Optimal Soil Eh, pH, and Water Management for Simultaneously

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Optimal soil Eh, pH, and water management for simultaneously minimizing arsenic and cadmium concentrations in rice grains Toshimitsu Honma, Hirotomo Ohba, Ayako Kaneko-Kadokura, Tomoyuki Makino, Ken Nakamura, and Hidetaka Katou Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.5b05424 • Publication Date (Web): 21 Mar 2016 Downloaded from http://pubs.acs.org on March 23, 2016

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Environmental Science & Technology

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Optimal soil Eh, pH, and water management for

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simultaneously minimizing arsenic and cadmium

3

concentrations in rice grains

4

Toshimitsu Honma,*,† Hirotomo Ohba,† Ayako Kaneko-Kadokura,†,‡ Tomoyuki Makino,§

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Ken Nakamura,§ and Hidetaka Katou§

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†

Niigata Agricultural Research Institute, Nagaoka, Niigata 940-0826, Japan

7

‡

Ojiya Branch, Nagaoka Agriculture Extension Center, Ojiya, Niigata 947-0028, Japan

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§

National Institute for Agro-Environmental Sciences, Tsukuba, Ibaraki 305-8604, Japan

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Abstract: Arsenic (As) and cadmium (Cd) concentrations in rice grains are a human health

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concern. We conducted field experiments to investigate optimal conditions of Eh and pH in soil

11

for simultaneously decreasing As and Cd accumulation in rice. Water managements in the

12

experiments, which included continuous flooding, and intermittent irrigation with different

13

intervals after midseason drainage, exerted striking effects on the dissolved As and Cd

14

concentrations in soil through changes in Eh, pH, and dissolved Fe(II) concentrations in the soil.

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Intermittent irrigation with three-day flooding and five-day drainage was found to be effective

16

for simultaneously decreasing the accumulation of As and Cd in grain. The grain As and Cd

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concentrations were, respectively, linearly related to the average dissolved As and Cd

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concentrations during the 3 weeks after heading. We propose a new indicator for expressing the

ACS Paragon Plus Environment

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degree to which a decrease in the dissolved As or Cd concentration is compromised by the

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increase in the other. For minimizing the trade-off relationship between As and Cd in rice grains

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in the field investigated, water management strategies should target the realization of optimal soil

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Eh of –73 mV and pH of 6.2 during the 3 weeks after heading.

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Introduction

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Rice (Oryza sativa L.), a staple food for half of the world’s human population, is a major

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source of arsenic (As) and cadmium (Cd), particularly in Asia and other countries.1,2 The

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International Agency for Research on Cancer3 has identified inorganic arsenic, i.e., arsenite

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(As(III)) and arsenate (As(V)), as human carcinogens. The As concentration in rice grains is

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approximately 10 times higher than those in other cereals such as wheat and barley,4 as a result

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of anaerobic conditions in rice-growing soils. Since the predominant As species in rice grain is

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inorganic As, minimizing the intake of As from rice in the diet is an important health issue.

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Recently, the Codex Alimentarius Commission5 adopted a maximum level of inorganic As of 0.2

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mg kg–1 in polished rice grain. According to a national survey6, the average inorganic As

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concentration in polished rice grain for major rice cultivars produced in Japan is 0.12 mg kg–1,

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with a maximum value of 0.26 mg kg–1. Moreover, 2.2% of grain samples from supposedly

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uncontaminated paddy fields have been shown to contain over 0.2 mg kg–1 of inorganic As in

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polished rice grain. Another survey7 has estimated that rice is the largest contributor to the total

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dietary intake of inorganic As in China, representing 60% of inorganic As intake.

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Arsenic may be present in soil in various chemical forms, including inorganic As and

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methylated As species such as monomethylarsonic acid (MMA) and dimethylarsinic acid

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(DMA). Inorganic As(III) is the predominant form of As present in soil and taken up by plants,

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and its transport to xylem is mediated by silicate transporters.8,9 Small quantities of methylated


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As species have also been found in some soils, most likely from either microbial methylation or

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prior application of As-based pesticides/herbicides.10 The availability of As in soil depends on

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Eh and pH.11,12 In paddy fields, flooding and drainage cycles have a major impact on As

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dynamics in soil solutions and on As bioavailability to rice plants. 13–15 When paddy soil is under

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aerobic conditions as a result of field drainage, As is less mobile. This is because As(V), the

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predominant inorganic As species under oxidizing conditions, is strongly sorbed to mineral soil

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components such as Fe and Al (hydr)oxides16. When anaerobic conditions develop in flooded

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soils, As is released from the solid phase into the aqueous solution phase through reductive

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dissolution of Fe (hydr)oxides and reduction of As from As(V) to As(III), which has increased

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solubility compared with As(V).13 Release of As from Fe (hydr)oxides is promoted upon

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decrease of Eh below –100 mV,17–19 and Eh of +100 mV is considered to be the point below

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which reduction of As(V) to As(III) occurs at neutral pH.20 Solubilized As is vigorously taken up

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by rice plants and accumulated in grains under flooded conditions.

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Cadmium contamination in rice grains also causes serious damage to human health, such as

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kidney damage, osteoporosis, and cancer.21 For example, Itai-itai disease was identified in the

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1950s in Japan among people eating rice grown in paddy fields polluted with high levels of Cd

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from current or abandoned mines.22 A health-based guidance value for Cd of 25 µg kg–1

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bodyweight per month was established by the Joint FAO/WHO Expert Committee on Food

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Additives,23 and a maximum concentration of 0.4 mg kg–1 for Cd in polished rice grain has been

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adopted by the Codex Alimentarius Commission.24 In Japan, a survey25 revealed that

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approximately 40% of Cd intake from food was from rice consumption and that 0.3% of rice

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grains contain Cd over the Codex maximum level.


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Cadmium solubility and bioavailability in soil mainly depend on soil redox potential (Eh) and

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pH. The predominant form of Cd taken up by rice plants is Cd2+, and the uptake is suppressed

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under reduced conditions.26,27 Based on thermodynamic considerations, Ito and Iimura28 ascribed

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the decrease in the plant-available Cd to sulfide formation, and the presence of CdS in a reduced

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paddy soil contaminated with Cd has been confirmed by the X-ray absorption spectroscopy.29

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Drainage of paddy fields results in aerobic conditions that enhance the availability of Cd for

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plant uptake through oxidation of CdS to Cd2+ and SO42–, which has a much higher solubility

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than CdS formed under flooding conditions.30 Soil pH also affects Cd solubility through the

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influence of pH-dependent surface charge on the affinity of Cd for sorption sites.31 Increasing

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soil pH from 6.1 to 6.9 has been reported to decrease Cd concentrations in rice grains in both

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upland and flooded cultivations.32

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It has thus been established that water management greatly impacts the bioavailability of As

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and Cd in paddy soils through changes in soil Eh. Widely adopted water management in Japan

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follows a sequence of flooding, mid-season drainage, intermittent irrigation around the heading

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stage, and drainage before harvest.33 In paddy fields contaminated with Cd, flooding for a total of

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six weeks before and after heading has been recommended for decreasing the Cd concentration

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in rice grain.34 The anaerobic conditions, however, raise As solubility. Arao et al.14 investigated

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the effects of water managements on As and Cd accumulation in rice grains, and found a trade-

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off relationship between As and Cd bioavailability. Maintaining aerobic conditions after the

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flowering stage significantly decreases As accumulation in rice straw and grains compared with

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rice grown under flooded conditions.35 However, aerobic conditions during the flowering stage

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lead to accumulation of dissolved Cd in soil. Yamane17 reported that decreasing Cd and As

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uptake could be achieved by maintaining aerobic conditions in the paddy soil before heading and


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switching to anaerobic conditions after heading. Arao et al.14 found that the most sensitive period

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for As and Cd accumulation was around the heading stage, particularly 3 weeks after heading.

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Hu et al.36 stressed the importance of water management in decreasing As and Cd bioavailability

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and uptake by rice, but no information was provided as to the Eh and pH values for decreasing

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As and Cd simultaneously. Optimization of the trade-off relationship between As and Cd in soil

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solutions and in rice grain is needed for paddy fields at risk of exceeding the Codex maximum

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levels of As and Cd. To our knowledge, however, the effects of irrigation intervals under field

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conditions on As and Cd uptake by rice and As speciation in rice grain have not been

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investigated.

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The main objectives of the present study were (i) to investigate the effects of different water

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management strategies on the dissolved As and Cd concentrations in soil, As and Cd uptake by

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rice, and As speciation in rice grains; and (ii) to identify optimal soil Eh and pH for minimizing

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the trade-off relationship between As and Cd. Rice grain yields and quality under different water

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managements were also investigated.

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Materials and Methods

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Experimental Field

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Field experiments were conducted in 2013 in a paddy field developed on an alluvial plain in

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central Japan. The soil was classified as a Typic Hydraquent by US Soil Taxonomy.37 The

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topsoil had total carbon and nitrogen contents of 16.2 g kg–1 and 1.53 g kg–1, respectively, 1 M

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HCl-extractable As concentration of 2.49 mg kg–1, and 0.1 M HCl-extractable Cd concentration

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of 0.84 mg kg–1, with a textural composition of 52% sand (0.02–2 mm), 30% silt (2 µm–0.02

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mm), and 18% clay (< 2 µm). The soil pH measured at a soil:water ratio of 1:2.5 (w/w) was 5.8.


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Field Experiments

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Seedlings of rice (Oryza sativa L. cv. Koshihikari) were transplanted on May 13. The rice

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plants were grown under flooded conditions for 36 days, followed by a 14 days of midseason

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drainage until July 2. Thereafter, five different water managements were practiced for a total of 6

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weeks, 3 weeks before heading and 3 weeks after heading. The water managements included (1)

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Flooded; (2) Int-F3D1, in which intermittent irrigation was repeated every 4 days, with 3-day

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flooding followed by 1-day drainage; (3) Int-F3D3, in which intermittent irrigation was repeated

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every 6 days, with 3-day flooding followed by 3-day drainage; (4) Int-F3D5, in which

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intermittent irrigation was repeated every 8 days with 3-day flooding followed by 5-day

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drainage; and (5) Rainfed, in which irrigation was not practiced. After the period with different

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water managements was over on August 26, intermittent irrigation with indeterminate intervals

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was conducted, with the final drainage for harvest on September 5. Each treatment had three

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replicated plots in the field, with each plot having a size of 6 m × 12 m. The rice was harvested

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on September 19.

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Plant and Soil Analysis

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Soil samples were collected on April 18 from the topsoil layer (0–15 cm depth) of the

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experimental plots for determination of chemical properties. For the rice plant analysis, four rice

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hills were sampled from each plot at the maximum tiller number stage (July 14), heading stage

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(August 7), ripening stage (September 6), and maturing stage (September 17). The rice grains

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removed from the shoots were air-dried, and those remaining on the 1.85 mm-sieve were used

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for analysis.

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Soil redox potential (Eh) was measured in duplicate with an Eh meter and platinum electrodes

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installed at 15 cm depth in each plot, and soil pH was measured using a glass electrode. Soil


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solutions were sampled at the same depth from mid-June to early September at intervals of 1–2

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weeks for determination of dissolved As, Cd, and Fe(II) concentrations. Dissolved Fe(II) was

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determined colorimetrically from the absorbance due to the Fe(II) 2,2′-bipyridyl complex.38

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Total As and Cd concentrations in the soil solutions were determined by flow injection (FI)-

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inductively coupled plasma mass spectroscopy (ICP-MS) according to Baba et al.39 with minor

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modifications.

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As(III), As(V), MMA(V), and DMA(V) in the rice grains were determined by ICP-MS

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according to the methods of Nishimura et al.40 and Baba et al.39 with minor modifications, after

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digestion with 0.15 M HNO3 and separation by high-performance liquid chromatography. Total

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As and Cd concentrations in rice samples and shoot samples were determined by FI-ICP-MS

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after digestion with HNO3 and H2SO4, and with HNO3–H2SO4 and HClO4, respectively. Grain

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qualities, such as the percentages of perfect grains and immature grains, were determined with a

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grain discriminator. Detailed procedures of the plant and soil analysis are given in the Supporting

145

Information.

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Statistical analysis

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Statistical analysis was performed using Statcel 2 software.41 Multiple comparisons between

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treatments were made by Tukey-Kramer test.

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Results

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Soil Eh, pH, and Dissolved As, Cd, and Fe(II) in Soil Solution

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Soil Eh, pH, and dissolved As, Cd, and Fe(II) concentrations were strongly affected by water

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management practices (Figure 1). Soil Eh, which ranged from –200 to –150 mV during the

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flooded period after transplanting, drastically rose upon midseason drainage. Different water


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managements during pre-heading 3 weeks and post-heading 3 weeks caused different responses

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of soil Eh. Soil Eh was kept low, around –200 to –150 mV, in the Flooded and Int-F3D1 plots,

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whereas the Eh fluctuated between –150 and 0 mV in the Int-F3D3 and Int-F3D5 plots. Even

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higher soil Eh was observed in the Rainfed plot throughout this period (Figure 1A). Soil pH

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decreased during midseason drainage period and then increased until the heading stage in all

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plots. After the heading stage, soil pH in the Flooded, Int-F3D1, and Int-F3D3 plots was

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maintained at pH 6.3–6.5, whereas in the Int-F3D5 and Rainfed plots, soil pH decreased from pH

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6.4 at the heading stage to 5.7 at harvest (Figure 1B).

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Midseason drainage resulted in an exhaustive decrease of dissolved Fe(II), which had

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increased during the flooding period, to a negligible level. During the pre-heading 3 weeks and

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post-heading 3 weeks, the dissolved Fe(II) in the Flooded and Int-F3D1 plots increased linearly

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with time. In the Int-F3D3 and Int-F3D5 plots, the increases in the dissolved Fe(II) before the

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heading stage were followed by the decreases after the heading stage. Dissolved Fe(II)

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concentration in the Rainfed plot remained much lower than in the other plots (Figure 1C).


8


300

(A) Soil Eh (mV)

200 100

Flooded Int-F3D1 Int-F3D3 Int-F3D5 Rainfed

0

-100 -200

200

Total dissolved As (µg L-1)

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-300

(D)

150

100

50

0 5/31 6/15 6/30 7/15 7/30 8/14 8/29 9/13

5/31 6/15 6/30 7/15 7/30 8/14 8/29 9/13

7.0

1.2

(B)

(E)

Dissolved Cd (µg L-1)

Soil pH

1.0 6.5

6.0

5.5

0.6 0.4 0.2 0.0

5/31 6/15 6/30 7/15 7/30 8/14 8/29 9/13 250

Dissolved Fe(II) (mg L-1)

0.8

(C)

5/31 6/15 6/30 7/15 7/30 8/14 8/29 9/13

Midseason drainage Water management period

200 150 100 50 0

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5/31 6/15 6/30 7/15 7/30 8/14 8/29 9/13

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Figure 1. Changes in (A) soil Eh, (B) soil pH, (C) dissolved Fe(II), (D) dissolved As and (E)

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dissolved Cd concentrations among different water management plots. The plots were flooded,

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intermittently irrigated with different irrigation intervals, or rainfed for pre-heading 3 weeks and

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post-heading 3 weeks.

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Dissolved As concentration showed changes similar to those in the dissolved Fe(II)

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concentration. Midseason drainage caused a dramatic decrease in the dissolved As followed by a

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steady increase with time in the Flooded and Int-F3D1 plots. In the Int-F3D3 plot, similar

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increase in the dissolved As until heading was followed by a decrease thereafter. Dissolved As in

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the Int-F3D5 plot also showed an increase until heading, but the increase was slower and the


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concentration after heading was very low. In the Rainfed plot, the dissolved As was the lowest

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among all plots during the water management period (Figure 1D). Dissolved Cd concentration

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increased remarkably upon midseason drainage and then showed rapid decreases following re-

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irrigation. During the water management period, the dissolved Cd concentration remained low in

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the Flooded, Int-F3D1, and Int-F3D3 plots, whereas in the Int-F3D5 and Rainfed plots, temporal

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increases in the dissolved Cd were observed (Figure 1E).

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Relationships among soil Eh, pH, and dissolved As, Cd, and Fe(II) concentrations Dissolved As and Cd concentrations during the growth period ranged from 0 to 185 µg L–1 and

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0 to 1.1 µg L–1, respectively. The relationships between the dissolved As and Cd concentrations

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are shown in Figure 2. Many of the solution samples had a combination of high As and low Cd

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concentrations or low As and high Cd concentrations. Notably, however, some solutions had a

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combination of low As and low Cd concentrations. Total dissolved As (µg L-1)

185

200


150 100 50 0 0.0

190 191

0.2

0.4 0.6 0.8 1.0 Dissolved Cd (µg L-1)

1.2

Figure 2. Relationship between total dissolved As and Cd concentrations in soil solution.

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Figure 3 shows the relations of total dissolved As and Cd concentrations to soil Eh, pH and

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dissolved Fe(II) concentrations. The total dissolved As decreased sharply with the increase in

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soil Eh, and when soil Eh was above –100 mV, only low concentrations were observed, with an


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dissolved Fe(II) and Eh; the dissolved Fe(II) concentration quickly decreased with the increase in

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soil Eh, and the concentrations were low when the Eh was above 0 mV (Figure S1 in the

198

Supporting Information). A distinct rise in the dissolved As was observed with the increase in

199

soil pH, particularly when the pH was above 6.3 (Figure 3(B)). Similar dependences on Eh

200

resulted in a positive correlation between the dissolved As and Fe(II) concentrations (Figure

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3(C)). In contrast, the dissolved Cd concentration increased with soil Eh and was negligible at Eh

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below –150 mV (Figure 3(D)). The dissolved Cd was appreciable only when the soil pH was low

203

and was negligible when the pH was above 6.3 (Figure 3(E)). The relationship between the

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dissolved Cd and Fe(II) concentrations (Figure 3(F)) was similar to that found between the

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dissolved Cd and As. The dissolved Cd concentration was very low when the dissolved Fe(II)

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concentration was above 50 mg L–1.

[As] = 5.84exp(-0.0145 Eh)

150


100 50 0

200

100 50

[Cd] =

2.00×10-6(Eh)2 + 0.2199

0.8 0.6 0.4 0.2

+ 0.0015 Eh

5.8

6.0 6.2 Soil pH

-300 -200 -100 0 100 200 300 Soil Eh (mV)

[As] = 0.0024[Fe(II)]2 + 0.3125 [Fe(II)] + 3.5886

150 100 50

0

6.6 1.2

(E) [Cd] =

1.0

6.4

5.34×1011exp(-4.8

0.8 0.6 0.4 0.2

pH)

50 100 150 Dissolved Fe(II) (mg L-1)

200

(F)

1.0

[Cd] = 0.35 [Fe(II)]-0.518

0.8 0.6 0.4 0.2 0.0

0.0

0.0

207

5.6 1.2

(D)

(C)

0

0



1.0

[As]= 3.56×10-12exp(4.72 pH)

150

-300 -200 -100 0 100 200 300 Soil Eh (mV) 1.2

200

(B)


(A)

DissolvedCd (µg L-1)

200


average (± SD) of 7.7 (± 7.5) µg L–1 (Figure 3(A)). A similar relationship was found between


195

5.6

5.8

6.0 6.2 Soil pH

6.4

6.6

0

50 100 150 Dissolved Fe(II) (mg L-1)

200

208

Figure 3. Relationships between the total dissolved As concentration and (A) soil Eh, (B) soil

209

pH, and (C) dissolved Fe(II) concentration (upper panels), and between the dissolved Cd


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concentration and (D) soil Eh, (E) soil pH, and (F) dissolved Fe(II) concentration (lower panels)

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in different water management plots.

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As and Cd concentrations in shoots and rice grains

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The As and Cd concentrations in shoots among the different water managements are compared

214

in Figure 4. The shoot As concentrations, which did not differ significantly among the plots 3

215

weeks before heading (July 14), rapidly increased in the Flooded, Int-F3D1, and Int-F3D3 plots.

216

Four weeks after heading (September 6), the shoot As concentrations in the Flooded and Int-

217

F3D1 plots were significantly higher than those in the more aerobic Int-F3D5 and Rainfed plots.

218

Differences in the shoot Cd concentrations were insignificant until heading among the plots. Low

219

or decreasing Cd concentrations were observed in the Flooded, Int-F3D1, and Int-F3D3 plots

220

until harvest, whereas a rapid increase in the Cd concentration was observed in the Int-F3D5 and

221

Rainfed plots after heading. 20

Int-F3D3

A

Int-F3D5

A

Rainfed

10

A AA

5

a

aaa

bc AB B

a

c

a

Rainfed B

0.4

a A

b b

b

b

AAA

b

A bbb

CC

C

0.0 7/14

222

Int-F3D5

0.6

0.2

0

Int-F3D3

0.8

BB

A

Int-F3D1

A ab

Cd (mg kg-1)

As (mg kg-1)

1.0

a

(B)

Flooded

a

Int-F3D1

15

1.2

(A)

Flooded

8/6

9/6

9/17

7/14

8/6

9/6

9/17

223

Figure 4. Comparison of (A) As and (B) Cd concentrations in shoots among different water

224

management plots during the growth period. Multiple comparisons between different plots were

225

made by Tukey-Kramer test (P < 0.05). Values with the same letters were not significantly

226

different.


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Figure 5 shows the As and Cd concentrations and As speciation in unpolished rice grains. As

228

and Cd concentrations in grains were strongly affected by the water management. The total As,

229

As(III), As(V), and DMA were in the order of Flooded ≈ Int-F3D1 > Int-F3D3 > Int-F3D5 >

230

Rainfed, with the concentrations in the Flooded plot 2.9–10.1 times as high as those in the

231

Rainfed plot. The predominant As species was inorganic As, particularly As(III). The inorganic

232

As / total As ratio was lower in the Flooded plot because of the increase in DMA and MMA

233

concentrations. The Cd concentrations in grains were higher in the aerobic plots, and were in the

234

order of Rainfed > Int-F3D5 > Int-F3D3 > Int-F3D1 > Flooded, with the concentration in the

235

Rainfed plot 18.5 times higher than that in the Flooded plot. Details of the results of statistical

236

analyses are given in Table S1 in the Supporting Information. As and Cd in rice grain (mg kg-1)

0.7 Cd Unrecovered As MMA DMA As(V) As(III)

0.6 0.5 0.4 0.3 0.2 0.1 0

237

Flood

Int-F3D1 Int-F3D3 Int-F3D5 Rainfed

238

Figure 5. Effects of different water managements on As and Cd concentrations and As

239

speciation in rice grains. DMA, dimethylarsinic acid; MMA, monomethylarsonic acid.

240

Growth of rice plant, grain yield, and grain quality

241

Influences of water management strategies on the growth of rice plants and grain yield were

242

limited as compared with those on As and Cd concentrations (Table S2 in the Supporting

243

Information). Except for the Rainfed plot, neither the unpolished rice yield nor the growth of rice

244

plants, such as measured by the culm length and the straw yield, was statistically different among


13


Page 14 of 27

the plots. Water managements did not affect the grain quality either; there were no significant

246

differences among the plots in the percentages of perfect grains or immature grains (Table S3 in

247

the Supporting Information). These results show that the As and Cd concentrations in rice grains

248

may be reduced by appropriate water managements without affecting the growth of rice plants

249

and grain quality. Rice grain As (mg kg-1)

245

(A)

0.8

T-As iAs

y = 0.0052 x + 0.147 R² = 0.9997

0.6 0.4 0.2

y = 0.00404 x + 0.135 R² = 0.9961

0.0

Rice grain Cd (mg kg-1)

0 0.20

20

40 60 80 100 Total dissolved As (µg L-1)

120

(B)

0.15 0.10 y = 0.692 x + 0.0099 R² = 0.9617

0.05 0.00 0.0

250

0.1 0.2 Dissolved Cd (µg L-1)

0.3

251

Figure 6. Relationships (A) between rice grain As concentrations and the total dissolved As

252

concentration averaged over post-heading three weeks, and (B) between rice grain Cd

253

concentration and the dissolved Cd concentration averaged over post-heading three weeks.

254

Sampling of soil solutions at 15 cm depth were conducted four times during the post-heading

255

three weeks. Symbols represent the average of triplicate measurements for each water

256

management plot. T-As = total As; iAs = inorganic As.


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257


Relationship between soil solution and rice grain concentrations of As and Cd

258

Figure 6 shows the relations of As and Cd concentrations in rice grains to the total As and Cd

259

concentrations in the soil solutions collected from 15 cm depth during the 3-week period after

260

heading. The dissolved concentrations are the average for each water management plot from four

261

sampling times during the period. There were positive linear correlations between rice grain

262

concentrations and total dissolved As and Cd concentrations in soil solutions, with high

263

coefficients of determination (R2) of 0.9997, 0.9961, and 0.9617 for total As, inorganic As, and

264

Cd, respectively.

265

Discussion

266

Effects of different water management strategies on As and Cd uptake

267

In the present study, we investigated the effects of periodic intermittent irrigation during pre-

268

heading 3 weeks and post-heading 3 weeks on As and Cd concentrations in grains. The Int-F3D3

269

irrigation, repeated every 6 days with 3-day flooding and 3-day drainage, reduced the grain

270

inorganic As concentration by 20% relative to the Flooded plot, and reduced the grain Cd

271

concentration by 89% relative the Rainfed plot. This was not satisfactory in view of the relatively

272

small decrease in the grain inorganic As. In the Int-F3D1 irrigation, repeated every 4 days with

273

3-day flooding and 1-day drainage, the grain inorganic As concentrations were much the same as

274

in the Flooded plot. The Int-F3D5 irrigation, with 3-day flooding and 5-day drainage, was the

275

most preferable for simultaneous reduction of inorganic As and Cd in grains, and reduced the

276

grain inorganic As concentration by 62% relative to the Flooded plot and the grain Cd

277

concentration by 56% relative to the Rainfed plot. We also note rapid increases in the dissolved

278

Cd concentration observed upon drainage during the water management periods, which stresses

279

the importance of avoiding prolonged drainage leading to excessively aerobic conditions. In


15


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280

practical situations, the efficiency of water management practices may be affected by the size of

281

paddy fields, owing to possible delay in drainage. In view of dynamic nature of the processes

282

involved, further research is needed to confirm whether the optimal irrigation interval identified

283

in this study is widely applicable across different soil types (e.g., different organic matter

284

contents), weather conditions, and As and Cd concentrations in soils.

285

Optimal soil Eh and pH for simultaneously decreasing grain As and Cd concentrations

286

Elevated dissolved As concentrations were observed in the present study as the Eh decreased

287

below 0 or –100 mV, accompanied by parallel increases in the dissolved Fe(II) concentration

288

(Figure 3). Striking increases in dissolved As were found when the soil pH was above 6.2–6.3.

289

These results are in line with earlier findings that release of As from Fe (hydr)oxides was

290

promoted upon decrease of Eh below –100 mV,17–19 and that the solid/solution distribution ratio

291

for As(III) and As(V) decreased dramatically with increasing pH from 5.5 to 7.0 and above.19

292

From the relations of the dissolved As and Cd concentrations to Eh and pH (Figure 3), a

293

threshold Eh of –100 to 0 mV and pH of 6.2–6.3 and a threshold Eh of –100 mV and pH of 6.3–

294

6.4 were identified for the solubilization of As and Cd, respectively, in soil.

295

It is of interest to find optimal Eh and pH for avoiding increased uptake of As and Cd by rice

296

in paddy fields suffering from dual contamination with As and Cd. As shown in Figure 2, the

297

dissolved As and Cd concentrations were simultaneously low under certain conditions. Based on

298

the As and Cd concentrations in soil solutions extracted from soil cores, Nakamura and Katou33

299

argued that while a high dissolved As concentration tended to coincide with a low dissolved Cd

300

concentration and vice versa, a decrease in the concentration of either As or Cd was not

301

necessarily accompanied by an increase in the other, suggesting that conditions exist where the

302

As and Cd concentrations are simultaneously low. The results in the present study corroborate


16

Page 17 of 27


304

by keeping the dissolved As and Cd concentrations at low levels during the post-heading 3-week

305

period because the rice grain concentrations were most sensitive to dissolved As and Cd during

306

this time (Figure 6).

307

1.0 0.8 Optimum Eh = –73 mV

0.6 0.4 0.2

Trade-off value [As] / [Asmax] [Cd] / [Cdmax]

0.0 -300 -200 -100 0 100 200 300 Soil Eh (mV)

[As]/[Asmax], [Cd]/[Cdmax], Trade-off value

this argument and suggest that simultaneous reduction of As and Cd uptake by rice is achievable

[As]/[Asmax], [Cd]/[Cdmax], Trade-off value

303

1.0 0.8 Optimum pH = 6.2

0.6 0.4 0.2 0.0 5.6 5.8

6.0 6.2 6.4 Soil pH

6.6 6.8

308

Figure 7. Relations of the trade-off value to soil Eh and pH. The trade-off value is defined as

309

the sum of [As]/[Asmax] and [Cd]/[Cdmax], where [As]/[Asmax] and [Cd]/[Cdmax] are the total

310

dissolved As and Cd concentrations normalized with respect to their maximum values expected

311

across the different water management plots during growth period.

312

A new indicator for the trade-off between the dissolved As and Cd concentrations

313

For evaluating the degree of trade-off between the dissolved As and Cd concentrations and

314

identifying optimal soil Eh and pH for simultaneously minimizing these concentrations, we

315

propose a new indicator, which we term the “trade-off value”. The trade-off value is defined by

316

Trade-off value = [As]/[Asmax] + [Cd]/[Cdmax]

(1)

317

where [As]/[Asmax] and [Cd]/[Cdmax] are the total dissolved As and Cd concentrations normalized

318

with respect to their maximum values expected across different water management plots during

319

the growth period (Details are given in the Supporting Information). A minimum trade-off value

320

is indicative of the most favorable condition in terms of simultaneous reduction of dissolved As


17


Page 18 of 27

321

and Cd concentrations. By non-linear regression analyses using the least-square method, we

322

obtained equations describing the relations of the total dissolved As and Cd concentrations ([As]

323

and [Cd], respectively) to Eh, pH, and dissolved Fe(II) concentration, as shown in Figure 3.

324

Based on the range of Eh values observed in the field and the equations describing the [As] and

325

[Cd] versus Eh relations, we estimated that [Asmax] = 155.6 µg L–1 and [Cdmax] = 0.781 µg L–1 in

326

the present study. Figure 7 shows the relations of [As]/[Asmax], [Cd]/[Cdmax], and the trade-off

327

value to the soil Eh and pH. The minimum trade-off values were found with an Eh of –73 mV

328

and pH of 6.2 (or an Eh range of –100 to –40 mV and a pH range of 6.1 to 6.2, allowing for a 5%

329

variation in the trade-off values).

Cd (mg kg-1)

0.20

Field experiment Estimated optimal

0.15 y = 0.0023 x-2.194 R² = 0.9553

0.10 0.05 0.00 0

330

0.2 0.4 Inorganic As (mg kg-1)

0.6

331

Figure 8. Relationship between Cd and inorganic As concentrations in grains. Each symbol

332

represents the average value for different water managements. Expected concentrations for the

333

optimum Eh of –73 mV are also shown.

334

We recognize that in a strict sense, these conditions may not be realized simultaneously.

335

However, from the [As]/[Asmax] versus Eh and pH relations and [Cd]/[Cdmax] versus Eh and pH

336

relations (eq (S6)–(S9)), we estimate that an Eh of –73 mV corresponded to a soil pH of between

337

6.1 and 6.2, which is close to the value of 6.2 found above. For optimum conditions with an Eh

338

of –73 mV, the normalized equations (eq (S6) and (S7)) predict that [As]/[Asmax] = 0.108, and


18

Page 19 of 27


339

[Cd]/[Cdmax] = 0.155. From these values and using the relationships shown in Figure 6, we

340

estimated the inorganic As and Cd concentrations in rice grain at 0.203 mg kg–1 and 0.094 mg

341

kg–1, respectively. Figure 8 shows the relationship between Cd and inorganic As concentrations

342

in grains from different water management plots. The Cd and inorganic As concentrations

343

expected for the optimum Eh of –73 mV is located close to the curve representing the

344

relationship obtained experimentally, and comparable to the Cd and inorganic As concentrations

345

in the Int-F3D5 plot (= 0.068 mg kg–1 and 0.188 mg kg–1, respectively), in which the water

346

management was most effective for simultaneous reduction of As and Cd. The new indicator of

347

“trade-off value” could be a useful tool for identifying the optimum soil Eh and pH, which

348

should be targeted by appropriate water managements during 3 weeks after heading. We note

349

that the [As]/[Asmax] versus Eh and pH relations and [Cd]/[Cdmax] versus Eh and pH relations are

350

specific to the soil tested, and that the optimum Eh and pH values may vary with experimental

351

conditions. Whereas the “trade-off value” developed in this study considers dissolved As and Cd

352

alone, exchangeable Cd2+ in soil constitutes a significant portion of plant-available Cd,42 and is

353

linked with dissolved Cd2+ through cation exchange equilibria. Our study (Figure 6) suggests that

354

the dissolved Cd is a good indicator of Cd uptake by rice plants, but possible effects of

355

solid/liquid partition of Cd2+ on the trade-off value merit future study. Further research is needed

356

to confirm whether the optimal irrigation intervals, and soil Eh and pH values are widely

357

applicable across different soil types, weather conditions, and As and Cd concentrations in soils.

358

Associated content

359

Supporting Information

360

Table S1–S3, Figure S1, details of field experiments and plant and soil analysis, description of

361

the new indicator for evaluating the trade-off between dissolved As and Cd concentrations


19


Page 20 of 27

362

(PDF). The Supporting Information is available free of charge on the ACS Publications website

363

at http://pubs.acs.org.

364

Author Information

365

Corresponding Author

366

*Phone: +81-258-35-0826; fax: +81-258-35-0021; e-mail: [email protected]

367

Notes

368

The authors declare no competing financial interest.

369

Acknowledgments

370

This work was supported by a grant from the Ministry of Agriculture, Forestry, and Fisheries

371

of the Japanese Government (Research project for improving food safety and animal health As-

372

240). The authors are grateful to Dr. Satoru Ishikawa for the determination of grain quality, Dr.

373

Koji Baba for the guidance of As and Cd analyses, and Dr. Aomi Suda and Ms Miki Tomizawa

374

for conducting chemical analyses. Laboratory assistance by Ms. Asako Eguchi, Michiko Niida,

375

and Miho Togawa is also acknowledged.

376

References

377

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Trade-off value

1.0

Optimum Eh for simultaneous reduction of As and Cd

0.8 0.6 0.4

Trade-off value [As] / [Asmax] [Cd] / [Cdmax]

0.2 0.0 -300

500 501

-200

-100

0

100

200

300

Soil Eh (mV)

Table of Contents/Abstract art


27

Optimal Soil Eh, pH, and Water Management for Simultaneously

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