Arsenic Bioavailability to Rice Is Elevated in Bangladeshi Paddy Soils

Oct 26, 2010 - (24) Li, R. Y.; Stroud, J. L.; Ma, J. F.; McGrath, S. P.; Zhao, F. J.. Mitigation of arsenic accumulation in rice with water manage- me...
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Environ. Sci. Technol. 2010, 44, 8515–8521

Arsenic Bioavailability to Rice Is Elevated in Bangladeshi Paddy Soils M. ASADUZZAMAN KHAN,† JACQUELINE L. STROUD,† YONG-GUAN ZHU,‡ STEVE P. MCGRATH,† A N D F A N G - J I E Z H A O * ,† Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, U.K., and Institute of Urban Environment, Chinese Academy of Science, Xiamen, 361021, China

Received June 9, 2010. Revised manuscript received August 23, 2010. Accepted October 14, 2010.

Some paddy soils in the Bengal delta are contaminated with arsenic (As) due to irrigation of As-laden groundwater, which may lead to yield losses and elevated As transfer to the food chain. Whether these soils have a higher As bioavailability than other soils containing either geogenic As or contaminated by mining activities was investigated in a pot experiment. Fourteen soils varying in the source and the degree (4-138 mg As kg-1) of As contamination were collected, 10 from Bangladeshi paddy fields (contaminated by irrigation water) and two each from China and the UK (geogenic or mining impacted), for comparison. Bangladeshi soils had higher percentages of the total As extractable by ammonium phosphate (specifically sorbed As) than other soils and also released more As into the porewater upon flooding. Porewater As concentrations increased with increasing soil As concentrations more steeply in Bangladeshi soils, with arsenite being the dominant As species. Rice growth and grain yield decreased markedly in Bangladeshi soils containing >13 mg As kg-1, but not in the other soils. Phosphate-extractable or porewater As was a better indicator of As bioavailability than total soil As. Rice straw As concentrationsincreasedwithincreasingsoilAsconcentrations; however, As phytotoxicity appeared to result in lower grain As concentrations. The relative proportions of inorganic As and dimethylarsinic acid (DMA) in grain varied among soils, and the percentage DMA was larger in greenhouse-grown plants than grain samples collected from the paddy fields of the same soil and the same rice cultivar, indicating a strong environmental influence on As species found in rice grain. This study shows that Bangladeshi paddy soils contaminated by irrigation had a higher As bioavailability than other soils, resulting in As phytotoxicity in rice and substantial yield losses.

About 70% of the water extracted from STW is used to irrigate rice during the dry (boro) season, adding substantial amounts of As to paddy fields (2, 3). This practice can lead to buildup of As in soil, which may exhibit a spatial pattern of As accumulation decreasing away from the irrigation inlet (4-6). Field surveys of Bangladeshi paddy soils show total As concentrations of up to 80 mg kg-1 (7). Severe losses in rice yield have been reported in field transects toward irrigation inlets due to As buildup and the resultant As toxicity to rice crops (8). Furthermore, irrigation with As-contaminated groundwater may lead to elevated As concentrations in rice grain and straw (7, 9, 10). In other regions of the world, soils may be contaminated with As due to mining activities or use of As-containing agrochemicals. Rice produced in miningimpacted areas in southern China was found to contain higher concentrations of As than in uncontaminated areas (11). Rice is the staple food for about half of the world’s population; in Bangladesh rice contributes up to approximately 80% of energy intake locally (12). Rice is more efficient at As accumulation than other cereals (13, 14) owing to the anaerobic conditions in the paddy soils and the inadvertent and efficient uptake of arsenite through the silicic acid pathway in rice (15, 16). For this reason, rice is a major source of inorganic As to the populations living on a rice diet (17-20). Unlike other terrestrial food crops, rice grain can contain considerable amounts of methylated As, especially dimethylarsinic acid (DMA) (20, 21). It is generally believed that inorganic As is more toxic than pentavalent methylated As species (21, 22). The relative proportions of inorganic As and DMA in rice grain vary widely depending on rice genotypes (23-25) and the conditions used to grow rice (15, 24, 26). However, whether rice methylates As in planta or acquires methylated As species from the environment, and how environmental conditions affect As speciation in rice grain remain unclear (27). The behavior of As in paddy soil and its accumulation by rice plants is of major concern. The impact of As accumulation in soil on yield and the transfer of As to the food chain depends on its bioavailability in soil. We hypothesize that the paddy soils in the Bengal delta contaminated by As in irrigation water have a higher bioavailability than soils either containing geogenic As or contaminated by other sources (e.g., mining activities), because irrigation water contains predominantly soluble inorganic As (28). Furthermore, the additions of As to these soils are recent events allowing insufficient time for As to age in soil, especially under anaerobic conditions in the paddy, which are conducive to As mobilization (15, 29, 30). This hypothesis was tested in the present study by comparing As mobilization and speciation in soil porewater, rice growth, and As uptake in 14 soils from Bangladesh, China, and the UK in a greenhouse experiment. In addition, we investigated As speciation in rice grain as influenced by soils and growing conditions (greenhouse vs field).

Introduction During the last 2-3 decades, Bangladesh and the neighboring West Bengal, India, have suffered from widespread arsenic (As) contamination in the drinking water extracted from shallow tube-wells (STW). Over half of the STW water samples in Bangladesh contained >10 µg As L-1, the current guideline value for drinking water set by the World Health Organization, with some reaching milligram per liter concentrations (1). * Corresponding author phone: 44 1582 763133; fax: 44 1582 469036; e-mail: [email protected]. † Rothamsted Research. ‡ Chinese Academy of Science. 10.1021/es101952f

 2010 American Chemical Society

Published on Web 10/26/2010

Materials and Methods Pot Experiment. Fourteen soils were used in this study (Supporting Information, Table S1), including 10 Bangladeshi paddy soils (labeled B1-B10) that have been contaminated with As to various degrees by irrigation with groundwater, two paddy soils from China (C1, C2) impacted by mining or geogenic As contamination, and two upland arable soils from the UK (U1, U2) that have elevated As concentrations due to geogenic reasons. The 10 Bangladeshi soils were collected from different areas near the inlet of irrigation water from STW, B1 from Noakhali district, B2 and B3 from Naraynganj, and B4-B10 from Faridpur district (Ganges Floodplain). VOL. 44, NO. 22, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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Selected soil properties, such as pH; texture; organic C%; CaCO3; total N; available P (Olsen P), phosphate-extractable As; and total Fe, Mn, As concentrations (by aqua-regia digestion), were determined following standard methods of soil analysis. The experiment was conducted inside a glasshouse (day/night temperatures 28/25 °C, light period 16 h per day with natural sunlight supplemented with sodium vapor lamps to maintain light intensity of >350 µmol m-2 s-1). A total of 42 pots (three pots per soil) were arranged randomly. A subsample of 500 g of soil (air-dried, 100 mg As kg-1). The concentration of available P varied widely with high levels being observed in U2 and in contaminated soils of Bangladesh (except B5). Small amounts of CaCO3 were present in all but three soils, and soil pH was circumneutral in most soils. The soils were rich in Fe (2.3-8.6%). Ammonium phosphate extracted between 1.5 and 11.4% of the total soil As. The extractability was higher in Bangladeshi soils (6.2-11.4%) compared with UK and Chinese soils (1.5-4.8%). Porewater As Concentration and Speciation. Porewater As is considered to be the pool of As that is most readily available for plant uptake. The concentration of As in porewater varied by approximately 3 orders of magnitude across the 14 soils from 0.01 to 13 mg L-1 (Figure 1a). For each soil the concentration was similar at the two sampling times (15 and 145 DAT); the only exception was U1, which had undetectable As in the porewater collected at 15 DAT. Porewater As concentrations generally increased with soil total As. However, the relationship between these two variables were different between the Bangladeshi soils and the other four soils; more As was mobilized into porewater in the Bangladeshi soils than in the other soils at the same total soil As concentration (Figure 1b). Arsenic speciation in the porewaters was dominated by As(III), which accounted for 46-99% (mean 88%) of the total As (Figure 1c). DMA was detected in the porewater of U1 soil at low concentrations, while monomethylarsonic acid (MMA) was not detectable. Rice Yields. Toxicity symptoms (stunted growth, brown spots, and scorching on leaves) were observed in the rice plants grown in the Bangladeshi soils containing >60 mg kg-1 total As. These soils (B2, B3, B5, B6, B7, B8) also produced low biomass yields of straw and grain, with grain being much more affected than straw (Supporting Information, Table S2). The soil B2 was the worst case, producing no grain. The reduction in grain yield was associated with decreases in the number of productive tillers, the number of filled grains per panicle, and 1000-grain weight (Supporting Information, Table S2). The two Chinese soils (C1, C2) and the UK soil U2 also had high concentrations of total As, but there were no toxicity symptoms in the rice plants, and grain yields were much higher than those in the contaminated Bangladeshi soils. Figure 2 plots the relationships between grain yield and soil total As, phosphate-extractable As, or porewater As; similar patterns were obtained when the straw yield data were used (not shown). The relationship between grain yield and soil total As was different between the Bangladeshi soils and the other soils; the decrease in grain yield with increasing soil As was much steeper in the former than the latter. However, when phosphate-extractable As or soil porewater As was used, the relationship became uniform for all soils and could be described satisfactorily by a single regression equation (exponential decay curve and log-linear, respectively). Arsenic Concentrations in Plants. The concentration of As in straw (1.4-17.2 µg g-1) was 5-62-fold higher than that

FIGURE 1. Arsenic concentrations in soil porewater (a), the relationship between porewater As concentration and soil total As (b), and As speciation in soil porewater (c). Porewater data in parts b and c are means of the two samplings. in grain (0.24-1.09 µg g-1). The grain and straw As concentrations varied significantly (p < 0.001) among different soils. Straw As concentrations increased with increasing soil total As concentrations, although the pattern was different between the Bangladeshi and other soils, with the former having higher straw As concentrations than the latter (Figure 3a). Similar to the relationship between yield and soil As, use of both phosphate-extractable As and soil porewater As appeared to unify the relationship with straw As concentration in all soils (Figure 3c,e). In contrast, grain As concentration did not show a consistent relationship with soil total As, phosphateextractable As, or soil porewater As (Figure 3b,d,f). In the Bangladeshi soils, grain As concentration doubled when soil total As increased from the lowest (4 mg kg-1) to a moderate level (13 mg kg-1). In the other Bangladeshi soils containing >60 mg kg-1 As, in which plants suffered from As toxicity, grain As concentration was similar to or even lower than that obtained with the lowest soil As concentration. The lowest concentrations of grain As were obtained in the two UK soils, while the two Chinese soils (total As 60-80 mg kg-1) produced grain As concentrations similar to those in the Bangladeshi

FIGURE 2. The relationships between grain yield of rice and soil total As (a), phosphate-extractable As (b), or porewater As concentration (c). high-As soils. Unlike for straw As, use of soil phosphateextractable As or porewater As did not improve the relationship with grain As concentration (Figure 3d,f). Shoot As concentrations of plants at the stem extension stage (45 DAT; Supporting Information, Table S3) showed a similar pattern to that of straw As at maturity. Multiple regression was used to identify soil porewater variables (including pH, Eh, and the concentrations of As, Si, P, S, Fe, Mn, Ca, Mg, and K; Supporting Information, Table S3) that may influence the As concentration in straw. Three variables were found to have a significant influence: the concentrations of As (p < 0.001) and Si (p ) 0.004) and the pH (p < 0.001) in porewater, giving rise to the following regression model that explained 81% of the variance in straw As concentration: Asstraw ) -27.1 + 1.1Aspw - 0.6Sipw + 5.4pHpw n ) 42, R2 ) 0.81, p < 0.001

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FIGURE 3. The relationships between the As concentrations in straw (a, c, e) or grain (b, d, f) As and soil total As (a, b), phosphate-extractable As (c, d), or porewater As concentration (e, f). Note the positive coefficients for porewater As (Aspw) and pH (pHpw) and the negative coefficient for porewater Si (Sipw), indicating their contrasting influences. Arsenic Speciation in Grain. Inorganic As [As(III) and As(V)] and DMA were detected in the grain samples. Inorganic As and DMA accounted for 33-77% and 23-67%, respectively, in the samples from the pot experiment (Figure 4a). Although As speciation differed between grains from different soils, overall there was no clear difference between Bangladeshi and other soils. In 2009, two rice grain samples were collected from field sites (Faridpur and Narayanganj) in Bangladesh, where soils were also collected for the pot experiment (B3 and B5, respectively). The same cultivar was grown in both the pot experiment and in the field sites, so a direct comparison was possible. The two field grain samples contained smaller concentrations of total As (0.13-0.22 µg g-1) than the corresponding samples grown in the pot experiment (0.41-0.50 µg g-1) but higher percentages of inorganic As than the pot experiment samples (Figure 4a). The percentages of inorganic As in the field samples (78-87%) were similar to those reported in other studies of field-grown rice of Bangladesh (25, 36). 8518

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The relationships between grain As species and total As concentration are shown in Figure 4b,c. The concentrations of both inorganic As and DMA increased linearly with grain total As, but the slope for DMA was 2.7 times that for inorganic As (Figure 4b). Therefore, the percent inorganic As decreased, while that of DMA increased, with total grain As (Figure 4c). Initially inorganic As was the dominant species, but above approximately 0.4 µg g-1 total As, DMA became the dominant species of As.

Discussion The soils used in the present study differ in the source and the degree of As contamination; those from Bangladesh are contaminated by irrigation of As-laden groundwater, while the Chinese and UK soils either are contaminated by mining activities or contain geogenic As. It is clear from the present study that the Bangladeshi paddy soils had a higher As bioavailability than the other soils from China and UK. Similar to previous reports (8, 15, 24, 29), As(III) was mobilized into the soil solutions upon flooding of the soils, and this mobilization was greater in the Bangladeshi soils (up to 13 mg L-1 in the most contaminated soil) than in the other four

FIGURE 4. Arsenic speciation in rice grain from greenhouse experiment and from paddy fields in Narayanganj and Faridpur, Bangladesh (a); the relationships between the concentration of total grain As and inorganic As or DMA (b); and the relationships between the percentages of inorganic As or DMA and total grain As concentration (c). soils (13 mg As kg-1 due to As phytotoxicity, with the effect being severe in the soils with >60 mg As kg-1 (Figure 2a). These soils were collected from paddy fields near the shallow tubewells from which As-contaminated groundwater was extracted for irrigation. Similarly, Panaullah et al. (8) showed that grain yield of rice decreased linearly from 7-9 to 2-3 t ha-1 with increasing soil As concentration from 10 to 70 mg kg-1 along a soil transect toward the irrigation inlet in a paddy field in Faridpur, Bangladesh. In comparison, there were no signs of As toxicity when rice was grown in the four Chinese

and UK soils containing As up to 79 mg kg-1, and grain yield was decreased only slightly at the highest As concentration (Figure 2a). The higher As bioavailability in the Bangladeshi paddy soils is understandable considering that the source of As contamination was irrigation water, from which As is likely to deposit into the soil by the formation and settling of Asbearing Fe oxides and by adsorption to soil minerals (4, 28), which could become labile especially under anaerobic conditions. In contrast, geogenic or mining-derived As may be present largely in the insoluble and nonlabile forms. It is well-known that total As concentration in soil does not reflect its bioavailability, and this is also demonstrated by the present study (Figures 2a and 3a). Ammonium phosphate-extractable As or porewater As appears to offer a much better indicator of bioavailability, as both unified the relationships of plant responses across different soils (Figures 2b,c and 3c,e). The extraction with ammonium phosphate is simple to perform and may be used to assess the pool of potentially available As in paddy soils. Apart from the relationship with As concentration in soil porewater, the As concentration in straw was found to increase with pH and to decrease with Si concentration. Increasing pH may facilitate the desorption of As from the sorption sites in soil and on the iron plaque of the root surface. The effect of Si on As accumulation in rice has been shown before (24, 37) and is consistent with arsenite sharing with the Si uptake pathway in rice (16). The concentrations of As in rice straw and grain in this study were within the range reported previously from both greenhouse experiments (6, 15, 23, 24, 38) and field surveys or experiments (8, 13, 25, 39). As has been discussed before, these concentrations are high enough to present a potential risk to humans and to cattle consuming straw (20, 40). While the concentration of As in rice straw increased with increasing soil As, grain As did not (Figure 3). This observation agrees with the field study of Panullah et al. (8), who found that grain As either decreased or did not vary significantly with increasing soil As concentration in field transects. On the basis of field survey samples, Lu et al. (5) showed that the grain As concentrations increased with soil total As concentrations within the baseline range and approached a saturation plateau when soil As exceeded about 10 mg kg-1. A likely explanation is that As phytotoxicity, which occurred in some of the Bangladesh soils in our experiment, may have inhibited As translocation from the shoot tissues to grain. For this reason, it was not possible to predict grain As concentration with soil measurements in the present study. Speciation of As in grain has important implications for the potential health risk because inorganic As is more toxic than the pentavalent methylated As (20, 21). Inorganic As and DMA are the major As species found in rice grain; the relative proportions of these two As species vary widely among rice grain collected from different regions of the world (20, 21). In our study, inorganic As and DMA each accounted for approximately one- to two-thirds of the total As in the grain samples produced from the greenhouse experiment. Interestingly, samples from the two Bangladeshi fields of the same rice cultivar had considerably smaller percentages of DMA than those grown in the same soils under the greenhouse conditions (Figure 4a). One explanation is that the field grain samples contained smaller concentrations of total As, and low As grain tended to have a low percentage of DMA and a high percentage of inorganic As (Figure 4c). In fact, the percentage of DMA increased, whereas the percentage of inorganic As decreased, with total As concentration (Figure 4c). These contrasting patterns have also been observed before (15, 25, 41). The relationships between As species and total As (Figure 4b) reveal that the concentration of DMA started from a very low level but rose much more steeply with increasing total As than inorganic As. It has not been VOL. 44, NO. 22, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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resolved whether DMA in rice is taken up from the soil or synthesized from inorganic As in planta (27). It is known, however, that DMA is much more efficiently translocated from rice roots to shoots (42) and from the shoot tissues to grain (43) than inorganic As. Methylated As species were not detectable in the soil porewater samples except in one UK soil (Figure 1c). However, it is not known if methylated As was produced in the rhizosphere, which was not specifically sampled in the soil porewater. Also, there is a possibility that methylated As species in soil porewaters could be undetectable by the HPLC method used due to a masking effect of sulfide produced from anaerobic reactions in the flooded soils. If DMA is synthesized in planta, then this synthesis appears to be enhanced by increased As burden in rice plants. If, on the other hand, DMA is derived from the soil, then environmental conditions that favor As accumulation in rice may also be conducive to As methylation in the soil. Indeed, anaerobic soil conditions were found to increase both the total As concentration and the percentage of DMA in rice grain (15, 24, 26). Regardless of the origin of DMA in rice, this study showed that environmental conditions (i.e., different soils and greenhouse vs field) have a large influence on As speciation in rice grain of a single cultivar. In conclusion, Bangladeshi paddy soils contaminated by As in irrigation water had a higher As bioavailability than other soils contaminated by mining or geogenic causes. Accumulation of As in Bangladeshi paddy soils was found to result in severe As phytotoxicity and yield losses in rice, potentially threatening agricultural sustainability and food security. Ammonium phosphate extractable As or porewater As gave a better prediction of straw As concentration and growth reduction due to As toxicity than total soil As. Arsenic speciation in rice grain differed between soils and, for the same soils, between greenhouse and field samples, indicating a strong environmental influence.

Acknowledgments The authors gratefully acknowledge the Rothamsted International Fellowship awarded to Md. Asaduzzaman Khan. Rothamsted Research is an institute of the UK Biotechnology and Biological Sciences Research Council.

Supporting Information Available Information on the soil properties, porewater measurements, and rice yields and yield components is available. This material is available free of charge via the Internet at http:// pubs.acs.org.

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