a high flux of mercury to soil through both particulate mercury
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deposition and the presence of dissolved Hg in precipitation.36 Meng et al.36 described how freshly
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deposited inorganic mercury from artisanal and small-scale mining is more chemically reactive
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than Hg that has been in soil for an extended period of time and is readily methylated in soil. This
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MeHg is then accumulated by rice plants, and concentrates in rice grain. Zhang et al.24 showed
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that chemically reactive Hg in soil will readily precipitate Se as a stable and insoluble Hg-Se
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complex in the rhizopshere or on the root surface of rice plants. We therefore propose that the lack
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of Se uptake by rice plants from soil at the artisanal area is due to the removal of bioavailable Se
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from soil solution by chemically reactive Hg that was being released to the atmosphere and falling
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to the ground through the rice sampling period of our study. This mechanism was unique to the
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artisanal area, as there was no active Hg mining across the abandoned area at the time of sampling.
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The abandoned area was characterized by a relatively low TGM concentration in ambient air and
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therefore limited deposition flux of fresh (and chemically reactive) Hg to soil. 14
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3.6 Implications of this model for Wanshan public health
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The two mining areas described in this paper are typical mining areas across the Wanshan region
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of Guizhou, China. The Se concentration in soil varies across Wanshan, but is much higher than
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the global soil Se background level (200 ng g-1).12 Despite the elevated Se concentration in soil,
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the Se concentration in rice is not always high. We have shown that the Se concentration in rice
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grain across the artisanal area is low and may lead to Se deficiency in the human population.
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Foods that contain less than 100 ng g-1 Se will generally lead to Se-deficiency.7 Using this
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criterion value, rice across the artisanal mining area was Se deficient (average concentration 51 ng
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g-1), whereas rice collected from the abandoned areas was sufficient (average concentration 235 ng
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g-1). We do not believe that the explanation for this difference in Se concentration in rice is the Se
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concentration in the soil as soil Se should not be a limiting factor for uptake. Instead we propose
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that the limiting factor for Se concentration in rice is the current-day concentration of Hg in the
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atmosphere, and subsequently, the deposition flux of Hg to the soil. This same deposition flux of
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mercury to soil is now recorded as the source of significant Hg (as MeHg) exposure to inland
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communities of China who consume rice.
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Ralston et al.37 suggested the ratio of Hg to Se may be the critical factor in determining the
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toxicity of Hg. Based on rodent data, Hg exposure that might otherwise produce toxic effects can
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be counteracted by Se, particularly when Se/Hg molar ratios approach or exceed 1:1. At this ratio
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there is adequate Se to prevent Hg toxicity.38 The scenario where artisanal and small scale mining
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leads to a high deposition flux of inorganic mercury to soil may therefore lead to both excessive
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exposure of the local population to Hg (as MeHg), and deficiency of the local population in Se. 15
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We therefore propose that in the context of rice production in artisanal mining areas, Hg
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contamination of the air is a significant threat to the Se nutrition of the mining communities. The
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combined effect of elevated Hg and Hg-induced Se deficiency in rice may be leading to more
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excessive exposure of the artisanal mining communities to Hg toxicity than is currently
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recognized. The interactive effect of these two elements, especially the profound effect of Hg on
341
Se uptake into rice grain, should be assessed more fully in the context of public health. Studies on
342
the effect of Hg on the uptake and accumulation of Se in plants and the underlying mechanisms of
343
this effect, especially phytophysiological processes, should be considered in the future.
344 345
Acknowledgments
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This research was financed by National Key Basic Research Program of China (973 Program
347
2013CB430004), Natural Science Foundation of China (41073098, 41203091, 41073062,
348
41173126, and 11105172), and also financed by the 135 project of IGCAS.
349 350 351
Supporting Information Available
352
Detailed information of sample analysis; detailed information of QA/AC; literature precedent for
353
applying PCA to extract hidden subsets from a dataset in order to detect possible sources;
354
explanation of the correlation between TGM and Se concentration in grain; one tables. This
355
information is available free of charge via the Internet athttp://pubs.acs.org/
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References
358 359 360 361 362 363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384 385 386 387 388 389 390 391 392 393 394 395 396 397 398 399
1. Litov, R. E.; Combs, G. F. Selenium in pediatric nutrition. Pediatrics. 1991, 87 (3), 339-357. 2. Kohrle, J.; Jakob, F.; Contempre, B.; Dumont, J. E. Selenium, the thyroid, and the endocrine system. Endocr. Rev. 2005, 26 (7), 944-984. 3. Bridges, C. C.; Zalups, R. K. Molecular and ionic mimicry and the transport of toxic metals. Toxicol. Appl. Pharmacol. 2005, 204 (3), 274-308. 4. Rayman, M. P. The importance of selenium to human health. Lancet. 2000, 356 (9225), 233-241. 5. Wolf, E.; Kollonitsch, V.; Kline, C. H. A survey of selenium treatment in livestock production. J. Agr. Food. Chem. 1963, 11 (4). 6. Chen, X. S.; Yang, G. Q.; Chen, J. S.; Chen, X. C.; Wen, Z. M.; Ge, K. Y. Studies on the relations of selenium and Keshan disease. Biol. Trace. Elem. Res. 1980, 2 (2), 91-107. 7. Dumont, E.; Vanhaecke, F.; Cornelis, R. Selenium speciation from food source to metabolites: a critical review. Anal. Bioanal. Chem. 2006, 385 (7), 1304-1323. 8. Monsen, E. R. Dietary Reference intakes for the antioxidant nutrients: Vitamin C, vitamin E, selenium, and carotenoids. J. Am. Diet. Assn. 2000, 100 (9), 1008-1009. 9. WHO.; FAO. Vitamin and mineral requirements in human nutrition (2nd edition), World Health Organization and Food and Agriculture Organization of the United Nations: Rome, Italy. 2004. ISBN 92 4 154612 3. 10. Food and Agriculture Organization of the United Nations Website; http://www.fao.org/ newsroom/en/news/2006/1000267/index.html. “Rice Is Life”: International Rice Commission Meets in Peru. 2006. 11. Fordyce, F. M. Selenium deficiency and toxicity in the environment. In: Selinus, O., (ed.) Essentials of medical geology. Elsevier, 2005. 12. Swaine, D. J. The trace element content in soil; Technical communication of the Commonwealth Bureau of Soil Science, Commonwealth Agricultural Bureau, England, 1995. 13. Williams, P. N.; Lombi, E.; Sun, G. X.; Scheckel, K.; Zhu, Y. G.; Feng, X. B.; Zhu, J. M.; Carey, A. M.; Adomako, E.; Lawgali, Y.; Deacon, C.; Meharg, A. A. Selenium Characterization in the Global Rice Supply Chain. Environ. Sci. Technol. 2009, 43 (15), 6024-6030. 14. Barrow, N.; Cartes, P.; Mora, M. Modifications to the Freundlich equation to describe anion sorption over a large range and to describe competition between pairs of ions. Eur. J. Soil. Sci. 2005, 56 (5), 601-606. 15. Arvy, M. P. Selenate and selenite uptake and translocation in bean plants (Phaseolus vulgaris). J. Exp. Bot. 1993, 44 (6), 1083-1087. 16. Terry, N.; Zayed, A. M.; De Souza, M. P.; Tarun, A. S. Selenium in higher plants. Annu. Rev. Plant. Biol. 2000, 51 (1), 401-432. 17. Zayed, A.; Lytle, C. M.; Terry, N. Accumulation and volatilization of different chemical species of selenium by plants. Planta 1998, 206 (2), 284-292. 18. Cao, Z. H.; Wang, X. C.; Yao, D. H.; Zhang, X. L.; Wong, M. H. Selenium geochemistry of paddy soils in Yangtze River Delta. Environ. Int. 2001, 26 (5-6), 335-339. 19. CNEMC. (China National Environmental Monitoring Center). Background concentrations of elements in soils of China. China Environmental Science Press: Beijing. 1990 (in Chinese). 20. Bao, Z. X.; Bao, J. M. The occurrences of selenium in the western Hunan-eastern Guizhou 17
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mercury ore belt. Geol. Explor. Nonferr. Metal. 1995, 4 (1), 30-34 (in Chinese). 21. Wang, G. L.; Zhu, X. Q. A background survey on seleniun in soil of Guizhou Provience. Res. Environ. Sci. 2003, 16 (1), 23-26. 22. Zhu, Z. M.; Lu, L. N.; Liu, W. The element background of Chinese soil; China Environmental Science Press: Beijing, 1990 (in Chinese). 23. Lisk, D. J. Trace metals in soils, plants, and animals. Adv. Agron. 1972, 24, 267-325. 24. Zhang, H.; Feng, X. B.; Chan, H. M.; Larssen, T. New insights into traditional health risk assessments of mercury exposure: implications of selenium. Environ. Sci. Technol. 2014, 48 (2), 1206-1212. 25. Zhang, H.; Feng, X. B.; Jiang, C. X.; Li, Q. H.; Liu, Y.; Gu, C. H.; Shang, L. H.; Li, P.; Lin, Y.; Larssen, T. Understanding the paradox of selenium contamination in mercury mining areas: High soil content and low accumulation in rice. Environ. Pollut. 2014, 188 (0), 27-36. 26. Zhang, H.; Feng, X. B.; Zhu, J. M.; Sapkota, A.; Meng, B.; Yao, H.; Qin, H.; Larssen, T. Selenium in soil inhibits mercury uptake and translocation in rice (Oryza sativa L.). Environ. Sci. Technol. 2012, 46, 10040-10046. 27. Meng, B.; Feng, X. B.; Qiu, G. L.; Cai, Y.; Wang, D. Y.; Li, P.; Shang, L. H.; Sommar, J. Distribution Patterns of Inorganic Mercury and Methylmercury in Tissues of Rice (Oryza sativa L.) Plants and Possible Bioaccumulation Pathways. J. Agr. Food Chem. 2010, 58 (8), 4951-4958. 28. Qin, H. B.; Zhu, J. M.; Liang, L.; Wang, M. S.; Su, H. The bioavailability of selenium and risk assessment for human selenium poisoning in high-Se areas, China. Environ. Int. 2013, 52, 66-74. 29. Wold, S.; Esbensen, K.; Geladi, P. Principal component analysis. Chemometr. Intel. Lab. Syst. 1987, 2 (1), 37-52. 30. Jackson, J. E. A user's guide to principal components. Wiley Series in Probability and Statistics, John Wiley & Sons Inc., 2005. 31. Jolliffe, I. T. Principal component analysis (2nd edition), Springer Series in Statistics, Springer: New York, U. S., 2002.. 32. Shan, Y. S.; Tysklind, M.; Hao, F. H.; Ouyang, W.; Chen, S. Y.; Lin, C. Y. Identification of sources of heavy metals in agricultural soils using multivariate analysis and GIS. J. Soil. Sediment. 2013, 13 (4), 720-729. 33. Haygarth, P. M.; Cooke, A. I.; Jones, K. C.; Harrison, A. F.; Johnston, A. E. Long-term change in the biogeochemical cycling of atmospheric selenium-deposition to plants and soil. J. Geophys. Res. 1993, 98 (D9), 16769-16776. 34. Haygarth, P. M.; Harrison, A. F.; Jones, K. C. Plant seleniun from soil and the atmosphere. J. Environ. Qual. 1995, 24 (4), 768-771. 35. Liu, G. J.; Zhang, Y.; Qi, C.; Zheng, L. G.; Chen, Y. W.; Peng, Z. C. Comparative on causes and accumulation of selenium in the tree-rings ambient high-selenium coal combustion area from Yutangba, Hubei, China. Environ. Monit. Assess. 2007, 133 (1-3), 99-103. 36. Meng, B.; Feng, X. B.; Qiu, G. L.; Liang, P.; Li, P.; Chen, C. X.; Shang, L. H. The Process of Methylmercury Accumulation in Rice (Oryza sativa L.). Environ. Sci. Technol. 2011, 45 (7), 2711-2717. 37. Ralston, N. V. C.; Ralston, C. R.; Blackwell, J. L.; Raymond, L. J. Dietary and tissue selenium in relation to methylmercury toxicity. Neurotoxicology. 2008, 29 (5), 802-811. 38. Peterson, S. A.; Ralston, N. V. C.; Peck, D. V.; Van Sickle, J.; Robertson, J. D.; Spate, V. L.; 18
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Morris, J. S. How Might Selenium Moderate the Toxic Effects of Mercury in Stream Fish of the Western US? Environ. Sci. Technol. 2009, 43 (10), 3919-3925.
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Table 1 Concentration of total Se in tissues of rice plant as a function of the two sampling areas
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(ng g-1)
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Table 2 Bioaccumulation factors (BAF) of Se in tissues of the rice plant as a function of sampling
450
area. BAF is calculated as the Se concentration in the tissues of rice plant/Se concentration in soil.
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Table 3 Rotated factor loadings and percent variance for the two principal components (PC) of Se
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in rice tissues and soil for the artisanal area
453
Table 4 Rotated factor loadings and percent variance for the two principal components (PC) of Se
454
in rice tissues and soil for the abandon area
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Table 1 Tissues, ng g-1
Artisanal area
Abandoned area
Mean±Std.E
Range
Mean±Std.E
Range
Polished
40±6
17-130
160±64
13-650
Bran
99±10
42-180
680±290
52-2900
Husk
52±4
26-82
200±75
36-820
Grain
51±3
23-76
235±99
27-970
Root
220±19
70-340
520±160
80-1700
Stem
66±7
27-120
330±140
35-1600
Leaf
150±15
67-280
440±150
63-1500
Soil
990±92
370-1900
2200±660
540-8900
457 458
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Table 2 Tissues Grain Root Stem Leaf
Artisanal area
Abandoned area
0.05 0.22 0.07 0.15
0.11 0.24 0.15 0.2
460
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Se
PC 1
PC 2
PC 3
Grain Stem Leaf Root Soil % of variance explained cumulative % of total variance
0.657 -0.410 0.922 0.127 -0.371 29
0.383 0.812 0.048 0.041 -0.791 29
0.442 0.390 0.036 0.936 0.262 26 84
Extraction method: principal component analysis. Rotation method: Varimax with Kaiser Normalization.
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Table 4 Se
PC 1
PC 2
Grain Stem Leaf Root Soil % of variance explained cumulative % of total variance
0.921 0.940 0.747 0.722 0.325 58
0.375 0.339 0.655 0.664 0.943 40 98
Extraction method: principal component analysis. Rotation method: Varimax with Kaiser Normalization.
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Figure 1. The study area and location of the sampling sites (Area A is the artisanal area, Area B is
472
the abandoned area)
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Figure 2. Total Se concentration in different tissues of rice plant collected from the two areas
474
(with Std. Error) (Area A is the artisanal area, Area B is the abandoned area)
475
Figure 3. Concentration of Se in the grain as a function of TGM for the two areas (Area A is the
476
artisanal area, Area B is the abandoned area)
477
Figure 4. The relative distribution of Se in the tissues of rice plants from the artisanal area (Area
478
A) and abandoned area (Area B)
479
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Figure 1.
481 482
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Figure 2.
1000
1000
800
800
600
700
200
-1
Total Se concerntation (ng g )
700
100
600
-1
900
900
Total Se concerntation (ng g )
483
Area A Area B
0
500
Polished
Bran
Husk
Tissues of grain
400 300 200 100 0 Grain
Stem
Leaf
Root
Tissues of rice plant
484 485
27
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Figure 3. Concentrations of Se in grain (ng/g)
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A
80
B
1000
R2=0.242, P=0.074
70
2
R =3E-05, P=0.921
800
60 600 50 400
40
200
30
0
20 0
100
200
300
400
500
600
700
20
TGM (ng/m3)
30
40
50
60
TGM (ng/m3)
487 488
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Figure 4.
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Article
Effect of atmospheric mercury deposition on selenium accumulation in rice (Oryza sativa L.) at a mercury mining region in Southwestern China Chao Zhang, Guangle Qiu, Christopher William Noel Anderson, Hua Zhang, Bo Meng, Liang Liang, and Xinbin Feng Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/es505827d • Publication Date (Web): 17 Feb 2015 Downloaded from http://pubs.acs.org on February 18, 2015
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Effect of atmospheric mercury deposition on selenium accumulation
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in rice (Oryza sativa L.) at a mercury mining region in Southwestern
3
China
4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24
Chao Zhang1, 2, Guangle Qiu1,*, Christopher W. N. Anderson3, Hua Zhang4, Bo Meng1, Liang Liang1, 2, Xinbin Feng1,* 1
State Key Laboratory of Environmental Geochemistry, Institute of Geochemistry, Chinese Academy of Sciences,
Guiyang 550002, P.R. China 2
Graduate University of Chinese Academy of Sciences, Beijing 100049, P.R. China
3
Soil and Earth Sciences, Institute of Agriculture and Environment, Massey University, Palmerston North, New
Zealand 4
Contaminants in Aquatic Environments, Norwegian Institute for Water Research (NIVA), Gaustadalleen 21, Oslo
0349, Norway
*Corresponding Author: Xinbin Feng Phone: +86-851-5895728 Fax: +86-851-5891721 Email: [email protected]
25
1
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Abstract: Selenium (Se) is an important trace element for human nutrition, and has an interactive effect on mercury (Hg) uptake by plants and Hg toxicity in animals. Rice (Oryza sativa L) is the dominant source of dietary Se in China, however the effect of soil Hg contamination on the Se concentration in rice is unknown. We collected 29 whole rice plant samples and corresponding soils from across an active artisanal mercury mining area and an abandoned commercial mercury mining area. The soil Se concentration was similar across the two mining areas and greater than the background concentration for China. However, the Se concentration in rice grain was dramatically different (artisanal area 51±3 ng g-1; abandoned area 235±99 ng g-1). The total gaseous mercury (TGM) concentration in ambient air at the artisanal mining site was significantly greater than at the abandoned area (231 ng m-3 and 34 ng m-3 respectively) and we found a negative correlation between TGM and the Se concentration in grain for the artisanal area. Principal component analysis (PCA) indicated that the source of Se in rice was the atmosphere for the artisanal area (no contribution from soil), and both the atmosphere and soil for the abandoned area. We propose that TGM falls to soil and reacts with Se, inhibiting the translocation of Se to rice grain. Our data suggests that Se intake by the artisanal mining community is insufficient to meet Se dietary requirements, predisposing this community to greater risk from Hg poisoning.
TOC/Abstract Art
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1. Introduction: Selenium (Se) is an essential trace element for mammalian physiology. However symptoms
51
of deficiency or toxicity are apparent outside of the narrow concentration range that is considered
52
adequate for physiological function.1 Selenium is recognized to have specific function in cellular
53
defense against reactive oxygen species, to protect against carcinogenesis, and to maintain the
54
activity of the thyroid hormone.2-3 Selenium is also thought to protect against infection with the
55
HIV virus and to inhibit the progression of this virus to AIDS.1, 4
56
Human exposure to Se occurs through the diet. Cereals, vegetables and meat have potential to
57
deliver adequate levels of dietary intake, however this will depend on the Se concentration in food
58
and the amount consumed.5-6 The concentration of Se in food is primarily dependent on the
59
concentration and speciation of Se in soil, and the ability of plants to accumulate Se from the soil
60
into edible tissues. 7 Consumption of foods that contain less than 0.1 µg g-1 Se will generally lead
61
to Se-deficiency, while a concentration greater than 1.0 µg g-1 will result in toxicity.7 The
62
recommended dietary allowance (RDA) of Se for humans in the USA and countries of the
63
European Commission is 55 µg day-1 for both men and women, while an upper tolerable nutrient
64
level (UL) for adults is 400 µg day-1.8-9 China has a maximum food standard limit of 300 ng g-1 Se
65
in cereal grains such as rice, and the concentration of Se in rice is regularly assessed as this cereal
66
is considered to the staple food for the majority of the Chinese population. Therefore, for much of
67
China, daily Se intake is dependent on the Se concentration in rice.10
68
Selenium is a rare element in our planet. The mean concentration of Se in igneous bedrock
69
(50 ng g-1) is less than any other essential nutrient element.11The provenance of rocks that weather
70
to form soil therefore leads to a varied distribution of the Se concentration in soil, and this, in turn,
71
affects the concentration of Se in rice (See Supporting Information for details). The global 3
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background concentration of Se in soil is 200 ng g-1, while the background concentration of Se in
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rice is 95 ng g-1.12-13 However, the Se concentration in rice shows large variations across China,
74
especially when known areas of seleniferous soil are compared to non-seleniferous areas (See
75
Supporting Information for details).
76
Plant uptake of Se is dependent on the speciation of Se in the soil. Two species of Se can be
77
present under ambient environmental conditions; selenite which is strongly retained to soil
78
colloids through the mechanism of specific adsorption, and selenate, which is weakly retained to
79
soil colloids due to electrostatic repulsion.14 Selenate is therefore generally more available to
80
plants than selenite and is the predominant form of Se in soil under alkaline or well-oxidized
81
conditions. However, in highly anoxic and reduced soil, selenite can become the principle species
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of soil Se and this is poorly available to plants.15 Selenate competes with sulfate for uptake by
83
plants because of the chemical similarity between selenate and sulfate, and it has been proposed
84
that uptake of both species occurs by way of a sulfate transporter in the root plasma membrane.16
85
The translocation of Se from root to stem is also highly dependent on the speciation of Se with
86
selenate being much more easily transported than selenite or organic Se.17 Plants can also
87
accumulate (absorb) Se from the atmosphere via leaf surfaces.16 In the Yangtze River Delta of
88
China, a foliage spray of sodium selenite is regularly used to rectify the problem of low Se content
89
of rice grains.18
90
To protect against an excessive Se concentration in crop plants such as rice, maximum
91
guidelines exist for Se in soil. In China the maximum allowable limit for Se in agricultural soil is
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290 ng g-1, a concentration that is coincidental with the soil Se background concentration for all of
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China.19 However, at contaminated locations, total soil Se concentrations can exceed this limit. 4
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The Wanshan Hg mining area of eastern Guizhou Province is one area that has been contaminated
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with Se. Mercury has been recovered from cinnabar ore in the Wanshan area since the Qin
96
Dynasty (211 B.C.). Selenium is present at high concentration in the ore20 and has historically
97
been released into the environment during ore processing. The background level of Se in soil
98
across all of Guizhou Province is 390 ng g-1, 21 higher than the soil Se background value for all of
99
China (290 ng g-1)22 and the world (200 ng g-1).23 Commercial-scale mining was closed in 2001,
100
but some artisanal and small scale mercury mining is ongoing in the Wanshan mining area
101
releasing mercury into the atmosphere today. However, the greatest legacy of mercury pollution is
102
from historical and now abandoned large-scale smelting activities. Within the Wanshan area it is
103
therefore possible to differentiate between lands that has been subject to historically high Se (and
104
Hg) input, and land that is subject to current day Se (and Hg) flux from artisanal and small-scale
105
mining. Paddy rice is the dominant crop species grown throughout the Wanshan region and
106
monitoring the Se and Hg concentration in rice grains is important to protect public health.24-25
107
Few studies have investigated the uptake and translocation of Se in cereal crop plants
108
growing in mining areas with high flux of Hg and Se. These two elements are known to have an
109
interactive effect on uptake and the subsequent concentration of these elements in cereal
110
grains.25-26 In the current study we have investigated the influence of the nature of Se and Hg
111
contamination (i.e. historic soil contamination or current day atmospheric contamination) on the
112
concentration of Se in tissues of paddy rice (Oryza sativa L). Specifically, we have investigated
113
the influence of Hg concentration and flux on the uptake and translocation of Se in rice. This work
114
has been carried out in order to provide mechanistic insight into the process of Se uptake by paddy
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rice growing in Hg-contaminated soil. 5
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2. Materials & Methods
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2.1 Study area
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Formal Hg mining in the Wanshan area ceased at the end of 2001. However, illegal artisanal
119
mining and smelting activities have continued to produce Hg to the current day. During the
120
retorting of cinnabar ore (from both industrial and artisanal activity), mercury and other elements
121
present within the ore, including Se (0.02 – 0.87% of the ore), 20 are released into the environment.
122
During the current study, rice and soil at a current-day artisanal mining area (sixteen sites), and a
123
now-abandoned industrial-scale mining area (thirteen sites) were sampled. All sampling was
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conducted during the rice growing season of 2009. Small-scale smelting was ongoing throughout
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the sampling period, with the consequential released of mercury to the atmosphere. Mining at the
126
industrial area ceased in 2001, however, historical large-scale Hg smelting released serious Hg
127
contamination to the ambient air, water, soil, sediment, and biota. Wanshan has a subtropical
128
monsoon humid climate with an average annual rainfall of 1200-1400 mm and the annual mean
129
temperature of 17°C. The altitude of this area ranges from 205 to 1149 m above sea level.
130 131
2.2 Sampling
132
Twenty- nine samples of whole rice plant (Oryza sativa L) and corresponding soil samples (from
133
10-20 cm depth) were collected by hand from across the study area (Figure 1). The whole rice
134
plant samples were washed in the field with tap water to remove soil particles that had adhered to
135
the plants’ surface. All rice and soil samples were then sealed in clean polyethylene bags and
136
stored in a cooler before being carried to the laboratory.
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In the laboratory, the whole rice plant samples were carefully washed with deionized water 6
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three times, and divided into root, stem, leaf, and seed components with Teflon scissors, then
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freeze dried (EYELA FDU-1100, Tokyo Rikakikai Co. LTD, Japan). The mass of root, stem, leaf,
140
and seed was recorded, and these components accounted for 3%, 31%, 10%, and 56% (average) of
141
total plant biomass, respectively. The seed was separated into husk and brown rice using a huller.
142
A rice milling machine was then used to separate the bran from the brown rice to yield white rice.
143
Rice grain, white rice, bran, and husk accounted for 57%, 12% and 31%, respectively of seed
144
biomass. All samples were ground to 150 mesh (IKA-A11 basic, IKA, Germany). The grinder and
145
huller were thoroughly cleaned before/after processing each sample with ethanol to avoid
146
cross-contamination during sample preparation. The powdered samples were kept in sealed
147
polyethylene bags.
148 149
Soil samples were freeze-dried (EYELA FDU-1100) and ground to pass through a 200 mesh sieve using an agate mortar and pestle.
150 151
2.3 Analysis
152
The experimental protocol employed for plant digestion and soil digestion, the analysis of Se
153
concentration in rice plant tissues and soil, the analysis of the total Hg concentration in plants, and
154
the analysis of total gaseous mercury (TGM) concentration are described in the Supporting
155
Information.
156 157
2.4 Quality assurance and quality control
158
Quality assurance and quality control were validated by using duplicates, method blanks, matrix
159
spikes, and certified reference materials (CRMs). Details of the protocols employed are presented 7
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in the Supporting Information.
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3. Results and discussion
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3.1 Se in the soil
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The mean concentration of total Se in soil was two-fold greater for the abandoned mining area
165
(2,200 ng g-1) than for the current-day artisanal mining area (990 ng g-1)(Table 1). These
166
concentrations are 2.6 and 5.6 fold greater than the soil background level of 390 ng g-1 Se for
167
Guizhou province, 21 but lower than the soil Se concentration recorded for seleniferous areas such
168
as Enshi in Hubei of China (See Supporting Information for details). The higher concentration of
169
Se in soil for the abandoned mining area can be attributed to the extent of historical large-scale Hg
170
smelting activities in this area. The cumulative release of elements to soil at the abandoned mining
171
areas exceeds that at the current-day artisanal mining area.27
172 173
3.2 Se in rice tissues
174
The Se concentration varied between the tissues of rice plants collected from the two areas (Table
175
2 and Figure 2). For plants collected from the artisanal area, the highest concentration of Se was
176
found in roots (average 220 ng g-1), whereas the lowest concentration was found in the polished
177
grain (40 ng g-1). In rice plants collected from the abandoned area the Se concentration in root
178
ranged from 80 to 1700 ng g-1, with a mean of 520 ng g-1, whereas the concentration in grain
179
ranged from 27 to 970 ng g-1 with a mean of 240 ng g-1. Figure 2 shows that the concentration of
180
Se in rice tissues collected from both the artisanal and abandoned areas follows the trend root >
181
leaf > stem >grain, an observation that is in agreement with the recent findings of Qin et al who 8
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investigated the distribution of Se in rice at Enshi in Hubei Province.28
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There are also differences in the concentration of Se in the various parts of the rice grain,
184
with plants from the abandoned area exhibiting a higher concentration of Se in all parts of the
185
cereal. The highest concentration of Se in the different components of rice grain was recorded for
186
the bran at both areas. The Se concentration of the bran was 3.2- and 2.1-fold higher than the Se
187
concentration in white rice and husk for the artisanal area, and 4.3- and 3.5-fold higher than the Se
188
in white rice and husk for the abandoned area. Our results are in agreement with those of a
189
previous investigation in the Wanshan area which showed that the Se concentration in whole rice
190
grain ranged from 20 to 670 ng g-1 with an average of less than 100 ng g-1.26 When compared to
191
the global average concentration of Se in white rice 95 ng g-1,13 rice from the abandoned areas
192
exceeds the global average, but rice from the artisanal areas is lower (40 and 160 ng g-1 for the
193
artisanal and abandoned areas respectively). However, the Se concentrations in the polished rice
194
samples collected in this work were much lower than those recorded from the Enshi seleniferous
195
region (range: 160 to 10200 ng g-1).28
196
According to the mass proportion of root, stem, leaf, and grain in a whole rice plant, and the
197
mass proportion of polished rice, bran, and husk in a whole grain, we calculated the relative mass
198
distribution of Se throughout rice plants collected from the two areas (Figure 4). Selenium was
199
predominantly accumulated in the above-ground parts of rice plants. For the artisanal area, 10% of
200
accumulated Se was stored in roots, while 90% was stored in the aerial tissues. These values were
201
5% and 95% for the abandoned area. For both areas, the greatest sink of plant Se was in the grain,
202
with Se in the grain predominantly accumulated in the polished rice, followed by bran and husk.
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The relative distribution of Se between plant components was similar, despite the large difference 9
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in Se concentration for rice plants collected from the two areas. This indicates that the plant
205
actively distributes accumulated Se throughout the various organs.
206
The bioaccumulation factors (BAF) of Se in the various tissues of the rice plant are presented
207
in Table 2. The BAF of Se in root for both areas was similar. However there was a significant
208
difference in the BAF of Se in stem and grain for plants collected from the two areas. In particular,
209
the BAF for Se in grain from the abandoned area was double that for the artisanal area (Table 2).
210
For both areas the highest BAF was observed in root, followed by leaf, stem and grain, with the
211
BAF in all the rice tissues greater at the abandoned area than at the artisanal area.
212 213
3.3 Investigating the source of Se in rice plants
214
Principal component analysis (PCA) is a multivariate statistical technique that reduces a large
215
number of variables to a small number of factors (principal components or PCs) that can be used
216
to explain the relationships and associations among objects and variables.29-31 For example, Shan
217
et al.32 applied PCA to extract hidden subsets from a dataset in order to detect possible sources of
218
heavy metals in agricultural soils (see Supporting Information). In order to identify the likely
219
origin of Se in the plants sampled from the two mining areas, we analyzed the Se concentration of
220
soil and the various tissues of rice plants collected from the two areas using PCA statistical
221
software (SPSS 18.0).
222
Principal Component Analysis of Se concentrations at the artisanal area defines three
223
components (PC1, PC2 and PC3) which account for 84% of the variance in the data set (Table 3).
224
PC1 expressed high positive loadings on leaf and grain and we interpret the inclusion of these two
225
variables in one component to indicate a common origin of Se. Selenium can be accumulated as a 10
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function of stomata uptake of gas phase Se or foliar absorption from particulate material. 33-35 We
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therefore propose that PC1 can be used to infer that the source of Se in the aerial tissues of rice
228
plants collected from artisanal area is the ambient air. There is precedent for this inference in
229
previous studies that have investigated how atmospheric Se flux can affect plants. Component
230
PC2 expressed a high positive loading for stem and a highly negative loading for soil. We interpret
231
this to represent an internal phytophysiological transfer process for Se absorbed from the
232
atmosphere. PC 3 expressed high positive loadings for all components: root, grain, stem and soil.
233
As the stem is the transport channel connecting the root to the grain, we propose that PC3 for the
234
artisanal area is an indicator for soil derived Se. The lower total variance described by PC3
235
indicates that soil is a minor source for Se uptake by rice plants at the artisanal area.
236
Principle Component Analysis of the Se concentrations for the abandoned area defined two
237
components which together accounted for 98% of total variance in the data set (PC1 58% and PC2
238
40%) (Table 4). Due to high loadings on grain, stem and leaf, but relatively low loading on root,
239
we infer that PC1 again describes ambient air as the source of Se. However, the positive loading
240
on soil for PC1 indicates that soil has an influence on PC1 for the abandoned area. We propose
241
that this influence may be Se volatilized from soil that is subsequently adsorbed by the aerial plant
242
tissues; however, the validity of this assumption must be further tested. PC2 has a high loading on
243
soil, root and leaf. As these are the two plant components with the highest BAF (Table 2) we infer
244
that soil is again the source of Se for PC2. PCA of Se for the abandoned area suggests that there is
245
no clear distinction between soil and air as the primary source of this element in rice and describes
246
an apparent interaction between these two sources that is not observed for the artisanal area.
247
Artisanal smelting of cinnabar ore was ongoing during the rice growing season in 2009 and 11
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therefore there was release of Hg into the atmosphere throughout this period. Monitoring of the
249
total gaseous mercury (TGM) concentration in air recorded a mean concentration of 231 ng m-3
250
which was significantly higher than the mean concentration recorded for the abandoned area (34
251
ng m-3). During smelting other volatile components of the ore will also have been released into the
252
atmosphere, including Se. The elevated TGM concentration for the artisanal area relative to the
253
abandoned area therefore suggests a differential concentration of Se in the atmosphere between the
254
two areas and supports the PCA modeled differential primary origin of Se in rice between the two
255
areas. Further research is needed to substantiate this interpretation of the PCA data. Measurement
256
of the total gaseous selenium concentration at the two areas and isotopic fingerprinting would
257
achieve this aim.
258 259
3.4 Wanshan daily dietary Se intake via rice consumption
260
Dumont et al.7 indicated that if the concentration of Se in food is less than 100 ng g-1, symptoms
261
of deficiency can be expected in human populations. Across the sampling sites in this study, the Se
262
concentration of polished rice exceeded 100 ng g-1 for only 17% of the 29 locations. The potential
263
magnitude of this problem can be further considered through analysis of rice consumption habits.
264
According to the National Bureau of Statistics of China, the daily per capita consumption of
265
rice in 2010 in China was 200 g dry weight per day for adults with an average weight of 60 kg.
266
Assuming that 100% of the ingested Se is absorbed in the body, we can approximately calculate
267
the adult daily intake of Se via rice consumption in each of the two study areas. For an adult,
268
consuming 200 g rice per day containing an average Se concentration of 40 and 160 ng g-1 for the
269
artisanal and abandoned mining areas respectively, total daily Se intake will be 8 and 32 µg 12
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respectively (intake will be lower if absorption is not 100%; these values are therefore
271
conservative). Based on these calculations, Se intake from rice in the abandoned mining area will
272
exceed the WHO/FAO/IAEA guideline level of 30 µg day-1 for women and is close the guideline
273
level for men (40 µg day-1).4 However, Se intake from rice in the artisanal mining area is
274
considerably lower than the guideline level for both men and women.
275
The soil Se concentration at both areas exceeded the Chinese guideline concentration for Se
276
in soil. Therefore, the low concentration of Se in rice at the artisanal site cannot be attributed to a
277
low soil Se concentration. Instead, we believe the high concentration of Hg in the atmosphere is
278
inhibiting Se uptake from soil. Zhang et al.24 , proposed a new criterion for Se and Hg exposure
279
assessment, based on their understanding of the interaction between Se and Hg; the physiology
280
and toxicology of Se; and the toxicology of Hg. According to Zhang et al., daily dietary Se intake
281
can have an important mitigating impact on the toxicity of Hg exposure. However, assessment of
282
Se intake alone without considering the potential for interactions with Hg may inadequately reflect
283
the Se status of individuals. Applying Zhang et al.’s criterion, the low Se intake predicted for the
284
artisanal mining area may lead to both a deficiency of Se and increased risk of Hg toxicity in the
285
population.
286
3.5 Conceptual model to explain the effect of atmospheric Hg on Se uptake by rice
287
According to the Principle Component Analysis, the source of Se in rice across the artisanal
288
area is the atmosphere, with little to no accumulation of Se from soil, despite the presence of a
289
significant concentration of soil Se. However, across the abandoned area, PCA indicates that rice
290
accumulates Se from both the atmosphere and the soil. We believe that the factor controlling the
291
uptake of Se from soil is the total gaseous mercury (TGM) concentration in ambient air. Where the 13
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TGM concentration in ambient air is low, rice plants are able to accumulate Se from the soil and to
293
translocate this to grain. However, where the TGM concentration in ambient air is high, uptake of
294
Se from soil and translocation is restricted. Supporting this hypothesis is a negative correlation
295
(R2=0.242, P=0.074) between TGM concentration in ambient air and the concentration of Se in
296
grain for the artisanal area only (Figure 3). No similar correlation was found for the abandoned
297
area. The rationale for using the correlation between TGM concentration in ambient air and Se
298
concentration in grain to qualify the effect of TGM concentration in ambient air is further
299
explained in the supporting information.
300
Previous work has shown that a high TGM concentration in ambient air due to artisanal and
301
small-scale mining will lead to a high flux of mercury to soil through both particulate mercury
302
deposition and the presence of dissolved Hg in precipitation.36 Meng et al.36 described how freshly
303
deposited inorganic mercury from artisanal and small-scale mining is more chemically reactive
304
than Hg that has been in soil for an extended period of time and is readily methylated in soil. This
305
MeHg is then accumulated by rice plants, and concentrates in rice grain. Zhang et al.24 showed
306
that chemically reactive Hg in soil will readily precipitate Se as a stable and insoluble Hg-Se
307
complex in the rhizopshere or on the root surface of rice plants. We therefore propose that the lack
308
of Se uptake by rice plants from soil at the artisanal area is due to the removal of bioavailable Se
309
from soil solution by chemically reactive Hg that was being released to the atmosphere and falling
310
to the ground through the rice sampling period of our study. This mechanism was unique to the
311
artisanal area, as there was no active Hg mining across the abandoned area at the time of sampling.
312
The abandoned area was characterized by a relatively low TGM concentration in ambient air and
313
therefore limited deposition flux of fresh (and chemically reactive) Hg to soil. 14
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3.6 Implications of this model for Wanshan public health
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The two mining areas described in this paper are typical mining areas across the Wanshan region
317
of Guizhou, China. The Se concentration in soil varies across Wanshan, but is much higher than
318
the global soil Se background level (200 ng g-1).12 Despite the elevated Se concentration in soil,
319
the Se concentration in rice is not always high. We have shown that the Se concentration in rice
320
grain across the artisanal area is low and may lead to Se deficiency in the human population.
321
Foods that contain less than 100 ng g-1 Se will generally lead to Se-deficiency.7 Using this
322
criterion value, rice across the artisanal mining area was Se deficient (average concentration 51 ng
323
g-1), whereas rice collected from the abandoned areas was sufficient (average concentration 235 ng
324
g-1). We do not believe that the explanation for this difference in Se concentration in rice is the Se
325
concentration in the soil as soil Se should not be a limiting factor for uptake. Instead we propose
326
that the limiting factor for Se concentration in rice is the current-day concentration of Hg in the
327
atmosphere, and subsequently, the deposition flux of Hg to the soil. This same deposition flux of
328
mercury to soil is now recorded as the source of significant Hg (as MeHg) exposure to inland
329
communities of China who consume rice.
330
Ralston et al.37 suggested the ratio of Hg to Se may be the critical factor in determining the
331
toxicity of Hg. Based on rodent data, Hg exposure that might otherwise produce toxic effects can
332
be counteracted by Se, particularly when Se/Hg molar ratios approach or exceed 1:1. At this ratio
333
there is adequate Se to prevent Hg toxicity.38 The scenario where artisanal and small scale mining
334
leads to a high deposition flux of inorganic mercury to soil may therefore lead to both excessive
335
exposure of the local population to Hg (as MeHg), and deficiency of the local population in Se. 15
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We therefore propose that in the context of rice production in artisanal mining areas, Hg
337
contamination of the air is a significant threat to the Se nutrition of the mining communities. The
338
combined effect of elevated Hg and Hg-induced Se deficiency in rice may be leading to more
339
excessive exposure of the artisanal mining communities to Hg toxicity than is currently
340
recognized. The interactive effect of these two elements, especially the profound effect of Hg on
341
Se uptake into rice grain, should be assessed more fully in the context of public health. Studies on
342
the effect of Hg on the uptake and accumulation of Se in plants and the underlying mechanisms of
343
this effect, especially phytophysiological processes, should be considered in the future.
344 345
Acknowledgments
346
This research was financed by National Key Basic Research Program of China (973 Program
347
2013CB430004), Natural Science Foundation of China (41073098, 41203091, 41073062,
348
41173126, and 11105172), and also financed by the 135 project of IGCAS.
349 350 351
Supporting Information Available
352
Detailed information of sample analysis; detailed information of QA/AC; literature precedent for
353
applying PCA to extract hidden subsets from a dataset in order to detect possible sources;
354
explanation of the correlation between TGM and Se concentration in grain; one tables. This
355
information is available free of charge via the Internet athttp://pubs.acs.org/
356
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References
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mercury ore belt. Geol. Explor. Nonferr. Metal. 1995, 4 (1), 30-34 (in Chinese). 21. Wang, G. L.; Zhu, X. Q. A background survey on seleniun in soil of Guizhou Provience. Res. Environ. Sci. 2003, 16 (1), 23-26. 22. Zhu, Z. M.; Lu, L. N.; Liu, W. The element background of Chinese soil; China Environmental Science Press: Beijing, 1990 (in Chinese). 23. Lisk, D. J. Trace metals in soils, plants, and animals. Adv. Agron. 1972, 24, 267-325. 24. Zhang, H.; Feng, X. B.; Chan, H. M.; Larssen, T. New insights into traditional health risk assessments of mercury exposure: implications of selenium. Environ. Sci. Technol. 2014, 48 (2), 1206-1212. 25. Zhang, H.; Feng, X. B.; Jiang, C. X.; Li, Q. H.; Liu, Y.; Gu, C. H.; Shang, L. H.; Li, P.; Lin, Y.; Larssen, T. Understanding the paradox of selenium contamination in mercury mining areas: High soil content and low accumulation in rice. Environ. Pollut. 2014, 188 (0), 27-36. 26. Zhang, H.; Feng, X. B.; Zhu, J. M.; Sapkota, A.; Meng, B.; Yao, H.; Qin, H.; Larssen, T. Selenium in soil inhibits mercury uptake and translocation in rice (Oryza sativa L.). Environ. Sci. Technol. 2012, 46, 10040-10046. 27. Meng, B.; Feng, X. B.; Qiu, G. L.; Cai, Y.; Wang, D. Y.; Li, P.; Shang, L. H.; Sommar, J. Distribution Patterns of Inorganic Mercury and Methylmercury in Tissues of Rice (Oryza sativa L.) Plants and Possible Bioaccumulation Pathways. J. Agr. Food Chem. 2010, 58 (8), 4951-4958. 28. Qin, H. B.; Zhu, J. M.; Liang, L.; Wang, M. S.; Su, H. The bioavailability of selenium and risk assessment for human selenium poisoning in high-Se areas, China. Environ. Int. 2013, 52, 66-74. 29. Wold, S.; Esbensen, K.; Geladi, P. Principal component analysis. Chemometr. Intel. Lab. Syst. 1987, 2 (1), 37-52. 30. Jackson, J. E. A user's guide to principal components. Wiley Series in Probability and Statistics, John Wiley & Sons Inc., 2005. 31. Jolliffe, I. T. Principal component analysis (2nd edition), Springer Series in Statistics, Springer: New York, U. S., 2002.. 32. Shan, Y. S.; Tysklind, M.; Hao, F. H.; Ouyang, W.; Chen, S. Y.; Lin, C. Y. Identification of sources of heavy metals in agricultural soils using multivariate analysis and GIS. J. Soil. Sediment. 2013, 13 (4), 720-729. 33. Haygarth, P. M.; Cooke, A. I.; Jones, K. C.; Harrison, A. F.; Johnston, A. E. Long-term change in the biogeochemical cycling of atmospheric selenium-deposition to plants and soil. J. Geophys. Res. 1993, 98 (D9), 16769-16776. 34. Haygarth, P. M.; Harrison, A. F.; Jones, K. C. Plant seleniun from soil and the atmosphere. J. Environ. Qual. 1995, 24 (4), 768-771. 35. Liu, G. J.; Zhang, Y.; Qi, C.; Zheng, L. G.; Chen, Y. W.; Peng, Z. C. Comparative on causes and accumulation of selenium in the tree-rings ambient high-selenium coal combustion area from Yutangba, Hubei, China. Environ. Monit. Assess. 2007, 133 (1-3), 99-103. 36. Meng, B.; Feng, X. B.; Qiu, G. L.; Liang, P.; Li, P.; Chen, C. X.; Shang, L. H. The Process of Methylmercury Accumulation in Rice (Oryza sativa L.). Environ. Sci. Technol. 2011, 45 (7), 2711-2717. 37. Ralston, N. V. C.; Ralston, C. R.; Blackwell, J. L.; Raymond, L. J. Dietary and tissue selenium in relation to methylmercury toxicity. Neurotoxicology. 2008, 29 (5), 802-811. 38. Peterson, S. A.; Ralston, N. V. C.; Peck, D. V.; Van Sickle, J.; Robertson, J. D.; Spate, V. L.; 18
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Morris, J. S. How Might Selenium Moderate the Toxic Effects of Mercury in Stream Fish of the Western US? Environ. Sci. Technol. 2009, 43 (10), 3919-3925.
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Table 1 Concentration of total Se in tissues of rice plant as a function of the two sampling areas
448
(ng g-1)
449
Table 2 Bioaccumulation factors (BAF) of Se in tissues of the rice plant as a function of sampling
450
area. BAF is calculated as the Se concentration in the tissues of rice plant/Se concentration in soil.
451
Table 3 Rotated factor loadings and percent variance for the two principal components (PC) of Se
452
in rice tissues and soil for the artisanal area
453
Table 4 Rotated factor loadings and percent variance for the two principal components (PC) of Se
454
in rice tissues and soil for the abandon area
455
20
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Table 1 Tissues, ng g-1
Artisanal area
Abandoned area
Mean±Std.E
Range
Mean±Std.E
Range
Polished
40±6
17-130
160±64
13-650
Bran
99±10
42-180
680±290
52-2900
Husk
52±4
26-82
200±75
36-820
Grain
51±3
23-76
235±99
27-970
Root
220±19
70-340
520±160
80-1700
Stem
66±7
27-120
330±140
35-1600
Leaf
150±15
67-280
440±150
63-1500
Soil
990±92
370-1900
2200±660
540-8900
457 458
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Table 2 Tissues Grain Root Stem Leaf
Artisanal area
Abandoned area
0.05 0.22 0.07 0.15
0.11 0.24 0.15 0.2
460
22
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Table 3 461
462 463 464
Se
PC 1
PC 2
PC 3
Grain Stem Leaf Root Soil % of variance explained cumulative % of total variance
0.657 -0.410 0.922 0.127 -0.371 29
0.383 0.812 0.048 0.041 -0.791 29
0.442 0.390 0.036 0.936 0.262 26 84
Extraction method: principal component analysis. Rotation method: Varimax with Kaiser Normalization.
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466 467 468 469 470
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Table 4 Se
PC 1
PC 2
Grain Stem Leaf Root Soil % of variance explained cumulative % of total variance
0.921 0.940 0.747 0.722 0.325 58
0.375 0.339 0.655 0.664 0.943 40 98
Extraction method: principal component analysis. Rotation method: Varimax with Kaiser Normalization.
24
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Figure 1. The study area and location of the sampling sites (Area A is the artisanal area, Area B is
472
the abandoned area)
473
Figure 2. Total Se concentration in different tissues of rice plant collected from the two areas
474
(with Std. Error) (Area A is the artisanal area, Area B is the abandoned area)
475
Figure 3. Concentration of Se in the grain as a function of TGM for the two areas (Area A is the
476
artisanal area, Area B is the abandoned area)
477
Figure 4. The relative distribution of Se in the tissues of rice plants from the artisanal area (Area
478
A) and abandoned area (Area B)
479
25
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Figure 1.
481 482
26
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Figure 2.
1000
1000
800
800
600
700
200
-1
Total Se concerntation (ng g )
700
100
600
-1
900
900
Total Se concerntation (ng g )
483
Area A Area B
0
500
Polished
Bran
Husk
Tissues of grain
400 300 200 100 0 Grain
Stem
Leaf
Root
Tissues of rice plant
484 485
27
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Figure 3. Concentrations of Se in grain (ng/g)
486
Page 28 of 29
A
80
B
1000
R2=0.242, P=0.074
70
2
R =3E-05, P=0.921
800
60 600 50 400
40
200
30
0
20 0
100
200
300
400
500
600
700
20
TGM (ng/m3)
30
40
50
60
TGM (ng/m3)
487 488
28
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80
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Figure 4.
490 491
29
ACS Paragon Plus Environment
