Soil Science and Plant Nutrition

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Effect of air temperature after heading of rice on

the arsenic concentration of grain

Tomohito Arao, Tomoyuki Makino, Akira Kawasaki, Ikuko Akahane &

Nobuharu Kiho

To cite this article: Tomohito Arao, Tomoyuki Makino, Akira Kawasaki, Ikuko Akahane &
Nobuharu Kiho (2018): Effect of air temperature after heading of rice on the arsenic concentration
of grain, Soil Science and Plant Nutrition, DOI: 10.1080/00380768.2018.1438811

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Published online: 15 Feb 2018.

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SOIL SCIENCE AND PLANT NUTRITION, 2018
https://doi.org/10.1080/00380768.2018.1438811

Effect of air temperature after heading of rice on the arsenic concentration of grain
Tomohito Araoa, Tomoyuki Makinob, Akira Kawasakic, Ikuko Akahaneb and Nobuharu Kihod
a
Director of Plant Products Safety Research, Central Region Agricultural Research Center, NARO, Tsukuba, Japan; bDivision of Hazardous Chemicals,
Institute for Agro-Environmental Sciences, NARO, Tsukuba, Japan; cAdvanced Analysis Center, NARO, Tsukuba, Japan; dDivision of Informatics and
Inventory, Institute for Agro-Environmental Sciences, NARO, Tsukuba, Japan

ABSTRACT ARTICLE HISTORY

High air temperatures during the grain-filling stage of rice (Oryza sativa L.) decrease grain yield and Received 14 July 2017
quality. Temperatures above the optimal growth temperature impair dry matter production due to Accepted 6 February 2018
reduced grain size. Since the arsenic (As) concentration in grain is determined by the As accumulation KEY WORDS
and the grain weight, we focused on the effect of air temperature before and after rice heading on the Inorganic arsenic; rice; air
As concentration in grain. Rice plants have been planted in the same field every year since 1974 with a temperature; heading stage;
similar set-up and water management. We analyzed the As concentrations in stored rice grains global warming
produced in 1995–2014 and evaluated the possible relationships with the meteorological data for the
associated production year. The average daily mean air temperatures (DMTs) from 2 weeks after the
heading day to 4 weeks after the heading day were significantly correlated with the inorganic As
concentrations in the grains, whereas there was no significant correlation between the grain As
concentration and the average DMT during 1 week after the heading day or 3 weeks before the
heading day. These findings indicate that high air temperature is more effective at increasing As in
grain in the late ripening stage of rice than before the ripening stage or in the early ripening stage.
Further experiments are necessary to clarify why As concentrations in grain increase when high air
temperatures occur in the late ripening stage of rice.

1. Introduction conditions. In contrast, more iAs accumulates in rice under

flooded conditions (Arao et al. 2009) because paddy cultiva-
Arsenic (As) is a metalloid with diverse organic and inorganic
tion mobilizes iAs in the soil by the reductive dissolution of
forms that are widely distributed in water, soil, and air. Small
iron (Fe) oxide and the subsequent reduction of As[V] to the
amounts of organic As and inorganic As (iAs) are contained in
more bioavailable As[III] (Takahashi et al. 2004).
most foodstuffs. As is present mostly as arsenobetaine in fish
The application of intermittent irrigation consisting of three
and shellfish (Hanaoka et al. 1988) and mostly as arsenosugars
days of flooding and five days of drainage around the heading
in seaweed (Francesconi and Edmonds 1997), both species are
stage of rice growth was effective for simultaneously decreas-
considered virtually nontoxic. iAs species (arsenate, As[V] and
ing the accumulation of iAs and Cd in grain without negative
arsenite, As[III]) have greater toxicity than organic As species,
effects on yield and quality (Honma et al. 2016a). An alterna-
and iAs is a nonthreshold class 1 carcinogen in humans based
tive and promising strategy is a combination of water man-
on epidemiological studies in groundwater-contaminated
agement with soil amendment to reduce the absorption of iAs
regions (IARC 2012). A market-basket study indicated that
and Cd (Honma et al. 2016b; Makino et al. 2016). Growing a
cereals contributed 62% of the total daily intake of iAs in
low-Cd-accumulating cultivar under aerobic conditions is the
Japan and algae contributed 28% (Oguri et al. 2014). Rice
most practical way to simultaneously reduce the Cd and iAs
and rice cakes contributed 97% of the iAs intake from cereals,
contents in grain (Ishikawa et al. 2016).
and virtually 100% of the iAs in algae was from hijiki
The Codex Alimentarius Commission set the maximum
(Sargassum fusiforme). Using a probabilistic approach, the
allowable levels of Cd and iAs in polished rice at 0.4 and
daily bioaccessible iAs intake in Japan was estimated to be
0.2 mg kg−1, respectively. The Commission also set the max-
19 and 59 μg/day at the 50 and 95 percentiles, respectively
imum allowable level for iAs in brown rice at 0.35 mg kg−1.
(Oguri and Yoshinaga 2014).
According to the analytical results of a survey of As concen-
Rice is a major dietary source of not only iAs but also
trations in rice conducted by the Ministry of Agriculture,
cadmium (Cd) in populations that consume rice as a staple
Forestry and Fisheries of Japan (MAFF 2014), 2.2% of polished
food. Approximately 40% of the Cd intake of the Japanese
rice cultivated in Japan in 2012 exceeded 0.20 mg kg−1 iAs,
population is derived from rice (MAFF 2016). When rice plants
and the average value (n = 600) of iAs was 0.12 mg kg−1 in
are cultivated under aerobic conditions, the Cd in paddy soil is
polished rice and 0.21 mg kg−1 in brown rice; the latter
more easily solubilized and accumulated in rice compared
represents an increase compared with the level of 0.15 mg
with the solubilization and accumulation under anaerobic
kg−1 in brown rice detected in 2004–2006. Although the cause

CONTACT Tomohito Arao arao@affrc.go.jp Director of Plant Products Safety Research, Central Region Agricultural Research Center, NARO, 2-1-18
Kannondai, Tsukuba, Ibaraki 305-8666, Japan
© 2018 Japanese Society of Soil Science and Plant Nutrition
2 T. ARAO ET AL.

of the higher iAs concentration in 2012 is unknown, differ- 3. Results and discussion
ences in the weather conditions in each year could have
Although the As concentration in brown rice stored in grain
contributed to the differing iAs concentrations in rice.
form for 1 year was stable (Naito et al. 2015), most rice samples
Global warming has increased the average air tempera-
were stored for more than 1 year, which could have affected the
ture, and high air temperatures during the grain-filling stage
grain As concentrations. However, there was no significant cor-
of rice decrease grain yield and quality (Morita and Nakano
relation between the number of years of storage until analysis
2011). Peng et al. (2004) reported direct evidence of
and the total As, iAs, and DMA concentrations in grain. The total
decreased rice yields from increased night-time tempera-
As concentrations in brown rice and polished rice varied in the
tures associated with global warming. Temperatures above
range of 0.10–0.24 and 0.06–0.16 mg kg−1, respectively. The iAs
the optimal growth temperature impair dry matter produc-
concentrations of brown rice and polished rice varied in the
tion due to reduced grain size. Ripening under high tem-
range of 0.09–0.22 and 0.06–0.13 mg kg−1 (Fig. 1), respectively.
peratures resulted in the occurrence of grains with various
The DMA concentrations of brown rice and polished rice varied
degrees of chalky appearance and decreased weight. The
in the range of <0.009–0.03 and <0.009–0.03 mg kg−1, respec-
effect of high temperatures on metabolism during grain
tively. The average extraction ratio (sum of As species/total As)
filling at the gene expression level was reported
for polished rice was 95 ± 7% and iAs accounted for 85 ± 7% of
(Yamakawa et al. 2007). Since the As concentration in
the total As. The percentages presented above correspond well
grain is determined by the As accumulation and the grain
with the results of 20 samples of polished rice previously col-
weight, we focused on the effect of air temperature before
lected from locations throughout Japan (Narukawa et al. 2011).
and after rice heading on the As concentration in grain.
The total As and iAs concentrations in polished rice were
reduced to 60–74% and 58–74% of those in brown rice. The
percent reductions presented above correspond well with the
2. Materials and methods results of Naito et al. (2015). More iAs was in the outer layer of
brown rice due to the localization of iAs in the bran layer (Zavala
The experimental field (10 m × 50 m) was located in
and Duxbury 2008).
Tsukuba, Ibaraki, Japan (Yuita and Kihou 2005; Takahashi
Since the rice plants were cultivated under flooding condi-
et al. 2004). The paddy field consisted of fine-grained gray
tions before and after heading, the Cd concentration in
lowland soil. The As content extracted by 1 M HCl and the
polished rice was low (<0.006–0.02 mg kg−1), except in 2012
Cd content extracted by 0.1 M HCl were 1.9 ± 0.15 mg
(0.09 mg kg−1, Fig. 1). Although the cause of the higher Cd
kg−1 (n = 16) and 0.15 ± 0.007 mg kg−1 (n = 16), respec-
concentration in 2012 is unknown, we assumed that the rice
tively. Rice plants have been planted in the field every
plants grown in 2012 were cultivated under aerobic condition
year since 1974 with a similar setup and water manage-
for several days around the heading stage. Therefore, we
ment. The soil surface in the paddy field was flooded with
excluded the data from 2012 in the Spearman’s rank correla-
irrigation water from the time immediately before rice
tion analysis.
transplanting in early May followed by 2 or 3 weeks of
The results of Spearman’s rank correlation analysis between
midseason drainage from late June. Thereafter, the paddy
the rice grain As concentrations and the meteorological data
field was flooded again until rice ripening in late August.
are listed in Table 1. There were no significant correlations
We analyzed the As and Cd concentrations in stored rice
between the grain As concentration and the average sunshine
grains produced in 1995–2014 and evaluated their possi-
duration, solar radiation or precipitation in the 3 weeks after
ble relationships with the meteorological data for the
the heading day (0-3W). The average DMT for 2-4W was sig-
associated production years.
nificantly correlated with the iAs concentrations in the grain
Rice seedlings (cv. Koshihikari) were transplanted in May,
(Table 1, Fig. 2), whereas there was no significant correlation
and mature rice was harvested in September. To prepare the
between the grain As concentrations and the average DMT for
polished rice, brown rice was processed by milling with a yield
of 90% (Komamura et al. 2005). Grain was stored in a refrig-
erator at 5°C until analysis. The total As, iAs, dimethylarsinic
0.14
acid (DMA), and Cd concentration in the stored grain (brown
rice: 1995–1996, 2001, 2003–2005, 2009–2010, and 2012–2014; 0.12
-1
Inorganic As conc. mg kg

polished rice: 1996–2001 and 2003–2014) were measured as

0.10
previously described (Makino et al. 2016).
Since there are no records of the heading days of rice, these 0.08
were estimated from the recorded transplantation days using 0.06
MeteoCrop DB Ver.2 (Kuwagata et al. 2011). Meteorological data
0.04 2012
(daily mean air temperature [DMT, °C], daily maximum air tem-
perature [°C], daily minimum air temperature [°C], daily total 0.02
sunshine duration [h], daily total solar radiation [MJ m−2], and
0.00
daily total precipitation [mm]) in Tsukuba were obtained from 0.00 0.05 0.10
the Weather Data Acquisition System of the Institute for Agro- Cadmium conc. mg kg
-1

Environmental Sciences, NARO. Statistical analyses were per-

formed using Microsoft Excel 2016. Figure 1. Inorganic arsenic and cadmium concentrations in polished rice.
 SOIL SCIENCE AND PLANT NUTRITION 3

Table 1. Spearman’s rank correlations between rice grain As concentrations and meteorological data.
Average daily mean air temperature
-3W-0 0-1W 1-2W 2-3W 3-4W 0-2W 0-3W 0-4W 1-4W 2-4W
Brown rice t-As 0.03 0.14 0.25 0.61 0.61 0.21 0.35 0.45 0.55 0.72*
iAs 0.14 0.12 0.45 0.71* 0.70* 0.30 0.55 0.66* 0.72* 0.75*
Polished rice t-As −0.12 0.29 0.22 0.44 0.32 0.29 0.38 0.37 0.40 0.43
iAs −0.03 0.32 0.56* 0.44 0.49* 0.52* 0.63** 0.62** 0.62** 0.49*
Average daily minimum air temperature
−3W-0 0-1W 1-2W 2-3W 3-4W 0-2W 0-3W 0-4W 1-4W 2-4W
Brown rice t-As 0.05 0.15 0.32 0.65* 0.56 0.26 0.49 0.55 0.65* 0.72*
iAs 0.08 0.24 0.48 0.72* 0.60 0.49 0.71* 0.72* 0.84** 0.76*
Polished rice t-As −0.06 0.35 0.21 0.57* 0.24 0.30 0.43 0.42 0.40 0.51*
iAs 0.03 0.40 0.53* 0.55* 0.43 0.55* 0.63** 0.64** 0.62** 0.61**
Average daily maximum air temperature Sunshine duration Solar radiation Pecipitation
−3W-0 0-3W 0-3W 0-3W 0-3W
Brown rice t-As −0.21 0.27 0.33 0.18 0.22
iAs −0.02 0.47 0.49 0.37 0.05
Polished rice t-As −0.27 0.27 0.29 0.19 0.17
iAs −0.15 0.52* 0.47 0.33 −0.01
*Significant at p < 0.05, **p < 0.01, t-As: total arsenic, iAs: inorganic arsenic, -3W-0: three weeks before the heading day, 0-1W: one week after the heading day,
1-2W: from one week after the heading day to two weeks after the heading day, 2-3W: from two weeks after the heading day to 3 weeks after the heading day,
3-4W: from three weeks after the heading day to 4 weeks after the heading day, 0-2W: two weeks after the heading day, 0-3W: three weeks after the heading day,
0-4W: four weeks after the heading day, 1-4W: from one week after the heading day to 4 weeks after the heading day, 2-4W: from two weeks after the heading
day to 4 weeks after the heading day.

a) brown rice
0.25 0.25
Inorganic As conc. mg kg-1

Inorganic As conc. mg kg-1

0.20 0.20

0.15 0.15

0.10 0.10

0.05
r=0.75 0.05
r=0.12
p=0.01 p=0.75
0.00 0.00
20 25 30 20 25 30
Average(2-4W) DMT °C Average(0-1W) DMT °C
b) polished rice
0.14 0.14
Inorganic As conc. mg kg-1

Inorganic As conc. mg kg-1

0.07 0.07
r=0.49 r=0.32
p=0.05 p=0.20
0.00
20 25 30 0.00
20 25 30
Average(2-4W) DMT °C Average(0-1W) DMT °C

Figure 2. Correlations between the inorganic arsenic concentration and the average daily mean air temperature.

-3W-0 and 0-1W (Table 1, Fig. 2). This indicates that high air
temperatures in the late ripening stage of rice would be more
effective at increasing As in the grain than high daily air
temperatures before the heading day or in the early ripening
stage. The average daily minimum air temperature in the same
stage was also significantly correlated with the grain As con-
centration which indicates that high air temperatures at night
would be more effective at increasing As in the grain than
high air temperatures during the day. Correlations between
the grain As concentration and the average sunshine duration
were not significant but the correlation coefficient was slightly
high. Although the sunshine duration was significantly corre-
lated with the average DMT (data not shown), there is a
possibility that sunshine duration directly affected iAs concen-
trations in the grain.
As accumulates constantly to an even level in the grain
during grain development, without dramatic changes in the As
concentration or As speciation when rice is grown normally in a
paddy field (Kuramata et al. 2011). The As concentration in grain
is determined by the As accumulation and the grain weight. The
average grain weight decreases under high temperature during
the grain ripening period of rice, and high night temperatures
4 T. ARAO ET AL.
(HNT) are more harmful to rice grain weight than high day
temperatures (HDT) (Morita et al. 2002). Compared with HDT,
HNT reduced the final grain weight by reducing the grain
growth rate in the early or middle stages of grain filling
(Morita et al. 2005). However, although the grain weight of
stored brown rice varied in the range of 19.6–21.4 mg (15%
moisture content), there was no significant correlation between
the As concentration and the weight.
Temperature has a considerable influence on soil micro-
bial activity and may affect the dynamics of microbial Fe
and As reduction. Decreasing the temperature from 23°C to
14°C and 5°C strongly slowed the soil reduction and Fe and
As release during the flooding of a contaminated floodplain
soil (Weber et al. 2010). High soil temperature could
increase the solubility and bioavailability of As and As
uptake by rice. Neumann et al. (2017) reported that As
concentrations in pore water and rice roots, straw, and
husks were positively correlated with soil temperature, but
the grain As did not change. Transpiration activity can be
increased by high air temperatures and xylem-mediated As
transport can be enhanced. Cd accumulation by plants is
directly related to transpiration (Ingwersen and Streck 2005).
Future experiments are necessary to clarify why grain As
concentration increases with high air temperatures in the
late ripening stage of rice.
Global warming will increase temperatures in rice-growing
areas, which could result in higher concentrations of iAs in
rice grain. In Japan, frequent extremely high temperatures
during ripening have led to the deterioration of grain quality,
especially after the year 2000 (Morita et al. 2016). Late or
early transplanting to avoid high air temperatures around the
heading stage of rice could be a countermeasure. Finding an
appropriate transplanting period to reduce the risk of poor
ripening under the many potential weather conditions is also
important.
As uptake and translocation in rice plants are affected by a
wide range of factors, including soil As speciation, soil physical
and chemical properties, and water management. Although
grain As concentrations were significantly correlated with soil
As concentrations (Fu et al. 2011), the accuracy of the estima-
tion should be improved to designate a paddy field in which
high As grain could be produced. Since this study found that
experiencing high air temperatures after rice heading can
increase the grain iAs concentrations, the highest average
temperature around the heading stage of rice in recent years
could affect the estimated risk of increasing iAs levels in grain
cultivated in paddy fields.
Acknowledgment
This work was supported by a grant from the Ministry of Agriculture,
Forestry and Fisheries of Japan (Research project for improving food
safety and animal health, As-420).
Funding
This work was supported by the Ministry of Agriculture, Forestry and
Fisheries of Japan [Research project for improving food safety and animal
health, As-240];
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