IJERD – International Journal of Environmental and Rural Development (2017) 8-1

Research article
erd

Reducing Cadmium and Copper Uptake of Soybeans byControlling Groundwater Level and its Impacts on Growthand Yield
SONGTAO LI*The United Graduate School of Agricultural Sciences, Iwate University, Morioka, JapanCHOICHI SASAKI
Faculty of Agriculture and Life Science, Hirosaki University, Hirosaki, Japan
Email: chsasaki@hirosaki-u.ac.jp

CHIHIRO KATO
Faculty of Agriculture and Life Science, Hirosaki University, Hirosaki, JapanNOBUHIKO MATSUYAMA
Faculty of Agriculture and Life Science, Hirosaki University, Hirosaki, Japan

TAKEYUKI ANNAKA
Faculty of Agriculture and Life Science, Hirosaki University, Hirosaki, JapanAKIRA ENDO
Faculty of Agriculture and Life Science, Hirosaki University, Hirosaki, Japan

KIICHI SASAKI
Aomori Prefectural Improvement Projects Federation, Aomori, Aomori, Japan
Received 15 November 2016

Accepted 5 May 2017(*Corresponding Author)

Abstract In Japan, cadmium (Cd), copper (Cu) and arsenic have been designated as specificharmful substances in the Agricultural Land Soil Pollution Act. Though the safety standards ofthese substances have not been provided for upland field crops in Japan, it is important tominimize the concentration of these contaminants in agricultural products for both international
trading and our health. The objective of this study is to clarify the effects of controlling
groundwater levels on Cd and Cu uptake and growth and yield of soybeans. For this experiment,
three plastic containers were prepared, and then 14cm-thick of non-contaminated gravel, 15cmthick of non-contaminated soil (0.12 mg Cd kg-1; 2.4 mg Cu kg-1) and 25cm-thick ofcontaminated soil (2.24 mg Cd kg-1; 43.4 mg Cu kg-1) were placed in this order from the bottomof each container. Then the groundwater level of each container was maintained as 5cm (GL5),10cm (GL10) and 40cm (GL40) during the growing period. As a result, Cd and Cu
concentration of soybean seeds of GL5, GL10 and GL40 were 0.25, 0.52 and 1.07 mg Cd kg-1,
respectively, and 5.08, 5.82 and 9.96 mg Cu kg-1, respectively. Significant difference in both Cd
and Cu concentration of soybean seeds were found among three models at 5% level. On theother hand, growth and yield of soybeans tended to decrease with the rise of the groundwaterlevel. Noticeably, plant heights and weights of a hundred grains were significantly different
among these three models. From the above, it can be concluded that controlling groundwaterlevels can reduce Cd and Cu uptake and affect growth and yield of soybeans.
Keywords soybeans, uptake of cadmium and copper, control of groundwater level,
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INTRODUCTION
Soil contamination in arable lands is a threat to human health through the intake of agricultural produce.
In Japan, since there has been some serious problems as seen in such grave impacts of heavy metals in
the cases of itai-itai disease induced by cadmium (Cd) and a decrease of rice yield affected by copper(Cu) (Yamane et al., 1997), “Agricultural Land Soil Pollution Act” was passed into law in 1970.
According to this law, Cd and Cu, and arsenic were designated as specifically harmful substances(Kobayashi, 1978). In 2010, the safety standard for Cd in brown rice was lowered to 0.4 mg kg -1 in
Japan, while other countries such as countries in the EU, China, Australia, etc., have stricter standards(MAFF, 2015). The safety standards for upland crops have not been provided yet in Japan. However,studies for reconsideration of Cd standards have been conducted as consumers’ interests in safety andsecurity of food (MAFF, 2007).
In Japan, an expansion of growing areas of soybeans is one of the important counter- measures forincreasing calorie based food self-sufficiency rate. Some countries provide the safety standard of Cd insoybean seeds as 0.2 mg kg-1, while in Japan, Cd concentration in soybean seeds which have been
produced even in non-contaminated field often exceeds this value (MAFF，2004 ). It is inferred,
therefore, that soybeans produced in Cd-contaminated and semi contaminated fields may contain much
more Cd. Thus there is real concern that Japanese domestic soybeans will not meet the standards ofexport-partner countries such as United States and Hong Kong etc. (Ishitsuka and Jindai, 2013) ininternational trading. As for Cu in soybeans, it is a future task for Japan to provide a safety standard
value, while some other countries already have such, e.g., 20 mg kg-1 in China (MAPRC, 2005).
As similar to the case of paddy fields, some techniques for reducing Cd uptake of soybeans e.g.,soil dressing, chemical methods such as controlling pH, and phyto -remediation etc. have been
evaluated recently (Akahane et al., 2013; Dong et al., 2007). These measures, however, cost muchmoney and take a long time, and so they have not been implemented widely yet (Haque et al., 2014a,b). Furthermore, soil dressing needs a large amount of soil and so it causes a heavy environmental
burden (MEGJ, 2010).
As a cost-saving and easy technique, Murakami et al. (2011) and Haque et al. (2014a, b) reported
that the Cd uptake of soybeans decreased by controlling oxidation reduction potential of the plowed
layer by changing the groundwater level since Cd becomes insoluble under a reduction condition.
Cu also becomes insoluble under reduction condition (Matsui and Okazaki, 1993) and thus it isexpected that controlling the groundwater level is also effective in reducing the Cu concentration incrops. The effects of a shallow groundwater level, especially higher than 10cm, on the Cu uptake ofcrops have not been evaluated yet and neither the distribution of Cu in soybean plant bodies.
Heretofore groundwater level was controlled by relief well and insoluble condition of Cu by pH
control amendment was made (Matsui and Okazaki et al., 1993; Yamane et al., 1997).
Against this background, the objective of this study is to clarify the effects of the controlling
groundwater level on Cd and Cu uptake and growth and yield of soybeans. To achieve the purpose,
growing tests of soybeans were conducted by using Cd- and Cu- contaminated soil samples. During theexperiments, the groundwater level was maintained as 5, 10 and 40cm to control the thickness of soil
layer, in which Cd and Cu was soluble.
This study will help to clarify the effects of rice-soybean crop rotation in contaminated ill- and/or
well-drained paddy fields on Cd and Cu uptake of soybeans and to develop techniques for reducing Cd
and Cu uptake with a low cost.
MATERIALS AND METHODS
Soil PropertiesⒸ ISERD

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In this experiment, we used soil sampled from the plow layer of a paddy field which had been
contaminated with agricultural water from mine drainage. Non-contaminated soil had been sampledfrom the plow layer of the paddy field at Kanagi farm of Hirosaki University, Aomori prefecture, thenortheastern part of Japan. Gravels had been collected from a nearby mountain, Mt.Iwaki, Aomori
prefecture.
Chemical and physical properties of the soil samples are shown in Table1. Soil textures ofcontaminated and non-contaminated soil were both clay loam. Cd concentration in contaminated soil,
non-contaminated soil and gravels were 2.27, 0.12 and 0.13 mg kg-1, respectively while Haque et al.
(2014a, b) had used contaminated soils of 3.39 and 1.57 mg kg-1. Cu concentration in the contaminatedand non-contaminated soil in this study was 43.4 and 2.4 mg kg-1, respectively. The contaminated soils
in this study contained seven times and twice as much Cd and Cu, respectively, as those in the averagenon-contaminated agricultural lands in Japan, the figures of which are 0.33 mg Cd kg-1 and 24.8 mg Cu
kg-1 (Asami, 2010).
Table 1 Physical and chemical properties of the soil samples
SampleDensity(g cm-3)

Soil
Texture

MgO
*

Na2O
*

CaO
*

K2O
*

Cu
*

Cd
*

T-N
(%)

T-C
(%)

C/N

OM
(%)

Polluted soil

2.57

CL

224

96

2032

232

43.4

2.27

0.28

3.39

12.2

5.86

Non-polluted
2.54
CL
120
64
400
120
2.4
0.12 0.16 2.07 13.3 3.62
soil
Gravel
2.68
147
18
539
58
1.5
0.13
0
0.05
Note: Soil texture is based on the International Soil Society classification. CL: Clay loam. Gravel diameter size 2-4mm.
*mg kg-1

Experimental Design
In this study, a growing test of soybeans was conducted with stratified field models. Three plastic
containers (41×61×63 cm) were prepared and then they were packed with 14cm-thick of gravels (drybulk density ρd=1.40 g cm-3), 15cm-thick of non-contaminated soil (ρd=0.89 g cm-3) and 25cm-thick ofcontaminated soil (ρd=0.80 g cm-3) in this order from the bottom of each container. After packing thesamples, oxidation reduction potential sensors were inserted at depths of 2.5, 7, 9, 12.5, 14.5, 22, 32,
37, 42cm. Soil temperature sensors were also buried at depths of 5, 15, 25 and 35cm in each container.
During the experiment period, the groundwater level of each container was maintained as 5, 10, and40cm; hereafter we call the models GL5, GL10 and GL40, respectively.
Cultivation Procedure
We used Ryuho soy bean (Glycine max (L.) Merr.cv.Ryuho) as the breed variety of our cultivation
experiment. The holes of 3 to 5 cm diameter at the four positions in each container were made, andthen 5 to 6 grains were seeded in June 16, 2014. Thinning out was done in 14 days after seeding andleft two of normal growth. Harvesting was conducted between late September and early October,which is the grain filling period in Japan. The groundwater level after seeding was 15cm, the groundwater levels after germination were 5, 10 and 40cm. The authors used Marriott bottles to control thegroundwater levels and checking of each groundwater level was carried out by using three groundwater
pipes attached to the containers. The recommended amount of chemical fertilizer for Ryuho soy bean
was added. 2L of irrigation water was supplied in 4-days intervals (equivalent to 2.0 mm d-1).
Protection treatment was done when it was necessary.

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Measurement Method
Oxidation-reduction potential (ORP) electrodes were installed for measuring oxidation-reduction
potential at arbitrary depths of the soil boxes. Measuring with the ORP meters (model UC-23, Central
Kagaku co. Ltd) was conducted during the entire period of cultivation experiment. The growth andyield assessments such as plant height, leaf age, branching, pod number and 100-grains weight, werecarried out based on the cultivation guideline of soybean in Akita Prefecture (Akita Prefecture, 2015).
After harvesting, Cd and Cu were extracted with HCl and HNO3 and their concentration in stem andleaf, root, grain and soil, was quantified by analyzing their specimens with the atomic absorption
spectrophotometry (MAFF, 1979). Other physical and chemical properties of the soil was alsomeasured with the standard methods in Japan. We found a significant difference in the results ofgrowth and yield assessments by using the Tukey-Kramer method.
RESULTS AND DISCUSSION
Oxidation-Reduction Potential (Eh)Eh(mV)For a long time, the reduction condition of soil has been known to cause insolubility of Cd and Cu, thishas been utilized to Cd uptake suppression (Yamane et al., 1997). That is, by increasing the solubilityof Cd and Cu in the soil in the oxidation condition, the uptake of these heavy metals from plant roots is
promoted. On the other hand, it is known that the uptake of these heavy metals is inhibited when theirsolubility is reduced in the reduction condition. In the oxidation-reduction potential (Eh), the oxidation
layer and the reduction layer are defined as Eh≧300mV and Eh＜300mV, respectively (Iimura, 1981).
Measured Eh values on each of the groundwater levels are shown in Figs.1, 2 and 3. In the GL5
container (Fig.1), Eh values measured at the 2.5cm depth was an oxidation layer of about 600mV;
however, below the 7cm depth Eh values indicated reduction condition. In the GL10 container (Fig.2),
Eh values at 2.5cm and the 7cm depths indicated more than 500mV; however, Eh values measured
below the 12cm depth was a reduction layer of Eh ＜ -100mV. In the GL40 container (Fig.3), except
for Eh values measured at the 42cm depth, all of the observation depths became oxidation layers of Eh≧ 500mV.

800
700
600
500
400
300
200
100
0
-100
-200
-300

Oxidation state
Reduction state

0

Soil depth fromthe surface
2.5cm
7cm
12cm
14.5cm
22cm
32cm
42cm

10 20 30 40 50 60 70 80 90 100
Measurement day
Fig.1 Temporal changes of Eh with GL5Ⓒ ISERD80

Eh(mV)

IJERD – International Journal of Environmental and Rural Development (2017) 8-1

Soil depth fromthe surface
2.5cm
7cm
Oxidation state
12cm
Reduction state
14.5cm
22cm
32cm
42cm

800
700
600
500
400
300
200
100
0
-100
-200
-300

Eh(mV)

0 10 20 30 40 50 60 70 80 90 100 110
Measurement day
Fig.2 Temporal changes of Eh with GL10
Soil depth fromthe surface
2.5cm
7cm
Oxidation state
12cm
Reduction state
22cm
32cm
37cm
42cm

800
700
600
500
400
300
200
100
0
-100
-200
-300

0 10 20 30 40 50 60 70 80 90 100110120
Measurement day
Fig.3 Temporal changes of Eh with GL40
From these results, it became apparent that controlling the upper part of the groundwater table tobe an oxidation layer and the part below the groundwater table to be a reduction layer can be possible.
It is inferred from this that thickness of supply layer of solubilized Cd and Cu are estimated as about
5cm for GL5, about 10cm for GL10, and about 40cm for GL40. From the temporal changes of Ehvalues measured at each level of the groundwater table, after clarifying the oxidation-reduction
environment of the root zone, preparation for comparing values of the uptake behavior of Cd and Cu
can be said to have been established. Although the values of heavy metal concentration in thecontaminated soil were different, the vertical directions of Eh distribution controlled in the GL10 and
the GL40 models were almost the same as the result of Haquet al. (2014a, b). In addition, it isestimated that the Eh values in the canonical paddy field depend on the soil crashing rate, the amountof organic matter, and soil pH.
Cd and Cu Concentration in Soybean Plants
Cd concentration in soybean seeds was GL5 (0.25mg kg-1) < GL10 (0.52mg kg-1) < GL40 (1.07mg kg -1)
and there were significant differences among the three treatments (p < 0.05) (Table 2). Those values
were three to ten times greater compared with Cd concentration in soybeans in non-polluted soil
(Murakami et al., 2011). Cd concentration in stems was GL5 (0.28mg kg-1) < GL10 (0.45mg kg-1) <GL40 (1.48mg kg-1) and there were little significant difference between GL5 and GL10. However,Ⓒ ISERD

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there was significant difference between GL5 and GL40, and also between GL10 and GL40 (p < 0.05).
Cd concentration in roots was GL10 (3.54mg kg-1) < GL5 (4.92mg kg-1) < GL40 (5.80mg kg-1) andthere was a significant difference between GL10 and GL40 (p < 0.05). The trend of Cd concentration
in soybean plants were seed < stem < root as found by Haque et al. (2014a, b). Cd concentration inseeds was about 1/10 compared with the one in roots in the case of GL5 and GL10. Cd concentration inseeds was about 1/5 compared with that of roots in the case of GL40. It is thought that Cd
concentration in soybean plants is affected by the groundwater level. Cd concentration in seeds was
0.25mg kg-1 in the GL5 treatment and it was close to the standard Cd content in non-polluted soil
(MAFF, 2004). There is a high possibility that Cd concentration in soybean seeds can be suppressed
when soybeans are cultivated in poorly drained Cd-contaminated paddy field. From these results, it
was considered that the control of the groundwater level had the effect of reducing the Cd
concentration in soybean seeds.
Table 2 shows Cu concentration in soybean plants. Cu also change the solubility by oxidationreduction potential as well as Cd. Cu concentration in soybean seeds was GL5 (5.08mg kg-1) < GL10
(5.82mg kg-1) < GL40 (9.96mg kg-1) and there were significant differences among the three treatments
at p < 0.05. The average Cu concentration in edible soybeans in Japan, the United State and China is
0.97-1.07 mg kg-1 (MEXT, 2016). The Cu concentration found in our current study was about fivetimes higher than the above figure. One reason may have been that the Cu concentration in the soil weused this time was twice higher than the average Cu concentration in typical Japanese soil. Cu
concentration in stems was GL5 (2.45mg kg-1) < GL10 (2.76mg kg-1) < GL40 (5.58mg kg-1) and there
was little significant difference between GL5 and GL10. However, there were significant differences
between GL5 and GL40, and also between GL10 and GL40 (p < 0.05). Cu concentration in roots was
GL40 (14.06mg kg-1) < GL10 (39.48mg kg-1) < GL5 (50.04mg kg-1) and there were little significant
difference between GL5 and GL10. However, there was significant difference between GL5 and GL40,
and also between GL10 and GL40 (p < 0.05). The trend of Cu concentration in soybean plants wasstem < seed < root. Cu concentration in seeds, however, was higher than that in stems unlike Cdconcentration in the plant. It is thought to be due to transfer characteristics of Cu in soybean plants. Cu
concentration in roots in GL5 and GL10 was twice higher than that of GL40. The morphologicalcharacteristic of roots is that there are many thick roots in the GL40 treatment and many fine root mat
in the GL5 and GL10 treatments. The different root morphology may have affected the uptake ofnutrient by soybeans. Cu concentration in soybeans at low groundwater levels was relatively high. Cu
concentration in soybeans was higher than that in brown rice (Paul et al., 2011). Soybean seeds tend toaccumulate more Cu than brown rice. Cu concentration in soybeans is defined as less than 20mg kg-1 in
China (MAPRC, 2005). On the other hands, there is no regulation value of soybean Cu content inJapan. However, those results of ours are valuable data because soybeans are important food and Cu in
this food is detrimental for human health. From the above results, the control of the groundwater levelis considered to be effective in reducing Cd concentration and Cu concentration in soybean seeds.
Table 2 Cd and Cu concentration in soybean of three different groundwater levels
Model
GL 5cmGL 10cm

Seed-Cd

Stem-Cd

0.25±0.04
0.52±0.06

ab

Root-Cd

0.28±0.02a

0.45±0.09a4.92±1.54

Seed-Cuab

3.54±0.56a5.08±0.27a5.82±0.33b

Stem-Cu

Root-Cu

2.45±0.19

a50.04±13.93a

2.76±0.98

a39.48±7.51a

GL 40cm
1.07±0.17c
1.48±0.41b
5.80±1.03b
9.96±0.62c
5.58±0.51b
14.11±3.66b
Note: Small letter indicates significant difference at 5% level according to Turkey-Kramer test; ± shows standard
deviation. For Seed Cd analysis (n=8); for other cases (n=5). Unit: mg kg-1

Soybean Yield and Its Components
Soybean yield and its components are indicated in Table 3. Average stem heights (n=8) were GL5 (59.7Ⓒ ISERD

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cm) < GL10 (66.8 cm) < GL40 (78.8 cm). Significant differences were recognized among the threemodels. Murakami et al. (2011) and Haque et al. (2014a, b) reported that in excess soil moisture
condition, soybean plants do not grow well after the germination and result in low yield. A similar
result was obtained in this study that the high groundwater level conditions suppress the growth of thestem.
The averages of the stem diameter and the number of seeds per pod (seed/pod) did not show any
significant difference. The average of the branch number showed little significant difference between
GL10 and GL40. However, there were significant differences between GL5 and GL10, and also
between GL5 and GL40. The averages of good seed weight per plant were GL5 (20.5 g) < GL10 (36.2g) < GL40 (56.3 g), showing significant differences among them. Averages of 100 seeds weight also
showed a similar trend as the good seed weight. The good seed weights of GL5 and GL10 models
lowered by about 36 % and 64 %, respectively, compared with that of GL40 model, which suggested
that even a slight difference in the groundwater level can bring a critical effect on the soybean yieldunder a high groundwater level condition. According to Shimada et al. (1995), it is important to control
the groundwater level according to the rain condition in actual paddy fields. Arihara (2000) reported
that the soybean yield was highest in the fields with a 40-50 cm groundwater level. His finding was
based on the investigation on the relationship between groundwater level and soybean yield.
The soybean yield in this experiment using Cd contaminant soil was higher under the low
groundwater level condition and lower under the high groundwater level condition.
Table 3 Soybean yield components of three different groundwater levels
Model
GL 5cmStem height(cm)
59.7±6.3a

GL 10cm

66.8±3.8bStem diameter(cm)
7.1±0.9a
7.6±0.8abBranch No.

Seed/Pod

3.6±0.9ab

5.1±0.8

1.6±0.2a

100 seed wt.
(g)28.3±2.3aGood seed wt.
(g)20.5±8.9a

1.6±0.2a

37.2±2.1b

36.2±6.3b

GL 40cm
78.8±5.2c
8.5±0.7b5.5±1.1b
1.6±0.1a
40.0±1.8c
56.3±4.7c
Note: Small letter indicates significant difference at 5% level according to Turkey-Kramer test; ± shows standard
deviation. Seed weight at 15% moisture. In all case (n=8).

CONCLUSION
Soybean was cultivated in containers using Cd contaminant soil (concentration:2.27 mg kg-1, thickness:
25 cm) under groundwater levels of 5 cm, 10 cm, and 40 cm with measuring the oxidation-reduction
potential in the soil. Soil was in oxidation condition above the groundwater level and in reduction
condition below it. Cd and Cu concentrations of stems and seeds were found to be lowered under ahigher groundwater level condition. Under a higher groundwater level condition, Cd concentration inroots showed a low value but that of Cu showed the opposite result. It was confirmed, as earlier studies
had reported, that growth and yield of soybeans were good when the groundwater level was low.
Controlling groundwater level can be one of the simplest and most economical methods for reducing
the Cd and Cu uptake by soybean plants. When we apply this method on site, relief well will beavailable for controlling ground water level. This can help minimizing toxic metals uptake from
polluted soils of soybean cultivated fields with high groundwater level in developing countries.
ACKNOWLEDGEMENT
The authors would like to thank Hiroaki Hasegawa, Jinhun Fan, Hideki Takahashi for their cooperation
throughout this research. In addition, we appreciate the support of this research by grants from theⒸ ISERD

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Faculty of Agriculture and Life Science, Hirosaki University and JSPS KAKENHI Grant Number
JP15K18756.
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