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Impact of Alternate Wetting and Drying Irrigation on Arsenic Uptake and Speciation in Flooded Rice Systems

Authors:

Abstract

Alternate wetting and drying (AWD) irrigation can be used to promote oxic soil conditions and decrease arsenic (As) mobility and uptake into rice plants. However, scant information is available quantifying plant As speciation and uptake at the field scale for AWD with different soil drying severities. It is hypothesized that as the severity of soil drying increases, plant uptake and subsequent accumulation of both inorganic and organic As in the grain will decrease. However, since AWD can increase cadmium (Cd) bioavailability, Cd concentrations in rice grains should be evaluated concomitant to As. In this two-year field study, As and Cd uptake were examined, with routine plant and water sampling during the growing seasons, under three AWD practices varying in soil drying severity (from most to least severe: AWD25: drying to 25% volumetric water content at the root zone; AWD35: to 35%; AWDS: Safe AWD, drying to perched water table 15 cm below the soil surface), compared to a continuous flooding (CF) control. Arsenic speciation was also analyzed in grain and vegetative tissues. AWD25 and AWD35 decreased As accumulation in roots and straws by a similar amount compared to CF, leading to a 41-68% decrease in grain total As concentration. Speciation analysis revealed that AWD25 and AWD35 decreased grain concentration of organic As by 70-100% and inorganic As by 14-61% compared to CF. In contrast, AWDS did not decrease As uptake by rice compared to CF. Grain Cd levels were 6.5 μg kg⁻¹ in CF, 16.6 μg kg⁻¹ in AWD35, and 27.4 μg kg⁻¹ in AWD25, suggesting AWD35 could serve as a mitigation option for As, while minimizing Cd accumulation.
Short Communication
Irrigation management for arsenic mitigation in rice grain: Timing and
severity of a single soil drying
Daniela R. Carrijo
a,
, Chongyang Li
b
, Sanjai J. Parikh
b
, Bruce A. Linquist
a
a
Department of Plant Sciences, University of California-Davis, 387 North Quad, Davis, CA 95616, USA
b
Department of Land, Air and Water Resources, University of California-Davis, 387 North Quad, Davis, CA 95616, USA
HIGHLIGHTS
Continuously ooded irrigation favors
the accumulation of arsenicin rice grain.
Treatments with one soil drying period
differing in timing and severity were
tested.
Across all timings, severe soil drying
(≤−71 kPa) decreased total As
concentration.
However, inorganic As (the most toxic
to humans) not always decreased.
Irrigation management affects both
total As and As speciation within rice
grain.
GRAPHICAL ABSTRACT
abstractarticle info
Article history:
Received 21 June 2018
Received in revised form 14 August 2018
Accepted 17 August 2018
Available online 18 August 2018
Editor: Jay Gan
The accumulation of arsenic (As) in rice grain is a public health concern since As is toxic tohumans; in particular,
inorganic Ascan cause many chronic diseases including cancer. Rice crops are prone to accumulating As, in part,
due to the anaerobic soil conditions triggered by the traditional continuously ooded irrigation practice. The ob-
jective of this study was to determine how the severity and the timing (i.e. crop stage) of a single soil drying pe-
riod impacttotal As concentration and As speciation within the rice (bothwhite and brown) grain,compared to a
continuously ooded (CF)control. Drying thesoil until the perched watertable reached 15 cm below thesoil sur-
face (same severity as in the Safe Alternate Wetting and Drying), which in this study corresponded to a soil
(015 cm) water potential of ~0, did not decrease grain As concentrations, regardless of timing. Drying the soil
to Medium Severity [MS: soil (015 cm) water potential of 71 kPa] or High Severity [HS: soil (015 cm)
water potential of 154 kPa] decreased total As by 4161%. However, inorganic As did not always decrease be-
cause the severity and the timing of soil drying affected As speciation within the grain. Overall, the soil had to be
dried to HS and/or late in the growing season (i.e., at booting or heading instead of at panicle initiation) to de-
crease inorganic As concentration inthe rice grain. This studyindicatesthat the imposition of a single soil drying
period within the growing season can mitigate As accumulation in rice grain, but it depends on the severity and
timing of the drying period. Further, irrigation management affects As speciation within the rice grain and this
must be considered if regulations on inorganic As are based on a percentage of total As measured.
©2018ElsevierB.V.Allrightsreserved.
Keywords:
Alternate wetting and drying
Arsenic speciation
Soil moisture
Crop stage
Oryza sativa
1. Introduction
Rice is the primary staple food for more people on Earth than any
other crop and provides one quarter of the global calorie intake
Science of the Total Environment 649 (2019) 300307
Corresponding author.
E-mail addresses: drcarrijo@ucdavis.edu (D.R. Carrijo), cyi@ucdavis.edu (C. Li),
sjparikh@ucdavis.edu (S.J. Parikh), balinquist@ucdavis.edu (B.A. Linquist).
https://doi.org/10.1016/j.scitotenv.2018.08.216
0048-9697/© 2018 Elsevier B.V. All rights reserved.
Contents lists available at ScienceDirect
Science of the Total Environment
journal homepage: www.elsevier.com/locate/scitotenv
(GRiSP, 2013). However, rice can be a signicant route of human expo-
sure to arsenic (As), especially in populations with high rice consump-
tion (Meharg, 2004;Bhowmick et al., 2018). Different forms of As are
found in rice grains, the most common being the inorganic species
arsenite (As
III
) and arsenate (As
V
) and the organic species
monomethylarsonic acid (MMA) and dimethylarsinic acid (DMA).
While the toxicities of the organic As species are considered to be low
(Hirano et al., 2004), exposure to inorganic As is associated with many
types of cancer, in addition to other non-carcinogenic diseases such as
diabetes and hypertension (Bjørklund et al., 2017). Inorganic As accu-
mulates in the bran, causing paddy and brown rice to have higher inor-
ganic As concentration than white rice (Sun et al., 2008). Maximum
levels for inorganic As of 0.35 and 0.2 mg kg
1
in paddy and white
rice, respectively, have been adopted by CODEX, a joint commission of
the World Health Organization and the Food and Agriculture Organiza-
tion (CODEX, 2018).
Arsenic in rice grain originates from the soil, where it can be natu-
rally present (e.g., parent rock) or carried over to via irrigation
(i.e., water with high As levels) or other sources (e.g., arsenical pesti-
cides, urban residue) (Kumarathilaka et al., 2018). Arsenic tends to ac-
cumulate in rice for two reasons. First, the uptake of As
III
and, in part,
MMA are mediated by the silicon uptake pathway; rice being a silicon
accumulator is therefore naturally effective in taking up As from the
soil (Suriyagoda et al., 2018). Second, rice is commonly grown under
ooded conditions for most of the growing season. Anaerobic soil condi-
tions increase As bioavailability in the soil because it triggers the reduc-
tion of As
V
to As
III
, which is more mobile in the soil, and of Fe
III
to Fe
II
,
dissolving iron hydro(oxides) that bindto As and, subsequently, releas-
ing As to the soil solution (Meharg and Zhao, 2012). In addition, the high
irrigation input to rice contributes to As building up in the soil if the ir-
rigation water has high As levels (Kumarathilaka et al., 2018).
Since soil ooding is a major contributor to As accumulation in rice
grains, irrigation practices that include one or more periods of soil dry-
ing within the growing season [e.g., alternate wetting and drying
(AWD), intermittent ooding, mid-season drain] have been proposed
as mitigation strategies (Bakhat et al., 2017). However, the impact of
these irrigation practices on grain As concentration is highly variable,
with decreases of 0 to 90% in total grain As being reported (Arao et al.,
2009;Linquist et al., 2015;Honma et al., 2016;Yang et al., 2016;
Norton et al., 2017a;Carrijo et al., 2018). This variability may be attrib-
uted, at least in part, to differences in the severity and timing (i.e. crop
stage) of soil drying.
The severity of soil drying affects soil redox potential (Eh), which is
intrinsically related to soil As bioavailability, and subsequently As up-
take. Grain As concentration decreases sharply with an increase in soil
Eh from 200 to 100 mV and tends to plateau at very small concen-
trations (b0.02 mg kg
1
) as soil Eh increases above 0 (Honma et al.,
2016). Carrijo et al. (2018) found that total grain As concentration de-
creased with increasing soil drying severity, although drying the top
soil (015cm) to a water potentiallower than 33 kPa did nottranslate
into a further decrease in grain As concentration. However, their study
was limited to total As concentrations and, given that As speciation
may be affected by soil drying (Yamaguchi et al., 2014), their conclu-
sions may not apply to all As species present in the grain.
The effect of timing of soil drying on grain As concentration has been
scarcely investigated, with the exception of a few pot studies (e.g., Arao
et al., 2009;Li et al., 2009). Soil drying would be most effective in min-
imizing grain As concentration if imposed when As uptake is highest
under ooded conditions. However, predicting temporal As uptake is a
difcult task considering the many variables regulating As availability
and uptake. Reports that the expression of Lsi1, a root transporter in-
volved in the uptake of As
III
, is enhanced around the heading stage
(Yamaji and Ma, 2007;Ma et al., 2008), suggest that this could be a
key stage for As uptake. In contrast, Li et al. (2015) reported that of
the total As present in aboveground tissues at harvest, 64% had been
taken up at the jointing (~panicle initiation) and booting stages, and
they attributed that to enhanced nutrient uptake and root size during
this period. In addition, As uptake is strongly inuenced by the forma-
tion of iron plaques on the surface of rice roots, and their formation
and capacity of sequestering As is dependent on crop stage (Garnier
et al., 2010;Awasthi et al., 2017;Yu et al., 2017). For example, Mei
et al. (2012) found that plants at the bolting (~booting) stage showed
higher root radial oxygen loss and higher root porosity than plants at
the tillering stage, and this translated into higher As sequestration in
the root plaque and lower As uptake.
In this study, we sought to quantify how the severity and the timing
of soil drying impact total As and As speciation within the rice grain. We
hypothesized that grain arsenic concentration (total and individual spe-
cies) would decrease with increasing soil drying severity independent
of crop stage.
2. Material and methods
2.1. Study site characteristics
Aeld experiment was conducted at the Rice Experiment Station
(39°2747N, 121°4335W) in Biggs, California, USA, during the sum-
mer of 2016. The soil at the site is a Vertisol, comprised of ne, smectitic,
thermic, Xeric Epiaquerts and Duraquerts, with a soil texture of 29%
sand, 26% silt and 45% clay, a pH of 5.3, 1.06% organic C and 0.08%
total N (Pittelkow et al., 2012). Total As concentration in the soil was
3.85 mg kg
1
(Carrijoet al., 2018) and in the irrigation water it averaged
1μgL
1
in the growing season. Total As in irrigation water was mea-
sured by collecting water samples from the main irrigation canal on
four sampling dates (July 8th and 25th, August 9th and September
16th). Samples were immediately ltered [through glass microber l-
ter paper (Whatman GF/F)] and acidied with nitric acid (6770%, trace
metal grade) to a pH of 2 prior to storage at 4°C. Total As in water was
quantied by inductively coupled plasma (ICP) mass spectrometry
(MS), following the same methodology described for rice grains in
Section 2.6.2. The climate is Mediterranean, and the total precipitation
and average daily temperature over the growing season (May through
October) was 10.1 mm and 21.7° C, respectively (CIMIS, 2018).
2.2. Treatments
There were ten irrigation treatments: a continuously ooded (CF)
control, which was maintained ooded (i.e., standing water maintained
at ~12 cm above the soil surface) from sowing to three weeks before
harvest (pre-harvest drain), and nine treatments in which a single soil
drying period was imposed, and that represented a combination of
three timings and three severities of soil drying. The three timings,
which determined the onset of the soil drying period, were: at panicle
initiation, during booting and at 50% heading (this extended into the
early grain lling period for most treatments). We did not include soil
drying timings that were earlier than panicle initiation due to the risk
of potential for high fertilizer nitrogen losses (LaHue et al., 2016). The
severities were: Low Severity (LS - reooded when the perched water
table reached 15 cm below the soil surface), Medium Severity (MS -
reooded when the soil volumetric water content at the 015 cm soil
depth reached 35%), and High Severity (HS - reooded four days after
the MS treatments). The choice on severity treatments aimed at
representing a wide range of severities, from the LS, whichis the sever-
ity used in a common form of AWD known as Safe-AWD(widely
adopted in some Asian countries and considered to not limit rice yields)
(Bouman et al., 2007;Lampayan et al., 2015),to the HS, which is consid-
ered to limit rice yields (Carrijo et al., 2018). All soil drying treatments
underwent a single drying period according to their respective timing/
severity, and except for this period, followed the same water manage-
ment as in the CF. Within each timing, all plots started drying together
and plots of the same severity were reooded at the same time when,
on average, the targeted severity was reached across plots. No
301D.R. Carrijo et al. / Science of the Total Environment 649 (2019) 300307
precipitation occurred during any of the drying events. Detailed infor-
mation about the irrigation treatments and general management prac-
tices are reported in Table 1.
2.3. Experimental design and general management practices
The experiment was laid out in a completely randomized design
with four replications. Plots were comprised of polyvinyl chloride cylin-
ders (30 cm in height and 76cm in diameter total area of 0.46 m
2
) that
were buried 20 cm deep in the soil inside a rice eld (0.3 ha basin) and
2 m apart. A fertilizer blend of mono-ammonium phosphate, urea, am-
monium sulfate and muriate of potash was banded at 57 cm below the
soil surface, which provided a total of 171, 45 and 25 kg ha
1
of N, P
2
O
5
and K
2
O, respectively. Following fertilization, seeds of the medium grain
variety M-206 were broadcasted at the rate of 168 kg ha
1
, and ood-
water was applied. Pesticides were applied to all cylinders as necessary.
Irrigation was managed in individual cylinders by having two holes
drilled in each cylinder just above the soil surface (which could be
plugged or unplugged for holding or draining water, respectively) and
a drip irrigation line mounted on top of the cylinders to supply water
(same irrigation source as for the rest of eld) when needed. At the
start of each soil drying treatment, the main eld was drained along
with the desired treatment cylinders. The cylinders destined to be
kept ooded were pluggedand oodwater was maintained usingirriga-
tion from the drip line. Except for when there was a soil drying treat-
ment, the main eld was maintained ooded as in the CF to maintain
plant growth outside the cylinders, thus preventing border effects. In
addition, whenever the eld was ooded (i.e. all treatments ooded),
cylinders were kept unplugged and, except for during the rst three
weeks after sowing, oodwater height was maintained above the top
of the cylinders (i.e., 12 cm above the soil surface) to allow oodwater
exchange between cylinders and eld.
2.4. Soil moisture measurements
Soil volumetric water content (VWC) at 015 cm depth was moni-
tored using capacitance sensors (10HS, Decagon Devices Inc., Pullman,
WA) connected to data loggers (Em50, Meter Group Inc., Pullman,
USA). The sensors were installed vertically in the soil with their centers
at 7.5 cm soil depth, and had a volume of inuence of 1 L, which
spanned from 0.5 to 14.5 cm soil depth. Soil water potential (WP) at
015 cm depth was monitored using electrical resistance sensors (Wa-
termark 200SS, Irrometer Co Inc., Riverside, CA) connected to data log-
gers (900 M Monitor, Irrometer Co Inc., Riverside, CA). The sensors
were installed vertically in the soil with their centers at 7.5 cm soil
depth. One VWC and one WP sensor wasinstalled in all soil drying treat-
ment plots and, for comparison, one VWC and one WP sensor was
installed in one of the CF plots. The perched water table (PWT) was
measured at the end of the drying period in all the LS treatment plots
using perforated tubes. In each LS treatment plot, a 30 cm long, 5 cm di-
ameter polyvinyl chloride tube perforated with 1 cm diameter holes
spaced approximately 2 cm apart was inserted 25 cm deep into the
soil after drilling a hole of the exact same diameter.
2.5. Yield, yield components and grain milling for As quantication
When plants were mature, all plants were manually harvested from
within each plot. The total number of tillers was counted and the num-
ber of panicles was counted from 50 representative tillers to estimate
the percentage of unproductive tillers. Grain and straw were dried at
65 °C until constant weight for the determination of yield and harvest
index, and 1000 grains were counted using a seed counter (Model
750-2C, International Marketing and Design Corp., San Antonio, TX)
and weighed. Yield and 1000-grain weight were adjusted for 14%mois-
ture. Brown rice was obtained by removing the husk from paddy grain
using a laboratory dehusker (Model FC2K-Y, Yamamoto Co. Ltd., Yama-
gata, Japan). White rice (i.e. polished rice) was obtained by removing
the husk and the bran from paddy grain using a laboratory mill (Paz-
1/DTA, Zaccaria USA, Anna, TX). Grains were ball milled to pass a 250
μm sieve and stored in the dark at 4 °C prior to As analysis.
2.6. As quantication
2.6.1. Chemicals
All water used for analysis was 18.2 MΩcm (Barnstead Nanopure).
Trace metal grade nitric acid (6770%), ammonium phosphate dibasic
(99%) and ammonium hydroxide (2830%) were from Fisher Chemical
(USA). Stock standards of arsenite (1001 mg L
1
) and arsenate
(998 mg L
1
) were from Spex Certiprep (USA) and of DMA (98%)
and MMA (98.5%) were from ChemService (USA). Rice our certied
reference material (CRM 1568b) was from National Institute of Stan-
dards and Technology (NIST).
2.6.2. Total As
Total As in grains was determined followingthe method of Sun et al.
(2008) with some modications described as follows. Samples of 0.5 g
(two analytical replicates per plot) were digested in glass digestion
tubes by adding 5 mL of nitric acid and allowing it to dissolve overnight
at room temperature. Samples were further digested in a heating block
at 105 °C until the cessation of a brown fog, and then at 120 °C until
complete dryness. The ash was re-dissolved with 10 mL of
0.28 mol L
1
nitric acid and ltered using a syringe lter (0.45 μm), tak-
ing care to discard the rst 1 mL of the ltrate. The extract was then di-
luted 5-fold with water.
Total As in grain samples (followingthe digestion method described
above) and irrigation water samples (as collected in the eld, without
further preparation) was quantied by inductively coupled plasma
mass spectrometry (ICP-MS 7900, Agilent Technologies, Santa Clara,
CA, USA) with a detection limit of 0.01 μgL
1
. As was monitored at m/
zof 75 and selenium was also monitored (m/z77, 78 and 82) to check
for polyatomic
40
Ar
35
Cl interferences on m/z75.
Table 1
Summary of management practices.
Crop development and general management practices Date DAS
Fertilization May 26 1
Sowing and initial soil ooding May 27 0
Panicle initiation
a
Jul 11 45
50% heading
b
Aug 15 80
Pre-harvest drain Sep 21 117
Harvest Oct 12 138
Water management in soil drying treatments Date DAS
Start of panicle initiation drying period
c
Jul 12 46
LS reooded Jul 15 49
MS reooded Jul 22 56
HS reooded Jul 26 60
Start of booting drying period Jul 28 62
LS reooded Jul 29 63
MS reooded Aug 5 70
HS reooded Aug 9 74
Start of heading drying period Aug 15 80
LS reooded Aug 17 82
MS reooded Aug 26 91
HS reooded Aug 30 95
Abbreviations: DAS = daysafter sowing; LS = lowseverity; MS= medium severity; HS =
high severity.
a
Determined according to theUniversityof California Agriculture and Natural Resources
degree day model for California rice varieties available at http://rice.ucanr.edu/
Degree_Day_Model/.
b
When 50% of the panicles in the eld had at least partially exserted from the boot.
c
The start day of a soil drying period was considered the day when the perched water
table was at the soil surface.
302 D.R. Carrijo et al. / Science of the Total Environment 649 (2019) 300307
2.6.3. As speciation
As speciation in grains was determined as in FDA (2012). In brief,
samples of 1 g (two and three analytical replicates per plot for white
and brown rice, respectively) were digested in plastic centrifuge tubes
with 4 mL of 0.28 mol L
1
nitric acid at 95 °C for 90 min. The digested
sample was centrifuged at 5858gfor 15 min and the supernatant was
neutralized with the mobile phase (10 mmol L
1
ammonium phos-
phate dibasic, pH of 8.25 adjusted with ammonium hydroxide) and am-
monium hydroxide to a target pH of 6.0 to 8.5. The resulting solution
was ltered (0.45 μm nylon) prior to analysis.
Four As species (As
III
,As
V
, DMA and MMA) were quantied by high
performance liquid chromatography (HPLC 1200 series, Agilent Tech-
nologies) coupled with ICP-MS 7900. Arsenic species (elution order:
As
III
, DMA, MMA and As
V
) were separated using an anion-exchange col-
umn (Hamilton PRP-×100, 250 mm ×4.1 mm ×10 μm) with isocratic
mobile phase at 1.0 mL min
1
and then quantied by ICP-MS following
the same procedure as for total As, but with a detection limit of 0.1
μgL
1
. The percentage of inorganic As in grains (grain inorganic As%)
was calculated as in Eq. (1):
Grain inorganic As%¼100 "AsIII þAsV
AsIII þAsVþDMA þMMA ð1Þ
where As
III
, As
V
, DMA and MMA are the grain concentrations of these
species as quantied by the As speciation analysis.
2.6.4. Quality control
In both totaland speciation analyses, at least one blank, one fortied
sample (for the total As analysis, As
V
was spiked at 0.1 mg As kg
1
grain; for the speciation analysis, all four species were spiked at
0.1 mg As kg
1
grain), and one reference material (CRM 1568b) were
included with every 10 samples analyzed. Analytical replicates were ac-
cepted when their coefcient of variation waswithin 15%. For each plot,
mass balance was performed between the sum of the four species deter-
mined by HPLC-ICP-MS and the total As determined by ICP-MS. Sample
grain moisture was measured and As concentrations are presented on a
dry mass basis. Recoveries of fortied samples and reference material
and mass balances were calculated as described in FDA (2012) and are
presented in Table S1, Appendix A.
2.7. Statistical analyses
All statistical analyses were performed in R software (R Core Team,
2016) and all variables were t to a linear model before being subjected
to analysis of variance (ANOVA). A one-way ANOVA was performed on
grain As concentration (separately for brown and white rice and total As
and individual As species), yield and yield components, with treatment
as a xed effect, followed by Tukey means separation. A two-way
ANOVA was performed on soil VWC and WP with timing and severity
(as well as their interaction) as xed effects, followed by Tukey means
separation; the CF control was excluded from this analysis since these
measurements were taken in only one CF plot. A one-way ANOVA was
performed on PWT with timing as a xed effect, followed by Tukey
means separation. Grain As concentration data from brown and white
rice were combined and a two-way ANOVA was performed on grain in-
organic As% with treatment and grain milling (including their interac-
tion) as xed effects. Grain milling means were separated by Tukey
means separation. The effect of treatment was analyzed using a set of
single-degree-of-freedom orthogonal contrasts to provide information
on the factorial part of the experiment (i.e. maineffects of timing and se-
verity and their interaction), and the Sidak correction was used to con-
trol the familywise error rate. The set of contrasts excluded all LS
treatments for reasons discussed in the results Section 3.4.
3. Results
3.1. Soil moisture in the soil drying treatments immediately before
reooding
To ensure that there were no confounding effects between timing
and severity of soil drying, we tested the hypothesis that soil moisture
measured at the end of the drying period was the same across
treatments of the same severity (Table 2). Although there were small
differences in the number of drying days required to achieve a desired
soil moisture, soil WP was the same within each severity
(i.e., independent of timing) and increased in the order: HS bMS bLS,
as expected. Similarly, there was no difference in soil VWC within
each severity except for the MS (p = 0.015), where soil VWC was
lower in the treatments dried at panicle initiation than at booting. The
PWT, measured only in the LS treatments, was the same across all tim-
ings and averaged 17 cm below the soil surface.
Given the inaccuracy of the soil WP sensor in the 0 to 10 kPa range
(Irmak and Haman, 2001;Shock and Wang, 2011), we assume that any
value in this range is ~0 kPa (Table 2). Averaged across timings, soil
VWC was 48%, 36% and 33% and soil WP was 1 (~0), 71 and
154 kPa at the end of the drying period in the LS, MS and HS treat-
ments, respectively (Table 2). For comparison, soil VWC and WP in
the CF control averaged 48% and 9 kPa (~0) throughout the season,
excluding the pre-harvest draining period. The severities achieved in
the LS and MS treatments were close to what was targeted (i.e., PWT
of 17 cm vs. 15 cm targeted for LS and VWC of 36% vs. 35% targeted
for MS). Averaged across timings, the drying period lasted 2, 10 and
14 days in the LS, MS and HS treatments, respectively.
3.2. As in white rice
In all the LS treatments, the concentration of total As (Fig. 1A) and
various As species (Fig. 1C) was similar to the CF control. For both MS
and HS treatments, independent of timing, total As concentration de-
creased by 4261% compared to the CF control. Of the four As species
(i.e., organic MMA and DMA, and inorganic As
III
and As
V
) quantied in
this study, only As
III
and DMA were detected in white rice. Drying the
soil to HS (independent of timing) or to MS at booting (but not at
other timings) decreased As
III
concentration by 3146% compared to
the CF control. DMA concentration decreased by 6171% when the soil
was dried down to MS or HS at panicle initiation or booting, but not at
heading, compared to the CF control.
3.3. As in brown rice
Similar to what was observed for white rice, total As (Fig. 1B) and As
speciation (Fig. 1D) in brown rice were similar in the LS and CF treat-
ments. Total As concentration in brown rice decreased in all the MS and
HS treatments, compared to the CF control, similar to what was observed
for white rice. However, the decrease was dependent on the timing of the
drying period. Drying the soil to HS at booting decreased total As by 59%,
whereas drying the soil to MS at panicle initiation or heading decreased
total As by 4142%. There was no MMA or As
V
detected in brown rice of
any treatment. In the MS and HS treatments, As
III
concentration was
4156% lower than in the CF control at booting or heading, but not at pan-
icle initiation. DMA concentration decreased by 7181% when the soil
was dried down to MS or HS at panicle initiation or booting, but not at
heading, compared to the CF control. Averaging across all treatments,
total As, As
III
and DMA concentrations were 24 and 50% higher and 12%
lower in brown rice than in white rice, respectively.
3.4. Grain inorganic As%
Both grain milling and treatment affected grain inorganic As% (per-
centage of inorganic As relative to the sum of all As species present in
303D.R. Carrijo et al. / Science of the Total Environment 649 (2019) 300307
grain), although there was not an interaction between them (Table 3).
White rice (63%) had lower grain inorganic As% than brown rice
(75%). The effect of treatment is represented by a set of orthogonal con-
trasts. The purpose of this analysis was to test the hypothesis that de-
creases in grain total As concentration caused by soil drying are
accompanied by changes in grain As speciation. Since drying the soil
to LS had no effect on grain As concentration (Fig. 1), all LS treatments
were excluded from this analysis. The estimates obtained from the set
of contrasts indicate that, in brown and white rice, grain inorganic As
%:1) is higher in the MS and HS treatments compared to CF (on average,
Table 2
Soil moisture(soil volumetricwater content,VWC, and water potential,WP, at 0-15 cm soil depth, andperched water table, PWT)immediately beforereooding, and soildrying duration.
Soil VWC and WP were monitored in one CFplot for comparison.
Treatment VWC WP WP mean PWT
b
Duration
c
Severity Timing % kPa kPa cm days
CF 48 9- - -
LS Panicle Initiation 50 (1)
a
a 0 (0) 1C 917.4 (3) 3
Booting 48 (0.4) a 2 (2) 913.0 (3) 1
Heading 47 (0.5) a 0 (0) 919.8 (2) 2
MS Panicle Initiation 33 (1) b 57 (5) 71 B - 10
Booting 38 (1) a 69 (13) - 8
Heading 37 (2) ab 87 (3) - 11
HS Panicle Initiation 33 (1) a 173 (26) 154 A - 14
Booting 35 (1) a 163 (28) - 12
Heading 31 (2) a 127 (13) - 15
ANOVA Timing ns ns - ns -
Severity *** *** - - -
Timing:Severity * ns - - -
Abbreviations: CF=continuously ooded, LS = low severity; MS = medium severity; HS = high severity; *** = p b0.001; * = p b0.05; ns=not signicant.
a
Numbersin parenthesis are standard error of means. Differentuppercase lettersin a column indicate signicantdifferences (p b0.05). Differentlowercase letters within each severity
indicate signicant differences (p b0.05).
b
Negative PWT indicates that it is below the soil surface.
c
The duration of a drying period was the number of days from when the PWT was atthe soil surface to when the soil was reooded.
Medium Severity High SeverityLow Severity Medium Severity High SeverityLow Severity
Medium Severity High SeverityLow Severity Medium Severity High SeverityLow Severity
Fig. 1. Total As and As species concentration in brown and white rice. As
V
and MMA were not detected in any of the samples. Error bars represent standard error of means. Different
lowercase or uppercase letters indicate signicant (p b0.05) differences between treatments. Abbreviations: CF = continuously ooded, PI = panicle initiation, Boot = booting, Head
= heading.
304 D.R. Carrijo et al. / Science of the Total Environment 649 (2019) 300307
68 vs. 57% for white and 80 vs. 68% for brown rice), 2) is higher if the soil
is dried during panicle initiation or booting compared to heading (on
average, 72 vs. 60% for white and 85 vs. 72% for brown rice), and 3) is
not affected by an interaction between timing and severity of soil
drying.
3.5. Yield and yield components
There were no differences between treatments with respect to yield,
number of tillers per m
2
, percentage of unproductive tillers, and 1000-
grain weight. However, the harvest index was higher in CF (53%) than
when the soil was dried to HS at booting (47%) (Table S2, Appendix A).
4. Discussion
Our results indicate that the severity of soil drying plays an impor-
tant role in mitigating the accumulation of As in rice grain. In contrast
to the more severe MS andHS treatments, drying the soil to LS(severity
used in the Safe-AWD) had noeffect on grain total As concentration or
As speciation, independent of timing (Fig. 1). This was likely because in
the LS treatments the soil moisture never dropped below saturation
(i.e., soil WP was ~0 kPa at the end of the drying period) (Table 2),
thus, the soil was not aerated sufciently to alter As soil bioavailability.
In contrast, in soils of the same textural class as the one in this study
(i.e., clay), others have reported a decrease in grain As concentration
when the soil was dried to LS multiple times (Islam et al., 2017;
Norton et al., 2017b). This would suggest that the different results ob-
served by Islam et al. (2017) and Norton et al. (2017b) were caused
by the higher number of soil drying periods imposed in their studies.
However, another study conducted in an adjacent eld reported that
when two severe (i.e., comparable to MS and HS here) drying periods
were imposed (rst at panicle initiation, second at booting), total As
concentration in white rice decreased by 5668%, compared to a CF con-
trol (Carrijo et al., 2017); similar reductions were obtained here with a
single drying period imposed at panicle initiation (4655%) or booting
(5761%). This suggests that the number of drying periods imposed in
the growing season may not be an important factor inuencing grain
As concentrations. Differences in soil properties (other than textural
class) may explain the discrepancy between the results of our study
and the studies of Islam et al. (2017) and Norton et al. (2017b), given
that the relation between PWT and soil WP is soil-specic(Lampayan
et al., 2015). That said, decreases in grain As concentration reported in
the studies of Norton et al. (2017b) and Islam et al. (2017) with LS are
generally low (1635%) compared to what was observed here with
the higher severities MS and HS.
While all MS (i.e., soil WP of 71 kPa after 10 days drying) and HS
(i.e., soil WP of 154 kPa after 14 days drying) treatments decreased
total grain As concentration compared to the CF control, this did not al-
ways translate into a decrease in As
III
and DMA concentrations (Fig. 1C
and D), because grain As speciation varied with the timing and severity
of soil drying (Table 3). Higher grain inorganic As% was observed when
severe drying periods (MS and HS) were imposed compared to CF, and
when the drying period was imposed earlier (i.e., panicle initiation or
booting) rather thanlater (i.e., heading) in the cropping season.As a re-
sult, there were soil drying treatments (e.g., MS-panicle initiation) that
were effective in decreasing total As, but not As
III
concentration. This is
important given that inorganic As is the most toxic form of As and the
primary focus of public health regulations (Signes-Pastor et al., 2016).
Based on these ndings, reports on the effect of soil drying on grain
total As (e.g., Carrijo et al., 2018, and LaHue et al., 2016) likely overesti-
mate the health benets of soil drying in reducing grain As. Further,
these results indicate that there is not a xed conversion factor from
total As to inorganic As concentration.For example, for white ricethe in-
organic As% ranged from 52 to 75% depending on the irrigation treat-
ment (Table 3). If, due to the high cost and complexity of As
speciation analysis, regulations targeting inorganic As are made based
on an estimated percentage from total As, irrigation practices must be
taken into account.
Differences in grain inorganic As% observed between the MS and HS
treatments and the CF control (Table 3) may be a result of As transfor-
mations inthe soil triggered by soil drying.Soil microbes can convert in-
organic As into organic As and vice-versa (i.e., methylation and
demethylation reactions, respectively) and aerobic conditions favor As
demethylation over methylation reactions (Frohne et al., 2011;
Meharg and Zhao, 2012;Reid et al., 2017). In addition, there is strong
evidence that rice plants cannot methylate As and that methylated As
species found in grain originate from the soil (Lomax et al., 2012;Jia
et al., 2013;Mishra et al., 2017). These ndings suggest that soil drying
increases the proportion of inorganic As in the soil (relative to the total
As), which is then taken up by the plant and transported to the grain.
This explains the higher grain inorganic As% in the MS and HS treat-
ments compared to CF (Table 3), as others have observed (Xu et al.,
2008;Somenahally et al., 2011;Das et al., 2016).
The lower grain inorganic As% observed when the soil was dried at
heading, compared to panicle initiation and booting (Table 3), may be,
in part, explained by differences in As species translocation within the
Table 3
Percentage of inorganic arsenicrelative to all arsenic speciespresent in grain (inorganic As
%) in white and brown rice.The concentrationof inorganic arsenic(inorganic As, mg kg
-1
)
is represented for comparison (replicated data from Figure 1). The treatment effect ex-
cluded all low severity treatments, since none of them affected grain As concentration.
Grain inorganic As% (relative to the sum of all As species in grain)
Treatment White rice Brown rice
1
a
CF 57 (5)
b
68 (6)
2 LS Panicle Initiation 52 (3) 65 (5)
3 Booting 54 (5) 61 (7)
4 Heading 56 (4) 69 (6)
5 MS Panicle Initiation 75 (4) 83 (3)
6 Booting 69 (2) 85 (3)
7 Heading 58 (3) 70 (6)
8 HS Panicle Initiation 73 (3) 88 (2)
9 Booting 70 (1) 82 (3)
10 Heading 62 (6) 74 (7)
Two-way ANOVA
Treatment ⁎⁎⁎
Grain milling ⁎⁎⁎
Treatment:Grain milling
ns
Grain milling Means
c
(%)
White rice 63 b
Brown rice 75 a
Treatment Orthogonal contrast estimate
d
CF vs. (MS+HS) (-) **
(1) vs. (3+4+6+7+9+10)
MS vs. HS ns
(3+6+9) vs. (4+7+10)
Panicle Initiation vs. Booting ns
(3+4) vs. (6+7)
(Panicle Initiation+Booting) vs. Heading (+) ***
(3+4+6+7) vs. (9+10)
Interaction (Panicle Initiation vs. Booting) ns
(3+7) vs. (4+6)
Interaction (Panicle Initiation +Booting vs.
Heading)
ns
(3+6+10) vs. (4+7+9)
Abbreviations: CF = continuously ooded,LS = low severity, MS = medium severity, HS
= high severity, * pb0.05, ** pb0.01, *** pb0.001, ns = not signicant.
a
Numbers are for treatment identication referred to in the set of contrasts.
b
Numbers in parenthesis are standard error of means.
c
Means were averaged across treatments since there was not a signicant (p b0.05)
interaction between grain milling and treatment. Different lettersindicate signicant(p b
0.05) differences.
d
A positiveor a negative sign indicates that the rstterm of the contrastis, respectively,
higher or lower than the second term.
305D.R. Carrijo et al. / Science of the Total Environment 649 (2019) 300307
plant. Zheng et al. (2011) found that almost all DMA present in the ma-
ture grain was transported to the ovary before owering while most of
the inorganic As was unloaded during grain lling. Their ndings sug-
gest that any effort made to decrease DMA uptake after owering
would not translate into a decrease in DMA concentration in grains, al-
though that is not true for As
III
. In agreement, all the MS and HS treat-
ments imposed at heading did not decrease DMA but decreased (with
the exception of the MS-heading treatment for white rice) As
III
grain
concentration, compared to the CF control. In a pot study, Arao et al.
(2009) also found that aerobic treatment after heading was more effec-
tive in decreasing As
III
than DMA grain concentration, compared to aer-
obic treatment before heading. It is worth noting that although soil
drying at heading may be effective in decreasing grain As
III
, it is likely
a risky strategy as rice is very sensitive to water stress during owering
and yields and grain quality may be reduced (Sarvestani et al., 2008;
Gunaratne et al., 2011).
Grain As speciation also varied with grain milling (Table 3), with
brown rice (75%) having higher grain inorganic As% than white rice
(63%). This has been previously observed and is attributed to As
III
being less mobile in the plant than DMA, which results in As
III
being
less efciently translocated from the bran to the endosperm of the
grain (Sun et al., 2008;Carey et al., 2010;Carey et al., 2011).
While grain As concentration was impacted by soil drying, yield
(and yield components, except for harvest index) remained similar to
the CF control, independent of the timing or severity of soil drying
(Table S2, Appendix A). Based on a meta-analysis, yields are generally
reduced when the soil WP at root depth is allowed to drop below
20 kPa (Carrijo et al., 2017). However, in this study in both the MS
and HS treatments the soil WP dropped below 20 kPa (on average,
71 kPa and 154 kPa for the MS and HS treatments, respectively)
and yet yields were not reduced. In a study we conducted in an adjacent
eld, similar yields were observed between severe soil drying treat-
ments and a CF control, and this was attributed to the availability of
water and the presence of roots at deeper soil layers (Carrijo et al.,
2018). This suggests that for at least some conditions such as those in
this study, yields can be maintained while at the same time As grain
concentrations can be reduced.
5. Conclusions
This eld study indicates that a single soil drying event during the
season has the potential to mitigate As accumulation in rice grains.
However, the severity and the timing of soil drying will determine if,
and to what extent, this potential can be realized. Grain As concentra-
tion was not affected unless the soil was dried to achieve negative soil
water potentials; in this study, this meant that the soil had to be dried
further than it is for Safe-AWD (alternate wetting and drying)
(i.e., perched water table at 15 cm below the soil surface). In white
and brown rice, the lowest grain As concentrations for all species de-
tected were observed when the soil was severely dried [i.e., soil
(015 cm) water potential of 154 kPa] at the booting stage. Impor-
tantly, the timing and the severity of soil drying affected grain As speci-
ation, which resulted in some soil drying treatments being effective at
decreasing total As but not inorganic As concentration. Overall, in
white and brown rice, the soil had to be dried severely and/or later in
the season (at booting or heading instead of at panicle initiation) to de-
crease inorganic As concentration in grain, compared to a continuously
ooded control. This effect of irrigation management on grain As speci-
ation needs to be considered if regulations targeting grain inorganic As
are based on an estimated inorganic As percentage from measured total
As concentrations.
Acknowledgements
This work was supported by: CAPES Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior Brazil; the Department
of Plant Sciences, University of California Davis; and the California Rice
Research Board. We would liketo thank Nadeem Akbar, Cesar Abrenilla,
Ray Stogsdill and Peter Green for their fundamental help with data col-
lection and analysis and eld work.
Appendix A. Supplementary data
Supplementary data to this article can be found onlineat https://doi.
org/10.1016/j.scitotenv.2018.08.216.
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307D.R. Carrijo et al. / Science of the Total Environment 649 (2019) 300307
... Microorganisms play a key role in As transformation through oxidation/reduction, and methylation/volatilization reactions, but transformation kinetics are poorly understood (Kumarathilaka et al., 2018). Alternate wetting and drying (AWD) irrigation can be used to promote oxic soil conditions and decrease arsenic (As) mobility and uptake into rice plants (Li et al., 2019). Other of the effective methods for reducing heavy metal accumulation in rice grains is selection and breeding of low grain-heavy metal accumulating cultivars (Khanam et al., 2020). ...
... The concentrations of DMA in rice grain were higher >202< under CF, compared to IF because microbial methylation in rhizosphere is favored under anoxic conditions, leading to more DMA uptake, compared to oxic conditions. In order to achieve a significant reduction in the concentration of As in the grain, it is necessary to perform a severe enough flood interruption (Li, et al 2019). As concentrati on in polished grain (mg kg -1) ...
... Conversely, the drying process of anoxic samples may lead to the oxidation of As(III) and Fe(II) and their co-precipitation and crystallization, which may reduce As extractability. Numerous studies have analyzed the effects of alternate wetting and drying of rice paddy soils [32][33][34][35], but they did not provide a clear picture of how such processes affect As speciation and extractability. ...
... Although in this experiment, the concentrations of As (III) and As (V) in the extracts were not determined, it seems obvious that during the slow drying, reduced forms of As were oxidized to the pentavalent forms and re-adsorbed. The processes of such oxidation of As, in the soils that were previously subjected to waterlogging, have been described by many authors, e.g., those who examined alternate wetting and drying rice systems [32][33][34][35]. Many studies proved that these processes were mainly microbiologically driven [39,40], and their dynamics were highly dependent on the properties of soils, the kinds of microbial communities, and the availability of carbon sources. ...
Article
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This study examined the changes in extractability and fractionation of arsenic (As) that can be caused by the drying of strongly polluted anoxic soil samples. Two untreated and manure amended soils were incubated for 7 and 21 days in flooded conditions. Thereafter, As water-and 1M NH4NO3-extractability and As fractionation in a 5-step sequential extraction according to Wenzel were examined in fresh, oven-dried and air-dried samples. Soil treatment with manure considerably affected the results of the sequential extraction. Air-drying caused a significant decrease in As extractability with 1M NH4NO3 and in As concentrations in the F1 fraction. The highest reduction of extractability (30-41%) was found in manure-treated soils. Oven-drying resulted in a smaller reduction (5-34%) of As extractability. These effects were explained by opposing processes of As mobilization and immobilization. Sequential extraction did not allow for balancing As redistribution due to drying, as As loss from the F1 fraction was smaller than the confidence intervals in the other fractions. The results showed that for the precise determination of As extracta-bility in anoxic soils, fresh samples should be analyzed. However, oven-dried samples may be used for a rough assessment of environmental risk, as the order of magnitude of easily soluble As did not change due to drying.
... This leads to enhanced solubility and mobility of As in soil. Arsenate (AsO 4 3− ) is the dominate species in a well-drained and an oxygen-rich environment, but arsenite (AsO 3 3− ) is a stable species in an anoxic environment (under reduced conditions), such as routinely ooded soil (Li et al. 2019). Except at high pH and Eh values, As (V) has poor solubility. ...
Preprint
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A pragmatic approach has been chosen to assess the risk of arsenic (As) in the water-soil-plant-human continuum in an arsenic-prone area of Nadia district in West Bengal. Arsenic is a dangerous carcinogen, and people’s exposure to As via rice consumption is widely recognized. For this purpose, 201 paired soil and rice grain samples were collected from the main rice-producing agricultural field in West Bengal and analysed for their pH levels, organic carbon, extractable As, and As content in rice grain. Olsen extractable As concentration varied from 0.48 to 3.57 mg kg − 1 with a mean value of 1.45 mg kg − 1 . Rice grain samples contained As in the 0.20 to 0.61 mg kg-1 range while the mean value was 0.43 mg kg − 1 . The hazard quotient for As intake via human consumption is due to the rice grain varying between 0.27 to 0.83. Lifetime cancer risks related to As intake through drinking water and dermal intake were 1.0 × 10 − 3 and 4.23× 10 − 5 , respectively, yielding a cumulative value for an overall lifetime cancer risk ranging from 5.70 × 10 − 4 to 4.10 × 10 − 3 with a mean value of 1.09 × 10 − 3 . Solubility-free ion activity model (FIAM) could explain up to 75% variation in As concentration in rice grain. This model has been successfully validated in half of the data set for its future use for the first time. A ready reckoner was developed based on FIAM to define toxic limits of extractable As in soil with reference to pH, OC, and grain As content.
... an alternate wetting and drying irrigation system, the arsenic concentration in rice was less than for a continuous flooding irrigation system. Li et al. (2019) reported the same results for the effectiveness of alternate wetting and drying irrigation system on arsenic uptake rice. On the other hand, the effect of moisture on arsenic uptake by plants and soil is undeniable and can directly affect the bioavailability of arsenic. ...
Chapter
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Arsenic contamination could affect human health and environmental safety. Pollution of soil and water resources by arsenic and its toxic compounds has attracted a great deal of attention and concern worldwide. The severity of arsenic‐related toxicities and side effects becomes more pronounced when we realize that, based on published scientific results, long‐term exposure to arsenic and its toxic compounds could lead to various disorders and cancers in humans. The transfer of large amounts of arsenic to water resources, especially drinking water used by humans, and the accumulation of these compounds in agricultural products and human food resources have increased these hazards’ severity. Due to all these negative impacts associated with the presence of arsenic in human life and agricultural environments, finding practical and effective strategies to remove and mitigate these impacts is crucial. There are some different strategies for detoxification and reduction of arsenic in environments. Agricultural management, chemical, and biotechnological methods, bioremediation of arsenic by microbial and fungal communities, accumulation, and inactivation of arsenic in the plant cells, and fertilizer application are among the most important of these strategies. In this chapter, the points mentioned earlier are discussed in detail.
... The issue of contaminated foods is not limited to the US. Recent reports have shown that As has been found in cereal and other foods in Belgium [8], Argentina [9,10], Korea [11], and Spain [12]. Prior concerns regarding As exposure were raised at the global level as they pertained to infant rice cereal [13]. ...
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Eliminating heavy metal contamination of foods is a goal yet to be achieved in the U.S. In recent months, efforts have been underway to have the Food and Drug Administration (FDA) re-evaluate the permissible limits of lead (Pb) and arsenic (As) allowable in cereals and juices aimed for consumption by children. This report discusses the recent scientific literature that support proposed revisions in these limits. It presents proactive suggestions for the FDA to consider in its response to concerns of ongoing Pb and As exposures in food and drinks. While more scientific studies are needed to better define ‘safe’ levels of Pb and As exposures and ingestion of these elements in general are neurotoxic, the higher sensitivity of children to these toxic elements makes it imperative that the FDA adjust standards to be most protective of infants, toddlers, and children.
Chapter
Arsenic uptake in rice (Oryza sativa) is recognized as a global health emergency, requiring the development of agronomic protocols to reduce human exposure to rice having elevated arsenic concentrations. Recent rice-arsenic investigations have centered around numerous agronomic approaches, including: (i) rice breeding and cultivar selection, (ii) altering irrigation water applications to reduce arsenic soil availability, (iii) application of soil amendments which either support arsenic adsorption on iron-plaque or provide antagonistic competition for root uptake, and (iv) phytoremediation. Given that rice cultivars vary in their arsenic accumulation capacity, this manuscript review concentrates on the influences of water management, soil amendments, and phytoremediation approaches on arsenic accumulation. Water management, whether alternating wetting and drying or furrow irrigation, provides the greatest potential to alleviate arsenic uptake in rice. Phytoremediation has great promise in the extraction of soil arsenic; however, the likelihood of multiple years of cultivating hyperaccumulating plants and their proper disposal is a serious limitation. Soil amendments have been soil applied to alter the soil chemistry to sequester arsenic or provide competitive antagonism towards arsenic root uptake; however, existing research efforts must be further field-evaluated and documented as producer-friendly protocols. The usage of soil amendments will require the development of agribusiness supply chains and educated extension personnel before farm-gate acceptance.
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Arsenic exposure through rice consumption is a growing concern. Compared to Continuous Flooding (CF), irrigation practices that dry the soil at least once during the growing season [referred to here as Alternate Wetting and Drying (AWD)] can decrease As accumulation in grain; however, this can simultaneously increase grain Cd to potentially unsafe levels. We modelled grain As and Cd from field studies comparing AWD and CF to identify optimal AWD practices to minimize the accumulation of As and Cd in grain. The severity of soil drying during AWD drying event(s), quantified as soil water potential (SWP), was the main factor leading to a reduction in grain total As and inorganic As, compared to CF. However, lower SWP levels were necessary to decrease grain inorganic As, compared to total As. Therefore, if the goal is to decrease grain inorganic As, the soil needs to be dried further than it would for decreasing total As alone. The main factor driving grain Cd accumulation was when AWD was practiced during the season. Higher grain Cd levels were observed when AWD occurred during the early reproductive stage. Further, higher Cd levels were observed when AWD spanned multiple rice growth stages, compared to one stage. If Cd levels are concerning, the minimum trade-off between total As and Cd accumulation in rice grain occurred when AWD was implemented at a SWP of −47 kPa during one stage other than the early reproductive. While these results are not meant to be comprehensive of all the interactions affecting the As and Cd dynamics in rice systems, they can be used as a first guide for implementing AWD practices with the goal of minimizing the accumulation of As and Cd in rice grain.
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The accumulation of trace elements in rice, such as antimony (Sb), has drawn special attention owing to the potential increased risk to human health. However, the effects of two common irrigation methods, alternate wetting and drying and continuous flooding, on Sb behaviors and subsequent accumulation in rice is unclear. In this study a pot experiment with various Sb additions (0, 50, 200, 1000 mg Sb kg⁻¹) was carried out with these two irrigation methods in two contrasting paddy soils (an Anthrosol and an Ferralic Cambisol). The dynamics of Sb in soil porewater indicated that continuous flooding generally immobilized more Sb than alternate wetting and drying, concomitant with a pronounced reduction of Sb(V) in porewater. However, a higher phytoavailable fraction of Sb was observed under continuous flooding. The content of Sb in the rice plant decreased in the order of root > shoot > husk > grain, and continuous flooding facilitated Sb accumulation in rice root and shoot as compared with alternate wetting and drying. The differences of Sb content in root, shoot, and husk between the two irrigation methods was smaller in aboveground parts, and almost no difference in Sb was observed in grain between the two methods. The findings of this study facilitates the understanding of Sb speciation and behavior in soils with these common yet different water management regimes.
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There is a lack of affordable and effective strategies to mitigate multiple heavy metal contamination in lowland rice production. We tested phosphorus (P) or silicon (Si) addition to a soil contaminated with both arsenic (As) and cadmium (Cd) for their mitigation potential in rice seedlings. Rice variety IR64 was grown in pots with either P (0, 2.5, 5, 10, 20 (recommended rate), 40 and 80 mg P kg⁻¹ soil), or Si (0, 0.15, 0.3, 0.6, 1.2 and 2.4 g Si kg⁻¹ soil) addition until the end of tillering phase (nine weeks). Over this period, growth of rice was enhanced by up to 35% with the addition of P until the recommended rate, whereas growth was reduced beyond 0.3 g Si kg⁻¹ application. Photosynthetic rate and maximum PSII quantum yield of the youngest fully expanded leaves were similar among P and Si treatments. Phosphorus addition increased shoot [As] and decreased shoot [Cd] by up to 59% and 63%, respectively, and both effects were visible only after plants reached P sufficiency. Silicon addition from 0 to 2.4 mg Si kg⁻¹ soil increased shoot [As] by up to 28% and decreased [Cd] by up to 25%. Accumulation of As and Cd in the leaves from top to bottom of the canopy increased by factors of 10 and 7.6, respectively. Therefore, P or Si application cannot generally be recommended as remedy for rice production on multiple heavy metal contaminated soil. However, rice plants have efficient mechanisms to translocate As and Cd to mature leaves.
Article
Rice (Oryza sativa L.) consumption represents a major route for the exposure to cadmium (Cd) and arsenic (As) in many countries. Two varieties of rice that were grown in soils contaminated with Cd and As were evaluated for the accumulation of these toxins in rice grains and the risks of exposure of local residents to Cd and As when treated with different amounts of silkworm excrement and types of water management. Silkworm excrement, water management and the variety of rice significantly affected the accumulation of Cd and As in rice. The combination of multiple measures can be more effective at reducing heavy metals than the use of single measure, i.e., silkworm excrement management, water management, and the selection of low accumulation variety. The use of a variety that accumulates low amounts of Cd combined with 1% silkworm excrement management can effectively increase the soil pH and electrical conductivity (EC) and decrease the contents of soil available Cd and the transfer coefficients of Cd in rice, subsequently reducing the concentrations of Cd in rice grains and lowering the health risks of the intake of Cd. Similarly, the use of a conventional rice variety combined with alternating periods of drying and wetting in the three weeks before and after the heading stage decreased the contents of soil available As and the transfer coefficient of As in rice, subsequently reducing the accumulation of As in the grains and lowering the health risk of the intake of As. The significantly lower concentrations of Cd and As in rice grains and the risk of intake of Cd and As from rice was observed using a conventional rice variety combined with alternating drying-wetting in the three weeks before and after the heading stage and 1% silkworm excrement management. Thus, the combination of multiple measures in the coexistence of Cd and As in contaminated soils can be a promising strategy to avoid serious health risks and ensure the safety of food for local residents.
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The accumulation of arsenic (As) in rice grain is a public health concern since As is toxic to humans; in particular, inorganic As can cause many chronic diseases including cancer. Rice crops are prone to accumulating As, in part, due to the anaerobic soil conditions triggered by the traditional continuously flooded irrigation practice. The objective of this study was to determine how the severity and the timing (i.e. crop stage) of a single soil drying period impact total As concentration and As speciation within the rice (both white and brown) grain, compared to a continuously flooded (CF) control. Drying the soil until the perched water table reached 15 cm below the soil surface (same severity as in the "Safe Alternate Wetting and Drying"), which in this study corresponded to a soil (0-15 cm) water potential of ~0, did not decrease grain As concentrations, regardless of timing. Drying the soil to Medium Severity [MS: soil (0-15 cm) water potential of -71 kPa] or High Severity [HS: soil (0-15 cm) water potential of -154 kPa] decreased total As by 41-61%. However, inorganic As did not always decrease because the severity and the timing of soil drying affected As speciation within the grain. Overall, the soil had to be dried to HS and/or late in the growing season (i.e., at booting or heading instead of at panicle initiation) to decrease inorganic As concentration in the rice grain. This study indicates that the imposition of a single soil drying period within the growing season can mitigate As accumulation in rice grain, but it depends on the severity and timing of the drying period. Further, irrigation management affects As speciation within the rice grain and this must be considered if regulations on inorganic As are based on a percentage of total As measured.
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Continuously flooded rice systems are a major contributor to global rice production and food security. Allowing the soil to dry periodically during the growing season (such as with alternate wetting and drying irrigation - AWD) has been shown to decrease methane emissions, water usage, and heavy metal accumulation in rice grain. However, the effects of AWD on rice yields are variable and not well understood. A two-year study was established to quantify the impacts of a range of treatments differing in AWD severity (degree of soil drying between flooding events) on yield (as well as factors that may affect yields), soil hydrology in the soil profile, and grain arsenic (As) concentrations relative to a continuously flooded control (CF). Three AWD treatments of increasing severity were imposed between full canopy cover (around 45 days after sowing) and 50% heading: AWD-Safe (field was reflooded when the perched water table reached 15 cm below the soil surface) and AWD35 and AWD25 (field was reflooded when the soil volumetric water content at 0–15 cm depth reached 35% and 25%, respectively). During the drying periods, the 0–15 cm soil layer in the AWD-Safe remained saturated, whereas in AWD35 and AWD25 the soil dried to the desired volumetric water contents. In contrast, soil moisture at 25–35 cm below the soil surface was similar across all treatments. Yield was not reduced in any of the AWD treatments, compared to the CF control. There were no consistent differences in yield components, ¹³C discrimination, and N dynamics. Results suggest that the availability of water and the presence of roots at the 25–35 cm soil depth during the drying periods ensured that the crop did not suffer drought stress and thus yields were maintained. Grain As concentration in the AWD-Safe treatment was similar to that in the CF control but decreased by 56–68% in AWD35 and AWD25. AWD-Safe is often promoted as a means of practicing AWD without reducing yields; however, in this study this practice did not reduce grain As concentration because the soil did not reach an unsaturated state. These findings demonstrate that knowledge of surface and subsurface hydrology, and the root system are important for understanding the potential of AWD.
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Methylated arsenic (As) species represent a significant fraction of the As accumulating in rice grains, and there are geographic patterns in the abundance of methylated arsenic in rice that are not understood. The microorganisms driving As biomethylation in paddy environments, and thus the soil conditions conducive to the accumulation of methylated arsenic, are unknown. We tested the hypothesis that sulfate-reducing bacteria (SRB) are key drivers of arsenic methylation in metabolically versatile mixed anaerobic enrichments from a Mekong Delta paddy soil. We used molybdate and monofluorophosphate as inhibitors of sulfate reduction to evaluate the contribution of SRB to arsenic biomethylation, and developed degenerate primers for the amplification of arsM genes to identify methylating organisms. Enrichment cultures converted 63% of arsenite into methylated products, with dimethylarsinic acid as the major product. While molybdate inhibited As biomethylation, this effect was unrelated to its inhibition of sulfate reduction and instead inhibited the methylation pathway. Based on arsM sequences and the physiological response of cultures to media conditions, we propose that amino acid fermenting organisms are potential drivers of As methylation in the enrichments. The lack of a demethylating capacity may have contributed to the robust methylation efficiencies in this mixed culture.
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Arsenic (As) is a non-essential toxic metalloid whose elevated concentration in rice grains is a serious issue both for rice yield and quality, and for human health. The rice-As interactions, hence, have been studied extensively in past few decades. A deep understanding of factors influencing As uptake and transport from soil to grains can be helpful to tackle this issue so as to minimize grain As levels. As uptake at the root surface by rice plants depends on factors like iron plaque and radial oxygen loss. There is involvement of a number of transporters viz., phosphate transporters and aquaglyceroporins in the uptake and transport of different As species and in the movement to subcellular compartments. These processes are also affected by sulfur availability and consequently on the level of thiol (-SH)-containing As binding peptides viz., glutathione (GSH) and phytochelatins (PCs). Further, the role of phloem in As movement to the grains is also suggested. This review presents a detailed map of journey of As from soil to the grains. The implications for the utilization of available knowledge in minimizing As in rice grains are presented.
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A fundamental way to schedule irrigation is through the monitoring and management of soil water tension (SWT). Soil water tension is the force necessary for plant roots to extract water from the soil. With the invention of tensiometers, SWT measurements have been used to schedule irrigation. There are different types of field instruments used to measure SWT, either directly or indirectly. Precise irrigation scheduling by SWT criteria is a powerful method to optimize plant performance. Specific SWT criteria for irrigation scheduling have been developed to optimize the production and quality of vegetable crops, field crops, trees, shrubs, and nursery crops. This review discusses known SWT criteria for irrigation scheduling that vary from 2 to 800 kPa depending on the crop species, plant product to be optimized, environmental conditions, and irrigation system. By using the ideal SWT and adjusting irrigation duration and amount, it is possible to simultaneously achieve high productivity and meet environmental stewardship goals for water use and reduced leaching.
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Rice is the main staple carbohydrate source for billions of people worldwide. Natural geogenic and anthropogenic sources has led to high arsenic (As) concentrations in rice grains. This is because As is highly bioavailable to rice roots under conditions in which rice is cultivated. A multifaceted and interdisciplinary understanding, both of short-term and long-term effects, are required to identify spatial and temporal changes in As contamination levels in paddy soil-water systems. During flooding, soil pore waters are elevated in inorganic As compared to dryland cultivation systems, as anaerobism results in poorly mobile As(V), being reduced to highly mobile As(III). The formation of iron (Fe) plaque on roots, availability of metal (hydro)oxides (Fe and Mn), organic matter, clay mineralogy and competing ions and compounds (PO4³⁻ and Si(OH)4) are all known to influence As(V) and As(III) mobility in paddy soil-water environments. Microorganisms play a key role in As transformation through oxidation/reduction, and methylation/volatilization reactions, but transformation kinetics are poorly understood. Scientific-based optimization of all biogeochemical parameters may help to significantly reduce the bioavailability of inorganic As.
Article
A global data analysis shows that rice grain arsenic (As) concentrations increase with increasing soil As concentrations until about 60 mg As kg⁻¹soil and then decreases. Of the total grain As, 54% is composed of inorganic As. Therefore, when considering the WHO-permissible grain inorganic As concentration, i.e. 0.2 mg As kg⁻¹, the permissible grain total As concentrations is 0.37 mg total As kg⁻¹grain. Soil total As concentration when grain total As concentration reaches permissible level is 5.5 mg As kg⁻¹soil. Therefore, the suitable soil As concentrations for screening rice cultivars in rice agroecosystems for As resistance is 5–60 mg As kg⁻¹soil. Rice has traits to reduce uptake and translocation of As to grains. Cultivars with higher root porosity, radial oxygen loss, or formation of iron plaques bind more As to iron plaques, reducing As uptake (i.e. As avoidance). Once taken up, glutathione/glutaredoxin-mediated As reduction, and phytochelatin-dependent complexation and sequestration in vacuoles result in less translocation of As to the grain. Moreover, generation of reactive oxygen species and the production of antioxidant enzymes further reduce As toxicity (i.e. As resistance). These resistance mechanisms in rice agroecosystems are further enhanced when adequate concentrations of silicon and sulfur are present in soils and tissues, and when plants are associated with arbuscular mycorrhizal fungi, particularly under aerobic or intermittent-aerobic soil condition. Therefore, As concentrations in rice ecosystems decrease in the order of: roots > leaves > grains, and in grains: hull > bran polish > brown rice > raw rice> polished rice > cooked rice. Within the grain, As speciation is affected by the location in the grain, forms of As species, the grain-filling stage, geographic origin, ecosystem management and cultivars used. Indica type accumulates more As in their grains than japonica type. Rice grain production, within safe limits of As, requires the consideration of soil As dynamics including soil management, cultivar responses including uptake and translocation, and post-harvest processing techniques.
Article
This paper reviews how active research in West Bengal has unmasked the endemic arsenism that has detrimental effects on the health of millions of people and their offspring. It documents how the pathways of exposure to this toxin/poison have been greatly expanded through intensive application of groundwater in agriculture in the region within the Green Revolution framework. A goal of this paper is to compare and contrast the similarities and differences in arsenic occurrence in West Bengal with those of other parts of the world and assess the unique socio-cultural factors that determine the risks of exposure to arsenic in local groundwater. Successful intervention options are also critically reviewed with emphasis on integrative strategies that ensure safe water to the population, proper nutrition, and effective ways to reduce the transfer of arsenic from soil to crops. While no universal model may be suited for the vast areas of the world affected with by natural contamination of groundwater with arsenic, we have emphasized community-specific sustainable options that can be adapted. Disseminating scientifically correct information among the population coupled with increased community level participation and education are recognized as necessary adjuncts for an engineering intervention to be successful and sustainable.
Article
Arsenic (As) bioaccumulation in rice grains has been identified as a major problem in Bangladesh and many other parts of the world. Suitable rice genotypes along with proper water management practice regulating As levels in rice plants must be chosen and implemented. A field study was conducted to investigate the effect of continuous flooding (CF) and alternate wetting and drying (AWD) irrigation on the bioaccumulation of As in ten rice cultivars at three locations having different levels of soil As and irrigation water As. Results showed that As concentration in different parts of rice plants varied significantly (P < 0.0001) with rice genotypes and irrigation practices in the three study locations. Lower levels of As in rice were found in AWD irrigation practice compared to CF irrigation practice. Higher grain As bioaccumulation was detected in plants in areas of high soil As in combination with CF irrigation practice. Our data show that use of AWD irrigation practice with suitable genotypes led to 17 to 35% reduction in grain As level, as well as 7 to 38% increase in grain yield. Overall, this study advances our understanding that, for moderate to high levels of As contamination, the Binadhan-5, Binadhan-6, Binadhan-8, Binadhan-10 and BRRI dhan47 varieties were quite promising to mitigate As induced human health risk.
Article
For the world's population, rice consumption is a major source of inorganic arsenic (As), a nonthreshold class 1 carcinogen. Reducing the amount of total and inorganic As within the rice grain would reduce the exposure risk. In this study, grain As was measured in 76 cultivars consisting of Bangladeshi landraces, improved Bangladesh Rice Research Institute (BRRI) cultivars, and parents of permanent mapping populations grown in two field sites in Bangladesh, Faridpur and Sonargaon, irrigated with As-contaminated tubewell water. Grain As ranged from 0.16 to 0.74 mg kg(-1) at Faridpur and from 0.07 to 0.28 mg kg(-1) at Sonargaon. Highly significant cultivar differences were detected and a significant correlation (r = 0.802) in the grain As between the two field sites was observed, indicating stable genetic differences in As accumulation. The cultivars with the highest concentration of grain As were the Bangladeshi landraces. Landraces with red bran had significantly more grain As than the cultivars with brown bran. The percent of inorganic As decreased linearly with increasing total As, but genetic variation within this trend was identified. A number of local cultivars with low grain As were identified. Some tropical japonica cultivars with low grain As have the potential to be used in breeding programs and genetic studies aiming to identify genes which decrease grain As.