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Ecotoxicology and Environmental Safety 80 (2012) 145151

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Ecotoxicology and Environmental Safety


journal homepage: www.elsevier.com/locate/ecoenv

Effect of water management, arsenic and phosphorus levels on rice in a


high-arsenic soilwater system: II. Arsenic uptake
A.S.M.H.M. Talukder a,n, C.A. Meisner b, M.A.R. Sarkar c, M.S. Islam d,
K.D. Sayre e, J.M. Duxbury b, J.G. Lauren b
a

School of Agriculture, Food and Wine, Waite Campus, the University of Adelaide, SA-5064, Australia
917 Brad Field Hall, Cornell University, Ithaca, NY 14853, USA
c
Department of Agronomy, Bangladesh Agricultural University, Mymensingh-2002, Bangladesh
d
Former Director General, Bangladesh Agricultural Research Institute, Gazipur-1701, Bangladesh
e
Bosques de Canelos 129, Bosques de las Lomas, Mexico DF, Mexico
b

a r t i c l e i n f o

abstract

Article history:
Received 15 October 2011
Received in revised form
20 February 2012
Accepted 22 February 2012
Available online 15 March 2012

Rice consumption is one of the major pathways for As intake in populations that depend on a rice diet
in several countries of South and South-east Asia. Pot experiments were undertaken to investigate the
effects of water management (WM), arsenic (As) contaminated soil-water and Phosphorus (P) rates on
As uptake in rice plants. There were 18 treatments comprising of three each of As rates (0, 20 and
40 mg kg  1 soil) and P rates (0, 12.5 and 25 mg kg  1 soil) and two WM (aerobic and anaerobic)
strategies on winter (boro var. BRRI dhan 29) and monsoon (aman var. BRRI dhan 32) rice at the Wheat
Research Center (WRC), Nashipur, Dinajpur, Bangladesh. Arsenic concentrations in rice grain and straw
increased signicantly (nnP r 0.01) with the increasing As rates in the soil. Arsenic availability in soil
pore-water solution was less (58%) under aerobic WM (redox potential-Eh 135 to 138 mV;
pH6.50 at 24.3 1C) as compared to anaerobic WM (ooded: Eh  41 to  76 mV; pH-6.43 at 23 1C).
The highest total grain As content 2.23 7 0.12 mg kg  1 and 0.623 70.006 mg kg  1 was found in T6
(P12.5As40-anaerobic) and T9 (P25As40-anaerobic) in BRRI dhan 29 and BRRI dhan 32, respectively, which
was signicantly higher (4145%) than in the same As and P treatments for pots under aerobic WM. The
As content in rice straw (up to 24.7 7 0.49 ppm in BRRI dhan 29, 17.3 7 0.49 mg kg  1 in BRRI dhan 32
with the highest As level) suggested that As can more easily be translocated to the shoots under
anaerobic conditions than aerobic condition. BRRI dhan 29 was more sensitive to As than BRRI dhan 32.
Under aerobic WM, P soil amendments reduced As uptake by rice plants. The study demonstrated that
aerobic water management along with optimum P amendment and selection of arsenic inefcient rice
varieties are appropriate options that can be applied to minimize As accumulation in rice which can
reduce effects on human and cattle health risk as well as soil contamination.
& 2012 Elsevier Inc. All rights reserved.

Keywords:
Arsenic
Phosphorus
Pore-water
Rice
Water management

1. Introduction
Rice (Oryza sativa L) is by far the most important cereal grown
in Bangladesh. Per capita cereal consumption is 150.4 kg year  1
of which rice is 91% (Alam et al., 2002). High As concentrations in
soil and the use of irrigation water with high As levels may lead to
elevated concentrations of As in cereals, vegetables and other
agricultural products in As affected areas of Bangladesh (Alam
et al., 2003a, b; Williams et al., 2006). Khan et al. (2009) found
that increasing arsenic concentrations of both soil and irrigation
water resulted signicantly increased As concentrations in both
rice grain and straw. Khan et al. (2010) also found that addition of

Corresponding author. Fax: 61 8 8303 7109.


E-mail addresses: asmhmpalash@yahoo.com,
asm.talukder@adelaide.edu.au (A.S.M.H.M. Talukder).
0147-6513/$ - see front matter & 2012 Elsevier Inc. All rights reserved.
doi:10.1016/j.ecoenv.2012.02.020

As either in irrigation water or in soil decreased grain yields by


2174% in boro rice and 8 to 80% in aman rice. Human exposure to
As is mainly through the intake of drinking water and foods, such
as rice grains, that contain elevated amounts of As (Duxbury and
Panaullah, 2007). Arsenic-contaminated rice could aggravate
human health risk because it is consumed in large quantities
especially in Asian countries (FAO, 2002).
Rice growing in the anaerobic situation was found to score the
highest amount of As among all grain crops (Marin et al., 1993).
Boro rice is exposed to As caused by both soil and irrigation water,
whereas the aman rice is exposed to As through the natural soil
As in addition to the build up of As over time due to use of
contaminated irrigation water (Duxbury and Panaullah, 2007).
Duxbury and Panaullah also assessed that As accumulation in
soils could be increased at the rate of 1 mg kg  1 crop  1 through
the use of 1.5 m of irrigation water containing 0.13 mg As L  1,
resulting in no net loss of As from the soil environment, it has a

146

A.S.M.H.M. Talukder et al. / Ecotoxicology and Environmental Safety 80 (2012) 145151

strong residual effects on following crops (Khan et al., 2010).


Dittmar et al. (2010) also found that annually there was an
estimated 4.4 70.4 kg ha  1 a  1 As deposited through irrigation
water. In the top 40 cm soil, the mean As accumulation over three
years were recorded to 2.470.4 kg ha  1 a  1, implying that there
was an average loss of As is 2.0 kg ha  1 a  1. Arsenic contaminated groundwater has caused As accumulation in soils as high as
83 mg As kg  1 soil (Ullah, 1998).
The As content of lowland paddy-rice grain is generally much
higher than that of upland rice or other cereal crops (Schoof et al.,
1999; Williams et al., 2007) because of the high availability of soil As
under anaerobic (lowland, ooded) conditions as compared to upland
(aerobic) rice. The global normal range of As concentration in rice is
0.080.20 mg kg  1 (Zavala and Duxbury, 2008). But, rice grains
contained As as high as 1.835 mg of As kg  1 have been found in
Bangladesh (Meharg and Rahman, 2003). For a Bangladeshi adult, the
average per day intake of As from As contaminated rice can be nearly
100 mg As (400 g dry wt  0.25 mg As kg  1), which is 5 times higher
when compared to 20 mg As intake from consumption of 2 L of water
at WHO recommendation (10 mg As L  1) (Panaullah et al., 2009).
The presence of high As concentrations in agricultural soils and
the use of As contaminated irrigation water may affect the movement
of As in soil and its accumulation by rice (Abedin et al., 2002a).
Arsenic dynamics and uptake by rice is impacted by complex soil
variables and environmental and management factors. Different soils
can behave differently. Two factors that have received considerable
attention are water management and soil phosphate to mitigate
arsenic phyto-toxicity and its uptake by rice plants. Hossain et al.
(2009) observed that Fe-oxide plaque formation on the root surface
has reduced As toxicity effects in a ooded-rice culture and thereby
resulted in increased grain yields and reduced grain-As accumulation.
On the other hand, the effect of applied phosphate was opposite.
Growing rice in an aerobic situations where As is adsorbed on
oxidized Fe surfaces and renders it largely unavailable to uptake by
the rice plant (Lauren and Duxbury, 2005; Duxbury and Panaullah,
2007). Arsenic may also be present as arsenate where uptake is
interrupted by phosphate (Abedin et al., 2002b), whereas arsenite is
found in ooded anaerobic soils and can be readily taken up by plant
cells allowing its passage into the plant parts (Meharg and Jardine,
2003) and which is not affected by phosphate (Abedin et al., 2002b;
Creger and Peryea, 1994). So, from the above discussion it has come
out that As uptake by rice plants parts would have a distinct negative
impact on quality and protability of rice products.
Water Management (WM) includes two systems: keeping the
amount of irrigation water applied to just attain soil moisture near
saturation (aerobic) vs. ooded anaerobic conditions. Understanding
such effects of WM and P amendment and their interactions under As
contaminated soil is critical to minimize As uptake by the rice plants.
Therefore, the objectives of the present study were to: (1) investigate
the impacts of water management on arsenic uptake by the rice
plants, and (2) determine the inuences of P amendment on As
uptake under different WM regimes.

2. Materials and methods


The high yielding boro (BRRI dhan 29), and aman (BRRI dhan 32) rice, were
grown in plastic pots at the Wheat Research Center, Nashipur (251380 N, 881410 E,
and 38.2 m asl), Dinajpur, Bangladesh. Both are popular rice varieties widely used
in Bangladesh (Khan et al., 2010). Soil used in the pots was extracted from a
typical eld in Dinajpur. Soil was Non-calcareous Brown Floodplain soil according
to the Bangladesh soil classication system (FAO-UNDP, 1988), sandy loam and
acidic in nature (Tables 1 and 2). The soils were analyzed for selected physical and
chemical characteristics before initiation of the experiment. The physico-chemical
properties of the pot soil are presented in Tables 1 and 2.
Treatments consisted of three levels each of As (0, 20 and 40 mg of As kg  1
soil) and P (0, 12.5 and 25 mg of P kg  1 soil) and two WM levels; ooded
(anaerobic) and near saturated conditions (aerobic) conditions. There were

Table 1
The physical properties of the pot soil.
Physical properties of soil

Value (%)

Sand (20.05 mm)


Silt (0.050.002)
Clay (o 0.002 mm)
Soil texture class
Moisture

60
18
22
Sandy loam
20.5

Table 2
The chemical properties of the pot soil.
Chemical properties of soil

Value

pH (1: 2) soil: water


Organic carbon (%)
Exchangeable potassium (meq/100 g soil)
Exchangeable calcium (meq/100 g soil)
Exchangeable magnesium (meq/100 g soil)
Total N
Available phosphorus (mg kg  1)
Available sulphur (mg kg  1)
Available zinc (mg kg  1)
Available iron (mg kg  1)
Available boron (mg kg  1)
Arsenic (mg kg  1)

5.5
0.25
0.23
2.35
0.70
0.064
7.31
1.09
0.53
23.24
0.23
10.00

eighteen treatment combinations in the experiment. The design was completely


randomized and each treatment was replicated three times.
2.1. Pot preparation
An amount of 5 and 3 kg soil was taken in each of 5 and 3 l plastic pots for
BRRI dhan 29 and BRRI dhan 32, respectively. The heights of the 3 and 5 l pots
were 14.1 cm and 18.6 cm and diameters were 14.4 and 18.9 cm, respectively.
There were altogether 54 pots for both BRRI dhan 29 and BRRI dhan 32. For
aerobic WM (near saturation), pots were placed into a plastic bowl 6.5 cm deep.
Each pot had ve holes to create an opportunity for removal of excess water or
uptake by the plant as and when necessary. On the other hand, under anaerobic
(ooded) WM, there were no holes in the pots to remove the excess irrigation
water to create a ooded situation.
2.2. Fertilizer application
2.2.1. Transplanted BRRI dhan 29
The total amount of P, potassium (60 mg K kg  1 soil), sulphur (12.6 mg S kg  1
soil) and zinc (3.6 mg Zn kg  1 soil) for each pot were calculated and added as a
solution of triple super phosphate, murate of potash, gypsum and zinc sulphate
(monohydrate), respectively in distilled water and was applied once before transplanting the rice seedlings during nal pot preparation. After fertilization, irrigation with
distilled water was applied to the pot to bring the soil up to saturation. Arsenic was
applied as a solution of Na2HAsO4.7H2O (24% As) in distilled water in concentrations of
0, 20 and 40 mg As kg  1 soil at one day after transplanting. The total amount of
nitrogen (124 mg N kg  1 soil) was supplied as a solution of urea in distilled water and
applied in three equal splits at 15, 45 and 55 day after transplanting (DAT).
2.2.2. Transplanted BRRI dhan 32
The total amount of P (0, 12.5 and 25 mg kg  1 soil) from triple super phosphate,
potassium (35 mg K kg  1 soil) from murate of potash, sulphur (12.6 mg S kg  1 soil)
from gypsum and zinc (3.6 mg Zn kg  1 soil) from zinc sulphate (monohydrate) for
each pot were calculated and mixed in distilled water and applied once before
transplantation of the rice seedlings during nal pot preparation. After fertilization, the
pots were irrigated with distilled water to bring the soil up to saturation. Arsenate was
applied as a solution of Na2HAsO4.7 H2O (24% As) in distilled water in concentrations of
0, 20 and 40 mg As kg  1 soil at one day after transplanting. The total amount of
nitrogen (70 mg N kg  1 soil) as a solution urea in distilled water was applied in three
equal splits at 15, 30 and 45 DAT.
2.3. Seedling transplanting
Two 35-day old seedlings per pot were transplanted into the plastic pots and
grown to maturity inside a clear polyethylene tent house. The overall temperature

A.S.M.H.M. Talukder et al. / Ecotoxicology and Environmental Safety 80 (2012) 145151


in the tent ranged from 24 1C to 38 1C and relative humidity from 79.9% to 96.2%.
Air temperature in the polythene tent was 5 1C to 6 1C and relative humidity was
2% to 3% higher than that of the ambient conditions. To avoid high temperature
and humidity, there was a good aeration provided by 0.61 m openings under the
covering clear plastic tent.

2.4. Water management


For aerobic WM, the pots were irrigated daily until the soil moisture attained
near saturation and this was maintained up to grain lling stage. There was no
waterlogged condition inside the pots. On the other hand, under anaerobic WM,
excess irrigation water was applied to create an over-saturated condition (ooded;
5 to 6 cm depth) which was maintained up to grain lling stage. Distilled water
was always used for irrigation. In aerobic pot culture there was an opportunity to
uptake excess water leached down through the holes.

147

2.12. Total arsenic


The plant samples (grain [dehusked unpolished rice] and straw) were digested
with concentrated nitric acid and perchloric acid. A sub-sample weighing 0.5 g
was transferred into a dry clean digestion vessel. Five ml of conc. HNO3 was added
and the sample allowed standing for overnight under fume hood. The following
day, the vessels were placed on a heating block and were heated at a temperature
slowly raised to 120 1C for 2 h. After heating, the vessel was allowed to cool and
2 ml of conc. HClO4 was added. Again, the vessel was heated 180 1C for an hour.
Heating was stopped when the dense white fumes of HClO4 occurred. Arsenic was
determined from this digest. Total arsenic content in grain or straw samples were
then determined from the digest by ow injection hydride generation ame
atomic absorption spectroscopy (Samanta et al., 1999).

2.13. Data collection and statistical analysis


2.5. Intercultural operations
Fertilizer top dressing, hand weeding and other phyto-sanitary measures were
taken as and when necessary, equally among all pots. A light trap was used to
control stem borer, rice bug and leafhopper, ies, etc. infestation at reproductive
stages of boro and aman rice in pot culture (Reissig et al., 1986).

Data on yield and yield contributing characters, included effective tillers


hill  1, grains panicle  1, sterile spikelets panicle  1, panicle length, 1000-grain
weight, root biomass, straw yield and grain yield and visual rating of straighthead
disease (reported in separate paper) and other parameters such as As uptake by
the plant parts, pore-water total As and Eh were also determined. Data were
subjected to analysis of variance using MSTAT-C and GenStat. Treatment means
were compared using Duncans Multiple Range Test (DMRT) at p o 0.05.

2.6. Redox potential


Eh is an electrical measurement that can indicate whether the soil is aerobic or
anaerobic. Eh was measured [Hanna pH/ORS (mV)/Temperature meter Model no
HI 991002] at maximum tillering stage of rice.

3. Results

2.7. Pore-warter

The Eh range, in waterlogged soils of BRRI dhan 29 and BRRI


dhan 32 in pot culture, varied from  41 to  76 mV [pH-6.43 at
23.2 1C]. The soil was highly reduced under ooded WM indicating that the soil was anaerobic. On the other hand, the Eh values
of both BRRI dhan 29 and BRRI dhan 32 pots varied from 135 to
138 mV [pH-6.50 at 24.3 1C] under near saturated WM, showing
that the soil was oxidized and aerobic.

Soil pore water samples were collected directly from the root zone of rice at
10 cm depth at maximum tillering stage (60 DAT) of each treatment of BRRI dhan
32. The water extraction device comprised of a porous ceramic cup attached to a
1 cm diameter, 30 cm long PVC pipe. A vacuum inside the PVC tube-ceramic cup
unit was created with the use of hand suction pump (Panaullah et al., 2009). The
collected water samples were passed through the membrane lter paper (Whatman branded 47 mm diameter with 0.45 mm pore size) by using a plastic syringe
to remove the colloidal materials. A 30 ml aliquot of pore-water sample from each
treatment was dispensed to a 60 ml washed plastic vial, adding one drop of 10 N
HCl into the plastic vial, stopper and shaken gently. Immediate after collection it
was stored in a refrigerator at below 10 1C and analyzed for total arsenic
concentration within 3 day.

2.8. Available phosphorus


Available P was extracted from the soil with 0.5 M NaHCO3 solution, pH 8.5
(Olsen et al., 1954). Phosphorus in the extract was then determined by developing
blue color with reduction of phosphomolyddate complex. The color intensity was
measured colorimetrically at 660 nm wave length (Page et al., 1982).

2.9. Available sulphur


Available sulphur content was determined by extracting the soil with CaCl2
(0.15%) solution as described by Page et al. (1982). The extractable S was
determined by developing turbidity by adding acid seed solution (20 ppm S as
K2SO4 in 6 N HCl) and BaCl2 crystals. The intensity of turbidity was measured by
spectrophotometer at 420 nm wave length.

2.10. Available zinc and iron


Available Zn and Fe contents in soil were determined by DTPA extraction
method as described by Hunter (1984). The extractable elements were measured
by Atomic Absorption Spectrometer (AAS) using air-acetylene ame and matrix
matched standards.

2.11. Available boron


Available boron content in soil was extracted from the soil by monocalcium
phosphate (MCP) extraction method as described by Hunter (1984). The B content
in the extract was determined by developing yellow color using curcumin and
measuring the absorbance on spectrophotometer at 555 nm wavelength.

3.1. Redox potential

3.2. Arsenic uptake by plant parts


3.2.1. Main effects of As, P and WM
Arsenic concentrations in rice grain and straw increased
signicantly (nnPr0.01) with the increases As rates applied to
the soil. Phosphorus also had a signicant (nnPr0.01) effect on As
uptake by plants. Under aerobic WM (Eh 135 to 138 mV;
pH-6.50 at 24.3 1C), As uptake by the plant parts was signicantly
(nnPr0.01) less as compared to anaerobic WM (Eh 41 to
 76 mV; pH-6.43 at 23.2 1C).
Increasing the rate of As (0, 20 and 40 mg As kg  1 soil) to the soil
signicantly increased the total grain As content from 0.316 to
1.263 mg kg  1 in BRRI dhan 29 and 0.159 to 0.473 mg kg  1 in BRRI
dhan 32, respectively (Fig. 1a). The highest straw As content of
14.65 mg kg  1 (in BRRI dhan 29) and 11.23 mg kg  1 (in BRRI dhan
32) was measured at the highest As level (40 mg As kg  1 soil)
(Fig. 1b).
The grain As content (Fig. 1a) varied from 1.076 to 0.748 mg kg  1
in BRRI dhan 29 and 0.333 to 0.362 mg kg  1 in BRRI dhan 32 and
was signicantly affected by the P levels specially in BRRI dhan 29. In
BRRI dhan 29, the highest total grain As content was recorded at
the12.5 mg P kg  1 soil level and was less in the 0 and 25 mg P kg  1
soil levels. A similar trend was also observed in total straw As content
in BRRI dhan 29 (10.31 mg kg  1 As) rice (Fig. 1b).
Aerobic WM practices signicantly reduced the total grain As
content vs. anaerobic WM from 0.607 to 1.123 in BRRI dhan 29
and 0.301 to 0.402 mg kg  1 in BRRI dhan 32 (Fig. 1a), respectively. Similarly the total straw As content was markedly lower in
aerobic vs. anaerobic in BRRI dhan 29 (from 6.42 to 12.46) and in
BRRI dhan 32 (5.48 to 9.11 mg kg  1), respectively (Fig. 1b).

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A.S.M.H.M. Talukder et al. / Ecotoxicology and Environmental Safety 80 (2012) 145151

3.2.2. Interaction effects of As, P and WM


Total grain As content was signicantly (nnPr0.01) affected by
the interaction of As, P and WM (Table 3). Under anaerobic ooded
condition the addition of P had positive effects on As uptake by the
rice plants whereas it was negative under aerobic conditions in both
BRRI dhan 29 and BRRI dhan 32 pot culture. Total grain As content
was decreased from 2.23 to 0.28 mg kg  1 under anaerobic and 1.23
to 0.20 mg kg  1 under aerobic WM in BRRI dhan 29. The highest
grain As content (2.2370.12 mg kg  1) was found in T6 (P12.5As40-

anaerobic). Under aerobic WM at the same As and P rates the total


grain As content was signicantly reduced (1.2270.04 mg kg  1). In
BRRI dhan 32, the total grain As content decreased from 0.63 to
0.13 mg kg  1 under anaerobic and 0.430.16 mg kg  1 under aerobic
WM. The highest grain As content (0.6370.006 mg kg  1) was
recorded at T9 (P25As40-anaerobic) followed by T8 and T6. With the
same P (25 mg P kg  1 soil) and As (40 mg As kg  1 soil) amendment,
grain As concentration was signicantly reduced to 0.3270.012
under aerobic WM. The total straw As content varied from 24.72 to
2.07 mg kg  1 under anaerobic and 13.58 to 1.057 mg kg  1 under
aerobic WM in BRRI dhan 29. The highest straw As content
(24.770.49 mg kg  1) was obtained in T6 (P12.5As40-anaerobic) but
under aerobic WM with same As and P level, the total straw As
content was also signicantly reduced to 10.3270.41 mg kg  1. In
BRRI dhan 32, total straw As content ranged from 17.33 to
1.89 mg kg  1 and 9.21 to 1.32 mg kg  1 under anaerobic and aerobic
WM, respectively. The highest straw As (17.3370.24 mg kg  1)
content was found in T9 (P25As40-anaerobic) treatment. Under aerobic
WM with same amount of As and P produced the least As content
(5.1170.06 mg kg  1) in straw.
Thus there was a positive strong relationship (r 0.88;
nn
Pr0.001) between As in the straw and grain for rice grown
for the different WM regimes (Fig. 2). Correlation coefcient
matrix showed that grain and straw As concentrations were also
correlated with each other, providing evidence that grain As
content highly depended on straw As content (Table 4).
3.3. Arsenic content in soil pore-water

Fig. 1. Main effect of arsenic, phosphorus and water management on arsenic


uptake by grain (a) and straw (b) of boro (var. BRRI dhan-29) and aman (var. BRRI
dhan-32) rice. Error bars represent least signicant differences of means
(*p r 0.05). As-Arsenic level (mg As kg  1 soil); P-phosphorus level (mg P kg  1
soil); A-aerobic water management; An-anaerobic water management.

Arsenic and WM markedly affected the total As content in soil


pore-water. Arsenic content in soil pore-water increased by
adding of As (0, 20 and 40 mg of As kg  1 soil responsible for
0.001, 0.036 and 0.109 ppm arsenic content in pore-water,
respectively) to the soil under the pot culture (Fig. 3a). Water
management also had signicant effects on total As content in soil

Table 3
Interaction effects of arsenic, phosphorus and water management on arsenic uptake by aman (var. BRRI dhan-32) and boro (var. BRRI dhan-29) rice plant tissue and total
arsenic content in pore-water at maximum tillering stage (60 day after seedling transplanting) of aman rice pots.
Treatment code

Interactions (WM  P  As)

Aman (mg kg  1)
Grain

Anaerobic-P0As0
P0As20
P0As40
P12.5As0
P12.5As20
P12.5As40
P25As0
P25As20
P25As40

T1
T2
T3
T4
T5
T6
T7
T8
T9
Mean

Aerobic-P0As0
P0As20
P0As40
P12.5As0
P12.5As20
P12.5As40
P25As0
P25As20
P25As40

T10
T11
T12
T13
T14
T15
T16
T17
T18
Mean
Grand mean
CV (%)

Boro (mg kg  1)
Straw

Pore-water

Grain

2.087 0.08 h
10.887 0.64 bc
15.82 70.86 a
2.097 0.19 h
9.587 0.68 cde
11.56 70.35 b
1.897 0.15 h
10.727 0.33 bcd
17.33 70.24 a

0.001 70 e
0.017 70.003 de
0.147 7 0.003 b
0.001 70 e
0.070 70 c
0.083 70.006 c
0.001 70 e
0.063 70.003 c
0.190 70.01 a

0.407 0.04
0.74 70.03
1.76 7 0.03
0.28 70.02
1.78 7 0.05
2.23 7 0.12
0.41 70.02
1.50 70.06
1.01 70.03

0.40 70.008

9.107 0.39

0.06 70.003

1.12 7 0.04

0.16 7 0 f
0.35 7 0.024 d
0.43 7 0.030 c
0.20 70.020 f
0.43 7 0.037 bc
0.32 7 0.012de
0.28 7 0.012 e
0.37 7 0.046 cd
0.52 7 0.003 b

1.327 0.21
7.347 0.30
9.217 0.49
1.497 0.14
9.147 0.71
8.377 0.20
2.097 0.13
5.267 0.35
5.117 0.06

0.001 70 e
0.017 70.003 de
0.027 70.057d
0.001 70 e
0.023 70.003 de
0.077 70.003 c
0.001 70 e
0.023 70.003 de
0.070 70.006 c

0.207 0.03
0.72 70.02
0.67 70.03
0.27 70.01
0.66 70.03
1.23 7 0.04
0.33 70.03
0.69 70.04
0.69 70.04

0.34 7 0.020
0.37 70.014
9.38

5.487 0.28
7.297 0.33
9.78

0.026 70.008
0.045 70.005
14.88

0.607 0.03
0.867 0.03
8.48

0.16 7 0.003
0.39 7 0.013
0.51 7 0.006
0.15 7 0.010
0.45 7 0.013
0.61 7 0.006
0.13 7 0.009
0.62 7 0.014
0.63 7 0.006

fa
cd
b
f
bc
a
f
a
a

h
f
cde
h
de
ef
h
g
g

Straw
g
f
b
gh
b
a
g
c
e

12.43 70.48
h
f
f
gh
f
d
gh
f
f

WM-Water managementanaerobic water management (ooded) and aerobic water management (near saturated).
P-Phosphorus level (mg P kg  1 soil); As-arsenic level (mg As kg  1 soil).
a

2.077 0.05 hi
14.66 70.35 cd
15.64 70.90 bcd
2.647 0.09 hi
17.54 71.08 b
24.72 70.49 a
4.237 0.36 gh
14.14 70.36 cd
16.27 70.64 bc

Figures with the same letters are not signicantly different as per Duncans Multiple Range Test at 5% level; 7 SEM of three replicates.

1.647 0.12 i
9.807 0.40 e
13.58 70.92 d
1.517 0.12 i
5.127 0.19 fg
10.327 0.41 e
1.067 0.08 i
7.367 0.21 f
7.367 0.30 f
6.417 0.30
9.427 0.39
10.96

A.S.M.H.M. Talukder et al. / Ecotoxicology and Environmental Safety 80 (2012) 145151

149

Fig. 2. Relationship between grain and straw As concentrations in (a) boro (var. BRRI dhan 29) and (b) aman rice (var. BRRI dhan 32); n 54.

Table 4
Correlation coefcients (r) between grain and straw arsenic concentrations of
aman (var. BRRI dhan-32) and boro (var. BRRI dhan-29) rice.

Aman grain
Aman straw
boro grain
boro straw
n

Aman grain

Aman straw

Boro grain

Boro straw

1
0.882n
0.789n
0.852n

1
0.732n
0.827n

1
0.878n

Signicant at 0.001 level; n54.

pore-water. The maximum arsenic (0.064 ppm) content in porewater was recorded under anaerobic WM (Fig. 3b).
The interaction effects of As and WM was signicant
(nnp r0.01) on total As content in soil pore-water (Fig. 3c) of
transplanted BRRI dhan 32 rice in pot culture. Arsenic contaminated ooded soil had a marked inuence on As content in porewater. The highest As content (0.14 mg kg  1) in soil pore-water
was recorded at As40 (40 mg of As kg  1 soil) under anaerobic
conditions which was 44% higher as compared to aerobic WM
(0.08 mg kg  1) with the same As level. The interaction effects of
P  As  WM (aerobic vs. anaerobic) was signicant (nnp r0.01)
on As content in soil pore water (Table 3). The highest As content
(0.19070.01 mg kg  1) in soil pore water was recorded in T9
(P25As40-anaerobic) followed by T3 (P0As40-anaerobic).

4. Discussion
4.1. Arsenic uptake by plant parts
The strongest relationship was found between plant As concentration and soil solution As (Fig. 1). Arsenic concentration in
rice plant parts generally followed the pattern: roots 4straw4
husk4 whole grain4husked rice (Xie and Huang, 1998). The data
(Fig. 1) for As concentration in grain and straw clearly showed
that irrespective of As doses, straw contained higher concentrations of As than grain. This effect was noticed for all As treatments. This nding was also conrmed by the other scientists
(Khan et al., 2010; Hossain et al., 2009; Talukder et al., 2011).
Overall, the arsenic concentration in BRRI dhan 29 grain was 2.46
times and straw 1.29 times higher as compared to BRRI dhan 32.
This suggested that the BRRI dhan 29 cultivar used in this study
had the ability to take up more As than the BRRI dhan 32 cultivar.
Duxbury et al. (2003) also reported As concentration in boro grain
rice 1.5 times higher than aman rice of Bangladesh.
Under an aerobic soil condition the most probable available form
of P might be inorganic phosphate. It is analogous of arsenate, the
oxidized inorganic form of As, and is taken up and translocated via
the phosphate transporter systems (Meharg and Macnair, 1992,
1994). The chemical form of phosphate and arsenate are PO3
and
4
AsO3
have similar valance (3) and exhibit similar
4 , both

physicochemical behavior in soils and compete directly for specic


adsorption sites on the soil particles (Woolson, 1977). Meharg and
Macnair (1994) reported that arsenate also acts as a phosphate
analog with respect to transport across root plasma membrane, with
phosphate competing much more effectively for transport sites.
Arsenate is a dominated species of As under aerobic conditions (Xu
et al., 2008; Li et al., 2009). Our results indicate that under aerobic
conditions grain and straw As content of BRRI dhan 29 and BRRI dhan
32 was signicantly reduced by the addition of P except for a few
exceptions (Table 3). Under aerobic pot culture, the As availability in
the soil solution is less due to maintaining of non ooded conditions
resulting in less As solubility and also there was less As uptake by the
plants. Alternatively, the decrease in As content in aerobic soil
condition might be caused by lower soil water-soluble As via the
replacement of phosphate by arsenate. So, it is more likely that
phosphate will compete with arsenate for uptake and suppress
arsenate uptake system, resulting in low accumulation of arsenate
(McBride, 1994). Results of this study regarding the effectiveness of
phosphate to reduce As plant uptake are also in agreement with the
ndings of many scientists (Abedin et al., 2002b; Creger and Peryea
1994). This result might be considered surprising as phosphate and
As are analogs and are taken up by plants through the same transport
system. Heavy additions of phosphate to a soil has been shown to
displace As as much as 80% of the total As present in the soil, with the
water-soluble As leaching down and adsorbing in a lower level of the
soil prole (Woolson et al., 1973). Displacement of As by P has been
used to ameliorate the toxic effects of As in some soils (Schweizer,
1967). Leaching of the displaced As from the rooting zone is necessary
for the reduction of As toxicity in soils by the addition of P (Barrow,
1974). Under aerobic soil conditions As may interact with P and xed
with applied P, resulting in As becoming unavailable to plants. It may
not happen under anaerobic conditions. Ghoshal et al. (2003) found
that P uptake was reduced with the increase in soil As concentration,
indicating a signicant AsP interaction. Arsenic uptake could be
suppressed by phosphate if soils have sufcient P reserve for plant
growth (Buresh et al., 1980; Alberts et al., 1990). On the other hand
under anaerobic WM situations, addition of phosphate to soils
increased As accumulation in grain and straw of BRRI dhan 29 and
BRRI dhan 32 (Table 3). Arsenite is the dominated As species found in
ooded anaerobic soils (Xu et al., 2008; Li et al., 2009) which is
readily taken up by plant cells (Meharg and Jardine, 2003) and is not
affected by phosphate (Abedin et al., 2002b; Creger and Peryea,
1994). Jahiruddin et al. (2004) reported that application of P
enhanced the As accumulation in ooded rice grain and straw while
the P content in grain and straw remained unaffected by As addition
to soil. Hossain, et al. (2009) also found that the effect of added
phosphate increased As concentrations in both grain and straw. It
might be possible that application of high levels of P may increase the
As toxicity in soils.
A signicant reduction of As accumulation by rice plant was also
caused by WM practices. In these experiments, under aerobic WM
(Eh 135 to 138 mV; pH-6.50 at 24.3 1C), plants took up a lower

150

A.S.M.H.M. Talukder et al. / Ecotoxicology and Environmental Safety 80 (2012) 145151

Fig. 3. Pore-water total As concentrations at 60 day after seedlings transplanting as affected by (a) arsenic levels, (b) water managements and (c) water management and
arsenic levels on aman rice (var. BRRI dhan 32). Error bars represent least signicant differences of means (*p r0.05). As-Arsenic level (mg As kg  1 soil).

amount of As due to its less availability in soil pore water (Table 3


and Fig. 3). However, redox values in the aerobic condition were high
enough that at least some Fe was oxidized with As potentially being
adsorbed by Fe, Al and other particles in the soil (Lauren and
Duxbury, 2005), leading to reduced As phytoavailability. Furthermore,
under anaerobic (Eh  41 to 76 mV; pH-6.43 at 23 1C) conditions,
the increases of As in the soil solution would resul from the
conversion of arsenate to arsenite (Xu et al., 2008; Li et al., 2009) as
the redox potential of the soil declined within 20 day ooding. As a
result, As was more available in soil water due to ooding (Xu et al.,
2008; Takamatsu et al., 1982; Onken and Hossner, 1995). In a similar
way, rice grown on permanent raised beds, which remain at higher
Eh value, contained less As than conventional cultivation on the at
(Talukder et al., 2011). Therefore, growing rice aerobically throughout
the entire season may be an effective way to mitigate As accumulation in rice without yield penalties, which is in agreement with the
ndings of Xu et al. (2008) and Talukder et al. (2011).
In contrast, there was a positive relationship between As in
rice straw and grain, implying that grain As content progressively
increased with the increases of straw As under both WM conditions. But results from the other eld study partly conrmed that
there was a positive relationship between grain and straw As
when rice was grown more aerobically to mitigate As toxicity
(Duxbury and Panaullah, 2007).
4.2. Arsenic content in soil pore-water
A remarkable reduction (48%) of total As content in soil porewater was found in aerobic WM compared to anaerobic management (Fig. 3b). A signicant increase of As was observed in the
soil pore-water at higher P and As amendments (Table 3). The
increasing rate of As was higher in anaerobic conditions due to
ooding and decreased Eh (  41 to  76 mV). Under anaerobic
conditions, the increase of As in soil solution resulted from the
conversion of arsenate to arsenite as the Eh of the soil declined

within 20 day ooding. As a result, As was more available under


ooded conditions (Takamatsu et al., 1982; Onken and Hossner,
1995). The considerable change of As content in soil pore-water
was caused by the interaction effects of P  As  WM (Table 3).
Arsenic content signicantly increased in soil pore-water at the
highest P amendment and As treated pots under anaerobic WM.
The observed increase in uptake of As into rice grain and straw
with increasing soil-As concentration is consistent with increases
in pore-water As. Panaullah et al. (2009) also found a similar
increasing trend in case of straw As content with increases in
pore-water As but not in grain As content.
So, next to drinking water, rice would be a major source of As
exposure to humans that depend on a rice diet. Furthermore
higher As concentration in rice straw can cause possible adverse
health effects by feeding the contaminated straw to the cattle
population still has to be considered. Therefore, As contamination
in rice is a serious problem, and it is urgent to develop strategies
for minimizing As accumulation and toxicity in rice plants.

5. Conclusion
This study has conrmed that anaerobic water management is the
main reason for the high enhanced As uptake in rice. Phosphorus has
a positive impact on As mitigation under aerobic WM. Similar, a
recent eld study has shown that the furrow irrigated, permanent
raised bed system might be a better options to reduce As accumulation as compared to conventional anaerobic system in rice (Talukder
et al., 2011). The processes discussed in this paper have important
implications to rice cultivation, especially under aerobic WM with P
amendment, which might impact As uptake by rice. However, further
detail study should be recommended to nd out the potential effects
of phosphate, its analog (arsenate) through the use of balance
fertilization under raised beds in reducing As uptake. Screening of
As inefcient rice varieties that perform well under raised beds

A.S.M.H.M. Talukder et al. / Ecotoxicology and Environmental Safety 80 (2012) 145151

conditions and are productive in an aerobic environment with less


water in needed. The aims of WM and varietal screening would be
helpful to reduce As deposition into the soils, reduce As accumulation
in rice grain and straw and maximize grain yield as well as conserve
the water resources.

Acknowledgments
Authors are grateful to the Bangladesh Agricultural Research
Institute (BARI), CIMMYT Bangladesh, Cornel University and Texas
A&M University for funding to do the Ph.D. experiments.
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