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Prediction of Heavy Metal Uptake by Different Rice Species in Paddy Soils near Contaminated Sites of Taiwan
Horng-yuh Guo1, Tseng-sen Liu1, Chian-liang Chu1, Chi-feng Chiang1
and Paul-Frans Römkens2
1Taiwan Agricultural Research Institute
189 Chung-cheng Rd., Wan-feng, Wu-feng,
Taichung 41301, Taiwan ROC
2Alterra, Dep. of Soil Science,
Wageningen UR. PO Box 47, 6700 AA Wageningen,
the Netherlands, 2009-04-08

Abstract

The quality of rice has become a social-economic issue in Taiwan due to soil pollution. In this study, eight sites of polluted farmlands located at Chang-hua, Ho-mei and Lu-kang were selected for cultivation of 12 selected cultivars, including the three most commonly grown varieties in Taiwan which are japonica, indica, and sticky rice. Results showed that soil properties have distinct and different effects on rice quality and variety. These new insights between the relationship of the quality of soil and of food should be used by soil environmental scientists around the world to improve scientific methods, provide tools to estimate risks, set soil standards and reduce the uptake of heavy metals by rice. Key words: Taiwan paddy soil, cadmium, rice, japonica, indica, aqua regia, CaCl2, soil quality, rice cultivars, heavy metals in soil, risk map, effect of soil pH

Key words: Taiwan paddy soil, cadmium, rice, japonica, indica, aqua regia, CaCl2, soil quality, rice cultivars, heavy metals in soil

Introduction

Due to physical and social environmental conditions, paddy rice is the major crop in Taiwan. Although the consumption of grained rice has decreased over the last few years, it still equals to 48.6 kg (or 53.3% of stable food) per capita in 2005 (COA 2006). This implies that the quality of the rice has a profound impact on the total exposure of human beings to, among others, heavy metals. Due to industrialization, urbanization and the increase of traffic, soils have become polluted all over the world which raised concern on food safety and quality, including Taiwan. To avoid unacceptable exposure of people to contaminants, safety limits on food was set. The allowed maximum level of cadmium content in edible brown rice was 0.5 mcg kg -1 for the past year; the new maximum level of edible brown rice has been reduced to 0.4 mcg kg-1 in 2007. In Taiwan, several cases have been reported, wherein, the quality of rice did not meet the international standards. These have affected the consumer faith regarding the quality of rice in Taiwan.

In 1991, the Taiwan agricultural authority had surveyed 341 local brown rice samples with heavy metals. Average levels of heavy metals are: arsenic 0.17 mcg kg -1, cadmium 0.07 mcg kg -1, chromium 0.16 mcg kg -1, copper 2.48 mcg kg -1, mercury 0.001 mcg kg -1, nickel 0.54 mcg kg -1, lead 0.43 mcg kg -1 and zinc 39.2 mcg kg -1 (Lin 1991).

Recently, Taiwan FDA has analyzed 73 and 93 brown rice samples for heavy metals during the first and second crops in 2003 (Chang et al. 2003). The average levels of metals reported were: 0.05 mcg kg -1 cadmium (ranging from below detection to 0.28 mcg kg -1), 0.003 mcg kg -1 mercury (below detection to 0.009 mcg kg -1), and 0.03 mcg kg -1 lead (below detection to 0.15 mcg kg -1) (Watanabe et al. 1996). This showed that the lowest and highest geometric means of Cd contents in rice from Asia ranged from 2.67 to 55.7 mcg kg -1. Values for rice grown outside of Asia are 0.88 to 132.20 mcg kg -1 respectively. These data show that average quality of rice is good. However, due to regional soil pollution, rice grown in specific areas (including the ones studied here) is of poor quality and the cadmium level in the rice is likely not to meet the national standards for cadmium in brown rice.

Taiwan government has taken various actions to considerably reduce the impact of heavy metals upon human health and the environment. Since 1982, different surveys of contaminated soils have been conducted by EPA of Taiwan. Finally, polluted farmlands with Grade 5 level of heavy metals has been recognized in 2002. The arable lands of Taipei, Tao-yuan, Taichung, Chang-hwa, Tainan and Kaohsiung are extensively contaminated with heavy metals for a long time as a result of the high density of industries within the farmlands (EPA 2002). Cd, Pb, Zn, Cu, Cr and Ni are the most serious contaminants in the paddy rice fields and occur in the vicinity of irrigation channel or drainage ways. A total of 319 hectares of farmland have been completely surveyed and identified.

The environmental response authorities should conduct soil remediation activities in accordance to the Article of the "Soil and Underground Water Remediation Act". Also EPA provided a provisional soil remediation guideline which involves the mixing of the polluted topsoil with the subsoil below. For farmlands with elevated levels of chromium, copper, nickel, and zinc, soil turn-over and dilution is an option. It is however necessary to also reduce the inputs of contamination to the soil, otherwise, the topsoil will become polluted again after some years.

Other proposed methods include acid washing or heat treatment which is suitable for soils contaminated by cadmium, lead, and mercury. Some other treatment methods like the replacement of polluted soil by clean soil or a combination of different methods were proposed as well (EPA 2004). Despite the efforts made and costs involved (the whole project costs were estimated 10 million US dollar) rice samples were still found to not meet the food quality standard this year. The main reason for this is that even at moderate or low pollution levels, uptake by certain rice cultivars can be high. Also, the impact of soil acidity, which is not considered in the soil test, plays an important role. Ideally, soil standards that protect the quality of food should consider these issues as well. At present, there is a lack of information on how to incorporate the so-called availability of contaminants in soil policy. This study aims to investigate the differences between species and the relation between the availability (rather than the total amount in soil) and quality of rice.

Heavy Metals and Food Safety: The Concept of Availability in Relation to Plant Uptake

Chaney (1980) introduced the concept of the "soil-plant barrier" and classified metals into four groups. Ag, Cr, Sn, Ti, Y and Zr were classified as the Group I elements, which pose little risk because they are not taken up to any extent by plants, which is mainly due to their low solubility in soil and, consequently, negligible uptake and translocation by plants. Group II includes the elements As, Hg and Pb which are strongly adsorbed by soil colloids. And while they may be absorbed by plant roots, they are not readily translocated to edible tissues, and therefore pose minimal risks to human health. Group III is comprised of the elements B, Cu, Mn, Mo, Ni and Zn, which are readily taken up by plants. They are phytotoxic at concentrations that pose little risk to human health. Group IV consists of Cd, Co, Mo, and Se, which pose human and animal health risk at plant tissue concentration that are not generally phytotoxic. The elements that have most commonly given rise to health concerns about food safety are the heavy metals Cd, Hg and Pb, together with the anionic metalloids As and Se (Reilly 1991).

To be available for uptake by plants, heavy metals must be present in the soil solution. There is considerable evidence that the chemical specification of heavy metals in solution affects their availability and toxicity to plants (Parker et al. 1995). For example, Cu 2+ (Graham 1981) and Cd 2* (Cabrera et al. 1988) have shown high level of correlation with the activity of free metals ions in soil solution rather than with total elements concentrations in soils when plants uptake these metals. Soluble heavy metal concentrations in soils are likely to be influenced to some extent by the total concentrations of heavy metals present in soils. Thus, in uncontaminated soils, heavy metal bioavailability is likely to be related to the nature of the soil parent material and the degree of soil weathering (McLaren 2003). In case of contaminated soils, solutions of heavy metal concentrations are likely to increase with total contaminant loading. Colloids in soil that are able to absorb heavy metals will therefore have a major influence in controlling heavy metal availability to plants. Soil organic matter has a large capacity to absorb or complex heavy metals. In many studies, organic matter has shown to be a dominant soil constituent affecting sorption a few decades ago, e.g., for Cu (McLaren and Crawford 1973), Cd (Gray et al. 1998) and Hg (Yin et al. 1996). Heavy metals may also be absorbed by clay minerals and oxides of Fe, Al, and Mn, but these may play a relatively minor role in maintaining solution of heavy metal concentrations compared to the overriding dominance of soil organic matter. The lack of significant correlations between heavy metal sorption and soil clay and oxide contents could be due to the low amounts of these constituents.

Soil pH has also been recognized as having a major influence on the availability of heavy metals that occur predominantly as cations (Cu 2+, Co2 +, Pb 2+, etc.). The availability to plants is highest in acid soils, and decreases as the soil pH increases due to sorption onto soil colloids or development with dissolved organic colloids.

The influence of soil pH on heavy metal availability is related to its effect on the reactions of controlling heavy metal concentrations in the soil solution. Under acid conditions, sorption of heavy metal cations by soil colloids is at a minimum, and the solution concentrations are relatively high (McLaren, 2003). As soil pH rises, sorption of heavy metal cations increases and the solubility of oxides decreases. The sorption of heavy metals that occur in anionic forms decreases with increasing soil pH, and hence solution concentrations and availability increase.

In the Belgian-Dutch border called "de Kempen", for example, total cadmium levels in soils usually range between 1 and 4 mcg kg -1 which is below the level required for clean-up. Due to the low soil pH and the soil type (mostly acidic sandy soils with low organic matter content), the uptake of the crop is high. At present, the crop quality therefore does not meet the standards for human consumption (vegetables) or animal food (in case of grass and maize). The major reason for the high uptake crops is the high availability of the cadmium in the soil due to the low pH. Considering the impact of soil type (including pH, and soil properties like organic matter, clay etc.) is therefore of importance to obtain soil quality standards that aim to protect food quality (Römkens, 2005; Brus et al. 2005) by considering effects of pH and other important soil properties.

Cadmium is one of the main pollutants in paddy soil near industrial areas and can be adsorbed and transported effectively by rice plants (Shah et al. 2001). Levels of most contaminants, except Cd, have rarely caused concern that is sufficient to require changes in agronomic practice to minimize food-chain contamination. Compared to the other heavy metals, cadmium is relatively mobile and bioavailable in soils, so that transfer through the food chain is a major risk pathway (Australian government 2005). As a consequence; it is harmful to human health. Also, it is potentially toxic to biota at low concentration (Das et al. 1997).

It is generally believed that the chemical form of cadmium taken up by plants is the free uncomplexed Cd 2+ ion present in soil solution. Any treatments or changes in soil conditions which affect the concentration of the Cd 2+ ion will therefore affect plant accumulation of cadmium. Table 1(1048) summarizes the factors listed by Chaney and Hornick (1978) that affect plant uptake of cadmium. This is also used by the Australian government (2005).

Rice Varieties and CD Uptake

Many reports showed that rice cultivars varied significantly with regard to Cd uptake and accumulation. Morishita et al. (1987) reported a comparative study on cadmium uptake by several rice cultivars in Andisols with a low total cadmium concentration in soil (0.102 mcg kg -1) in 1983 and 1985. It was observed that japonica brown rice varieties have the lowest average uptake rate compared to the other three varieties namely, javanica, indica and Hybrid. Average cadmium levels in brown rice ranged from 2.1 to 27.0 mcg kg -1 among 28 japonica varieties and from 4.1 to 55.5 mcg kg -1 among 23 indica varieties. Arao and Ishikawa (2006) reported that 49 varieties of rice were cultivated in Cd-polluted soils, the japonica varieties were categorized into the low grain Cd group. Several indica or indica-japonica varieties accumulated considerable amounts of Cd in grains as well as in straw.

Some reports from China, however, seem to have an opposite result and indicated that indica varieties have lower uptake rates of cadmium compared to japonica varieties. Liu et al (2003) conducted a study on 20 rice cultivars of different genotypes and origins by adding 100 mcg kg -1 cadmium to the soil. The result showed that the effects of Cd on rice growth and development varied greatly among cultivars. Some varieties were highly tolerant to soil stress imposed by cadmium, while others were very sensitive. Differences existed among the cultivars for Cd uptake and distribution of rice plants, but the difference were not necessarily related to rice genotypes.

Liu et al. (2007), in an attempt to understand certain mechanisms causing the variations between rice cultivars with regard to Cd uptake and accumulation, conducted pot soil experiments with two rice cultivars at different levels of Cd, i.e., 0 (the control), 10, 50 mcg Cd kg -1 soil. The results showed that the rice cultivar with higher concentrations of LMWOA (low-molecular-weight organic acids) in soil accumulated more Cd in the plants. The results indicate that LMWOA secretion by rice root, especially in Cd-contaminated soils, is likely to be one of the mechanisms determining the plant Cd uptake properties of rice cultivars.

Soil Assessment

At present, the quality of soil in Taiwan is measured by its total metal content. This of course is a very practical and robust approach. Soil samples can be stored since the analysis is not affected by drying or other soil treatments. However, it has been shown that the total metal content in the soil and the uptake by arable crops are not always related to each other. In some soils, the uptake of metals like cadmium is high even though the total metal content of the soil is low, even far below the current soil clean up values. After evaluating a range of different soil extractants such as weak electrolytes, organic acids, dilute mineral acids, chelating agents, ion-exchange resins and combinations of some of these, European countries propose to use extracts in dilute solutions of CaCl 2 for assessing plant available Cd (Salt and Kloke 1986). However, there is no agreement on the optimal soil/solution ratio, extraction times and concentration of CaCl 2 (0.01-0.1 mM). Also, at present there are no `standards' for cadmium measured in 0.01 M CaCl 2. To evaluate the soil quality, one has to be able to compare the measured amount in the extract to a standard just like the control or action level. In the case of rice cropping this means that the study should allow deriving such `critical levels' to which the food quality does not meet the food standards anymore.

In this study, to specifically derive soil quality standards for arable soils, the following points have to be considered:

  • 1. Study the uptake of metals by different rice varieties: the relationship between the soil and the crop therefore has to be established for all relevant cultivars
  • 2. Study the relationship between the availability of cadmium in the soil as measured by CaCl 2 and the uptake of the different rice varieties. Here we will test if such relationships exist and can be used to predict the uptake of cadmium by rice
  • 3. Apply the results to make risk maps showing areas where the soil quality is insufficient to grow rice that meets the food quality standard.

Materials and Methods

All experiments were carried out in existing paddy fields. In total, 8 different sites of heavy metals polluted (controlled sites by EPA) farmlands located at Chang-hua city (CH), Ho-mei town (HM) and Lu-kang town (LK) (24°05'N., 120°30'E) were selected to study the quality of soil and rice in 2005 ( Table 2(1387)).

In the Chang-hwa area, many existing paddy fields are known to be polluted by heavy metals. Pollution with metals like chromium, copper, nickel, cadmium and zinc is related to emission by industry in the Chang-hwa region.

Soil samples were collected from the root zone of each plant. It is important to take the soil and crop samples from the same location in order to derive the relationship between soil quality and uptake by rice. Since the degree of pollution varies considerably within each field, 9 different sampling plots were established within each field along the pollution gradient. Because the uptake of different cultivars is also quite variable, each of the 9 sampling plots were further divided into 12 sub-sampling plots, one for each cultivar. In total 108 (9 x 12) soil and rice samples were thus collected from each field.

After collection of the soil and plant material (plants were harvested prior to the normal harvest time) the soil samples were air-dried, and sieved on a 2mm sieve prior to analysis. Because the soil samples were collected from the root zone, they contain slightly more organic matter than what is commonly observed in these soils. The basic soil properties of 8 plots of Chang-hwa region are shown in table 2.

In 2006, 4 additional sites of heavy metal-polluted (controlled sites of EPA) farmlands located at Tou-yuan (24°58'N., 121°18'E.) and Hsin-chu city (24°48'N., 120°56'E.) were included to study the impact of highly polluted soil (Cadmium) on cadmium uptake by rice. The sample collection and analysis procedures were similar to those described earlier for the Chang-hwa region. The soil properties of 4 plots of Tou-yuan and Hsin-chu region are described in Table 3(1103).

Bioavailability of Heavy Metals in Soils

For heavy metals bioavailability measurement, the soil samples were extracted by 0.1M HCl, 0.43 M HNO 3, 0.05M EDTA, and 0.01M CaCl 2 solution in a 1:10 soil: extractant ratio. All extracts were obtained after shaking for 1 hour and filtration through Whatman No.42filter paper. Heavy metal concentrations in the filtrates were determined by ICP-AES+Ultrasonic Nebulizer. The soil's total heavy metal content was determined by aqua regia. Soil samples were heated in a microwave furnace according to standard methods, filtered, and analyzed for Cd, Cr, Cu, Ni, Pb, Zn by ICP-AES.

Rice Plant Tissue Analysis

In 2005 and 2006, 12 cultivars of rice (as shown in Table 4(1120)), including the three major rice varieties that are presently cultivated in Taiwan namely japonica and indica species and sticky rice, were included in the study. The amount of N, P and K fertilizers were applied according to standard methods and regulations of the fertilizer guidebook used by the farmers. Whole rice plants with root zone soils were harvested at maturity stage. After each root zone soil was sampled, the plants were washed thoroughly three times with tap water and three times with de-ionized water. The roots, stems, leaves, and grains were separated. The roots, stems and leaves were oven-dried at 70°C overnight. The grains were oven_dried at 60°C. The grain husks were removed mechanically using standard equipment. To avoid contamination while grinding the plant material, the oven-dried plant tissues were ground with pure titanium knives in standard grinders to reduce the size of tissue samples. The Cd, Cr, Cu, Ni, Pb, and Zn concentrations of the samples were determined by ICP-AES following HNO 3-HClO 4 (4:1) digestion procedures.

Data Analysis

Data were analyzed using Windows EXCEL 2000 and SURFER 7.0 (Golden software, Inc., USA) for geo-statistical mapping.

Results and Discussion

Bioavailability of Cadmium in Soils: WHY Use Cacl2?

The uptake of metals from soil is related to the difference in the availability. The differences in the availability of elements in soil are explained not only by the metal content but also to the difference in soil pH, organic matter, texture, etc. The CaCl 2 extractable Cadmium is representative for such an available fraction. Usually this amount is much lower compared to the total (Aqua Regia) extractable cadmium. However, there is no single extract that represents the true availability for all plant species and the search for a universal extract therefore is futile. Nevertheless it is believed that certain extracts like CaCl 2 are at least a good estimate for a number of species. Many other extracts have been investigated by soil scientists, trying to link the soil quality to the uptake by plants, but most of these were chemically much `stronger' which means they are capable of extracting a higher amount of metals from the soil than is actually available to plants. An `ideal' extract should therefore mimic the conditions that prevail in the soil solution. A dilute CaCl 2 extract is considered to be comparable to soil solutions in terms of ionic strength and ion composition in real soil solutions. It also does not affect soil pH too much which is important since soil pH has a large effect on the availability.

The cadmium contents of soils samples from the Chang-hwa region were extracted by 0.1M HCl, 0.43 M HNO 3, 0.05M EDTA, 0.01M CaCl 2 solution and compared with that of digested by aqua-regia. The maximum, minimum, median, average and standard deviation value are shown in Table 5(1349). Usually soil cadmium contents measured by aqua regia have the highest value and extracted by 0.01M CaCl 2 have the lowest value among these extracting methods. The amounts measured by 0.1M HCl, 0.43 M HNO 3, 0.05M EDTA are rather similar. The results are shown in Table 5(1349).

The correlation matrix of the soil cadmium concentration extracted by aqua regia, 0.05M EDTA, 0.1M HCl, 0.43M HNO 3, and 0.01M CaCl 2 is shown in Table 6(1104). This analysis shows that 0.05M EDTA, 0.1N HCl, 0.43M HNO 3 extraction methods and aqua regia digested method significantly correlated with one another, but 0.01M CaCl 2 has a very low correlation with the other 4 methods. This is due to the fact that the amount extracted by CaCl 2 strongly depends on the pH of the soil. Two soils with a similar total cadmium content (aqua regia) but different pH will also have a different amount of cadmium extracted by CaCl 2 ( Table 7(1319) and Fig. 1(1205)).

The fact that there is a close correlation between 0.1 M HCl, 0.43 N HNO 3 and 0.05 M EDTA, indicates that these methods are equally strong in their capacity to extract cadmium from the soil. Usually the amount extracted by either one of these three methods is lower than the amount extracted by aqua regia. The difference between the amount extracted by cadmium and these three (HCl, HNO 3 or EDTA) is considered to be rather unavailable. This part of the cadmium in the soil is included in minerals or other soil particles and is not available for plant uptake or leaching. It is also called the `non-reactive' fraction in contrast to the amount extracted by 0.1 M HCl, 0.43 N HNO 3 or 0.05 M EDTA which are representative for the amount of cadmium in the soil that is adsorbed onto soil colloids but is in equilibrium with the soil solution. The `reactive' fraction is the amount that controls the cadmium concentration in the soil solution together with pH, organic matter and clay content.

Table 7(1319) shows that the soil organic matter content is highly correlated to CEC as has been found many times. In most soils, organic matter is an important factor controlling CEC since it has a high surface charge density. It also shows that the 0.01 M CaCl 2 extractable Cd concentration is significantly negatively correlated to soil pH, but there is no obvious relation with CEC and the organic matter content in the soil. This reflects the pH dependent availability of cadmium, with availability increasing at low pH. On the other hand, Aqua regia extractable Cd is slightly positively correlated to soil organic matter and CEC, but there is no relation with soil pH. This is due to the fact that cadmium in these soils is predominantly bound to organic matter. So in a soil with high organic matter content, more cadmium is retained. Another explanation is that the majority of cadmium in these soils is from organic material supplied by the irrigation water.

As stated before, the uptake of cadmium by plants is related to several factors including Cd Tot, Cd CaCl2 and soluble Cl which are usually positively correlated to uptake. In most soils' pH, organic matter and cation exchange capacity is negatively related with uptake, whereas P and Zn are either positively or negatively related depending on the levels present in soil (Haghiri, 1974; MacLean 1976; Williams and David 1977; Whitten and Ritchie, 1991; McKenna et al. 1993; Li et al.1994; and McLaughlin et al. 1994.).

Usually the availability of cadmium is crucial and to assess whether or not cadmium in these soils is controlled by soil properties, the relationship between pH on one hand and the ratio of Cd-CaCl 2 and Cd-aqua regia on the other was established. The latter ratio is called the distribution coefficient and is a measure of the distribution between cadmium adsorbed on the soil and that in solution. It can also be described as a measurement of the availability of cadmium in soil.

The relationship of soil pH and log Cd CaCl2/Cd Tot of Chang-hwa soils is shown in Fig.1. It can be shown that the data for the first and second harvest are presented separately. The results indicate that there is no difference in the relationship between cadmium in the soil, in the solution and pH for the two harvesting periods. The coefficient of the slope of approximately -1 indicates that with an increase in the pH with one unit, the concentration of cadmium in the soil solution decreases with a factor of 10. To construct fig. 1, 0.43 N HNO 3 extractable cadmium content was used. The soil cadmium activity and pH relationship in Hsin-chu and Tou-yuan area has a similar trend as well as the samples from the Chang-hwa region. But the trend is less pronounced due to the limited variation in soil pH.

Soil pH clearly affects the availability of Cd (Williams and David 1976). Increasing the soil pH reduces the concentration of Cd in the soil solution and consequently Cd uptake by vegetables (MacLean 1976). The data shown in figure one suggest that pH may be the principal factor which controls the proportion Cd CaCl2/Cd Tot between the soils. The untransformed data show that changes in soil pH to below pH 5 caused a rapid shift in the availability of Cd. Data in Fig. 1(1205) indicate that Cd availability could be reduced by increasing soil pH by liming or other soil amendments which can increase soil pH. Soil pH management can be applied to control soil cadmium availability in acid region. Mench et al. (1998) increased soil pH values from 5.7 to 7.6 using basic slag in Chromic Luvisols over Jurassic lime stones which resulted in a decrease of the Cd content in wheat grain from 0.14 to 0.05 mcg Cd kg -1 DW.

Heavy Metals in Soil

A special characteristic of the paddy rice fields is that the heavy metal content across the fields have high spatial variability. This is the main reason why the soils were sampled in a grid. Each grid was between 5 and 14 m 2 (size ranging from 5 to 7 m in length and 1 to 2 m in width), the exact cell grid size was depended on the actual plot size. Within each field, paired soil and plant tissue samples from 108 plots (9 sub plots x 12 cultivars) were analyzed. The concentrations of aqua regia digested heavy metals in the fields as shown in Table 8(1131) and Table 9(1015). In the Chang-hwa area, Cu, Cr, Ni, Zn were the main pollutants, because of the vicinity of metal plating industry in this area during the past decades. In the Hsin-chu plots, Cd, Cu, Cr, Zn were the main elements of concern whereas in the Tou-yuan fields, Cd, Cu, Pb of effluents from nearby electronics industries caused high levels in the soil.

Data in Tables 8 and 9 indicate that the level of heavy metal between fields can vary widely. According to the observation from geo-statistical maps (not shown here), the pollutants seem to have come from irrigation inlets or drainage outlets or side contamination. In some cases, illegal effluents from nearby factories containing extremely high pollutant levels have resulted in the distribution of contaminants across the fields. Sometimes heavy rainfall causes the drainage ways to overflow with waste water which has also contributed to the pollution of the soil in the fields. It was observed that Ni and Pb had especially greater variation coefficient across the fields compared to the other elements. On the other hand, Cd, Cu and Zn seem to be distributed less differently across the field but a large difference between levels within a field nevertheless could be found in some cases.

Tables 10 and 11 show the heavy metal levels for the brown rice cultivars studied in the Chang-hwa region in 2005. Tables 12 and 13 show the heavy metal levels for the brown rice cultivars studied in the Hsin-chu and Tou-Yuan region for the 1 st crop in 2006. Due to the sample preparation, lead contamination had occurred and the data for lead were therefore omitted from the tables.

For all the fields, it was observed that rice cultivars of indica genotype have higher concentrations of cadmium than those of japonica. In contrast to cadmium, japonica genotype rice varieties seem to have higher lead levels than indica genotypes, at least in the Tou-yuan plots.

The rice concentrations in the majority of samples from the Chang-hwa plots meet the new FDA criteria of rice for cadmium which is 0.4 mcg kg -1. In several fields in the Chang-hwa area, however, the indica genotype does not meet the 0.2 mcg/kg WHO standard for cadmium in brown rice. Due to the very high cadmium levels in the soils of the Tou-yuan plots, sometimes in combination with low pH levels, all cultivars failed to meet the 0.2 mcg kg -1 cadmium control level of brown rice. But some cultivars, especially the japonica, do meet the new FDA standard for cadmium.

It was also observed that the 2 nd crop of brown rice on the average had higher cadmium content than that of the 1 st crop. This increase in uptake might be related to the higher temperatures during the growing season of the second crop of that year.

Two cultivars of japonica genotype could not meet the FDA standard for lead, based on the average level found across the fields. The high variability of cadmium across the fields caused a high variability in the uptake by rice as well. But since zinc and copper levels in the soil also increased, this resulted in an effect on cadmium uptake. In soils with a high zinc or copper content, the uptake of cadmium was lower, which made the relation between soil cadmium and cadmium in the rice more complex. The interference of copper and zinc with cadmium is one of the reasons why high cadmium content in the soil does not automatically lead to a high cadmium uptake by rice as well.

The correlation matrix of cadmium concentration in the different tissue parts of rice is listed in Table 14(1099). It indicates that the cadmium concentration in roots have very low relationship with that of the other tissue parts of rice, whereas stems, leaves and brown rice have a very high relationship with the others.

Table 15(1097) shows that the cadmium concentration of roots has a very high relationship with the weak acid extracts and aqua regia except with CaCl 2 extraction. This suggests that the cadmium in the soil is highly related to the cadmium content adsorbed to the root. Another explanation is that the roots still contain small soil particles. However, the uptake by the plants is not related to the total cadmium anymore but only to the available fraction in the soil which is measured by the CaCl 2 extraction. This fraction is the one that can actually be taken up by the plants (see also next paragraph).

Availability of Metals in Soil in Relation to Uptake by Crops

The relationships that link cadmium in the soil to the cadmium in the plant are based on the generally accepted view that metals are taken up by the plant from the soil solution. This means that ideally there is a relationship between the metals in the soil solution (concentration or free metal ion activity) and the heavy metal levels in the plant (Brus et al, 2005). Usually this relationship is described using log-linear equations ( Fig. 2(1106)), wherein the concentration of the metals equals that of metals available in the soil solution. The concentration in the soil solution, however, is difficult to measure and often extracts are made using a dilute salt solution to extract the amount of metals from soil that are believed to be in the soil solution. A commonly used extract is 0.01 M CaCl 2. The metals measured in a 1:10 soil:solution extract using 0.01M CaCl 2 is believed to be a realistic estimate of the soil solution concentration. Using data from different soils that reflect a wide range in soil properties and degree of contamination, the so-called "soil-plant relationship" can be derived through regression analysis. In this study, the measured concentration of metals in different plant compartments (roots, leaves, grains) is related to the measured concentration in the soil solution (extract). The values of á and â can be derived from experimental data by linear (multiple or stepwise) regression after log transformation of the data. Sometimes also the pH of the soil solution can be used as an additional explaining variable.

In most cases however, data on the soil solution are not available. Of course if a clear relationship between the concentration of metals in a specific extract like 0.01 M CaCl 2 and the plant is obtained, the direct measurement of CaCl 2 extractable metals can be used as an indicator of the soil quality. Once the relationship between CaCl 2 extractable metal and plant has been established, screening of soils using CaCl 2 can be used to predict what the levels in the rice will be.

However, in many cases, screening of soils is still (and will be) based on the determination of the total metal content. Usually, soil data like organic matter, clay and pH are also available. These data can also be used to predict the uptake of metals by rice because there is a close relationship between soil properties and the metal content in the soil and the concentration in the soil solution (Römkens et al. 2004) ( Fig. 3(1117)).

The addition `1' indicates that a and b in equation [2] differ from those in equation [1]. "OM" stands for organic matter, `clay' for the percentage < 2mm. Also CEC can be used if available since, like OM and clay, CEC represents the binding capacity of the soil. Fig. [1] shown earlier already indicates that for the soils studied here, the concentration in the soil solution indeed can be predicted by an equation like equation [2]. Once relationship [1] and [2] have been established, the quality of rice from other sites that were not included in the study can be estimated. Of course it should be kept in mind that the model is valid only within the range of soil properties and contamination levels that were used to derive the model. If, for example the highest cadmium level in soil samples in the database is less than 2 mcg kg -1, the model cannot be used to predict uptake from soils that contain 15 mcg kg -1.

Finally equation [1] and [2] can be combined to predict the uptake by rice directly from soil properties without having to measure the soil solution (de Vries et al. 2007) ( Fig. 4(1138))

Again, the values for coefficient a 2, b 2 etc. in equation [3] will be different from those in equation [2].

The regression equations to predict cadmium uptake by brown rice from soil properties according to equation [3] are presented in table 16. The predicted cadmium content in several varieties calculated are compared to the measured ones in figure 2. Different extracts for cadmium in soil were used to predict the uptake by rice which in this case were aqua regia (data not shown), CaCl 2 ( Fig. 5(1092)) and 0.1M HCL (data not shown). The results indicate that the prediction of brown rice of cadmium concentration, considering soil pH, OM, CEC and Cd extracted by 0.01M CaCl 2, is not always satisfactory. This means, there are other soil factors or management activities that control the uptake of rice that need to be considered. In general however, the variability in the uptake of cadmium by rice can be explained well compared to standard methods that consider the metal content of the soil only.

Despite the fact that some of the models clearly need to be improved, some experimentally derived models were used to calculate the so-called "risk map" for rice cropping. This was done by calculating the critical levels of cadmium in the soil above where the rice cadmium content exceeds the food quality standard. The soil database from Taiwan was used to compare this critical level with actual measured values across the country. The areas where the actual cadmium content is lower than the critical cadmium content are marked in red. This means that in these areas, the quality of rice will probably not meet the food standard ( Fig. 6(1147)). The result indicates that this areas exist where the quality of indica species will be insufficient (ie cadmium in the rice will exceed the standard of 0.2 or 0.4 mcg kg -1). Such areas include soils derived from marine sediment as well as polluted soils. One of the options that are easy to implement by farmers is to grow japonica genotype rice in these regions.

Conclusions

The results from this study clearly demonstrate that the uptake of heavy metals, especially cadmium, is related to the availability in soil. In the soils studied in 2005 and 2006, the availability was mainly controlled by soil pH and the total cadmium content of the soil. The availability can be measured quite accurately by 0.01 M CaCl 2. Using a combination of soil properties including pH, organic matter and CEC, the actual uptake by rice for different cultivars can be predicted well although the fit is different for different species. The results also show that in soils with low cadmium content, even below the current monitoring (2 mcg kg -1) or action value (5 mcg kg -1) used in Taiwan, the uptake of cadmium by indica species is too high. The quality of the rice does not meet the WHO or the FDA standards although the soil quality, according to the current soil quality standard, is sufficient. This clearly illustrates the need for a revision of current standards used in Taiwan. A distinction between indica and japonica species is necessary since indica species have high uptake and should not be cultivated on soils containing more than 0.4 to 1.0 mcg kg -1 cadmium. In contract to this, some japonica cultivars can be grown safely on soils that contain more than 5 mcg kg -1. Further testing of the relationship between soil quality and uptake by rice is necessary to improve the development of soil quality standards that may protect the general population from exposure due to cadmium uptake by rice.

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    . Factors affecting cadmium uptake by plant from soil (Australian government 2005) . Soil properties of the sites at Chang-hwa (2005) . Soil properties of the sites at Tou-yuan and Hsin-Chu included in the study in 2006 . The cultivars of rice used in the experiments in 2005 and 2006
    . Soil Cadmium concentration extracted by aqua regia, 0.05M EDTA, 0.1N HCl, 0.43M HNO 3 and 0.01M CaCl 2 (all in ?g kg-1); data from 2005 only (Chang-hwa) . Correlation matrix of the soil cadmium concentration for aqua regia, 0.05M EDTA, 0.1M HCl, 0.43M HNO 3, and 0.01M CaCl 2 extraction methods . Correlation matrix of Cd concentrations in different extracts versus soil properties . Total heavy metal content in the root zone soils in Chang-hwa plots, average of 1 st and 2 nd crops, 2005 in mcg kg -1 . Total heavy metal content in the root zone soils in Tou-yuan and Hsin-chu plots, 1 st crop, 2006 in mcg kg -1 . Heavy metal concentration (mcg kg -1) of brown rice in Chang-hwa region, 1 st crop 2005. Italic values indicate levels > 0.2 mcg kg -1 (WHO standard); values in bold indicate levels > 0.4 mcg kg -1 (FDA standard); values in bold underlined indicate
  • that the average is > 0.4 mcg kg -1 . Heavy metal concentration (mcg kg -1) of brown rice in Chang-hwa region, 2 nd crop 2005. Italic values indicate levels > 0.2 mcg kg -1 (WHO standard); values in bold indicate levels > 0.4 mcg kg -1 (FDA standard); values in bold underlined indicate that the average is > 0.4 mcg kg -1 . Heavy metal concentration of brown rice in Hsin-chu plots, 1 st crop, 2006. Italic values indicate levels > 0.2 mcg kg -1 (WHO standard); values in bold indicate levels > 0.4 mcg kg -1 (FDA standard); values in bold underlined indicate that the
  • average is > 0.4 mcg kg -1 . Heavy metal concentration of brown rice in Tou-yuan plots, 1 st crop, 2006. Italic values indicate levels > 0.2 mcg kg -1 (WHO standard); values in bold indicate levels > 0.4 mcg kg -1 (FDA standard); values in bold underlined indicate that the average is > 0.4 mcg kg -1.

Index of Images

Table 2 Soil Properties of the Sites at Chang-Hwa (2005)

Table 2 Soil Properties of the Sites at Chang-Hwa (2005)

Figure 2 Log-Linear Equation [1]

Figure 2 Log-Linear Equation [1]

Figure 3 Log-Linear Equation [2]

Figure 3 Log-Linear Equation [2]

Figure 4 Log-Linear Equation [3]

Figure 4 Log-Linear Equation [3]

Table 1 Factors Affecting Cadmium Uptake by Plant from Soil (Australian Government 2005)

Table 1 Factors Affecting Cadmium Uptake by Plant from Soil (Australian Government 2005)

Figure 5 Measured Versus Predicted Cadmium Concentrations in Brown Rice Using the Equations Shown in Table 16 Based on Cacl<Sub>2</Sub> Extractable Cadmium. Indica Species Are Shown in the Right Hand Columns.

Figure 5 Measured Versus Predicted Cadmium Concentrations in Brown Rice Using the Equations Shown in Table 16 Based on Cacl 2 Extractable Cadmium. Indica Species Are Shown in the Right Hand Columns.

Figure 6 Example of a Risk Map for Cadmium for Cultivar Tainun Sen 20 Showing Areas Where Brown Rice Will Contain More Than 0.2 MCG KG<Sup>-1</Sup> CD. the Critical Cadmium Soil Concentration Is Equal to 0.4 MCG KG<Sup>-1</Sup>

Figure 6 Example of Risk Map for Cadmium for Cultivar Tainun Sen 20 Showing Areas Where Brown Rice Will Contain More Than 0.2 MCG KG -1 CD. the Critical Cadmium Soil Concentration Is Equal to 0.4 MCG KG -1

Table 3 Soil Properties of the Sites at Tou-Yuan and Hsin-Chu Included in the Study in 2006

Table 3 Soil Properties of the Sites at Tou-Yuan and Hsin-Chu Included in the Study in 2006

Table 4 The Cultivars of Rice Used in the Experiments in 2005 and 2006<BR>

Table 4 The Cultivars of Rice Used in the Experiments in 2005 and 2006

Figure 1 Relation between Soil PH and Log CD<Sub>Cacl2</Sub>/CD<Sub>Tot</Sub> in Samples from Chang-Hwa Area.

Figure 1 Relation between Soil PH and Log CD Cacl2/CD Tot in Samples from Chang-Hwa Area.

Table 5 Soil Cadmium Concentration Extracted by Aqua Regia, 0.05M Edta, 0.1N HCL, 0.43M Hno<Sub>3</Sub> and 0.01M Cacl<Sub>2</Sub> (All in ?G KG-1); Data from 2005 Only (Chang-Hwa)

Table 5 Soil Cadmium Concentration Extracted by Aqua Regia, 0.05M Edta, 0.1N HCL, 0.43M Hno 3 and 0.01M Cacl 2 (All in ?G KG-1); Data from 2005 Only (Chang-Hwa)

Table 6 Correlation Matrix of the Soil Cadmium Concentration for Aqua Regia, 0.05M Edta, 0.1M HCL, 0.43M Hno<Sub>3</Sub>, and 0.01M Cacl<Sub>2</Sub> Extraction Methods

Table 6 Correlation Matrix of the Soil Cadmium Concentration for Aqua Regia, 0.05M Edta, 0.1M HCL, 0.43M Hno 3, and 0.01M Cacl 2 Extraction Methods

Table 7 Correlation Matrix of CD Concentrations in Different Extracts Versus Soil Properties

Table 7 Correlation Matrix of CD Concentrations in Different Extracts Versus Soil Properties

Table 8 Total Heavy Metal Content in the Root Zone Soils in Chang-Hwa Plots, Average of 1<Sup>ST</Sup> and 2<Sup>ND</Sup> Crops, 2005 in MCG KG<Sup>-1</Sup>

Table 8 Total Heavy Metal Content in the Root Zone Soils in Chang-Hwa Plots, Average of 1 ST and 2 ND Crops, 2005 in MCG KG -1

Table 9 Total Heavy Metal Content in the Root Zone Soils in Tou-Yuan and Hsin-Chu Plots, 1<Sup>ST</Sup> Crop, 2006 in MCG KG<Sup>-1</Sup>

Table 9 Total Heavy Metal Content in the Root Zone Soils in Tou-Yuan and Hsin-Chu Plots, 1 ST Crop, 2006 in MCG KG -1

Table 10 Heavy Metal Concentration (MCG KG<Sup>-1</Sup>) of Brown Rice in Chang-Hwa Region, 1<Sup>ST</Sup> Crop 2005. Italic Values Indicate Levels > 0.2 MCG KG<Sup>-1</Sup> (Who Standard); Values in Bold Indicate Levels > 0.4 MCG KG<Sup>-1</Sup> (Fda Standard); Values in Bold Underlined Indicate

Table 10 Heavy Metal Concentration (MCG KG -1) of Brown Rice in Chang-Hwa Region, 1 ST Crop 2005. Italic Values Indicate Levels > 0.2 MCG KG -1 (Who Standard); Values in Bold Indicate Levels > 0.4 MCG KG -1 (Fda Standard); Values in Bold Underlined Indicate

Table 11 Heavy Metal Concentration (MCG KG<Sup>-1</Sup>) of Brown Rice in Chang-Hwa Region, 2<Sup>ND</Sup> Crop 2005. Italic Values Indicate Levels > 0.2 MCG KG<Sup>-1</Sup> (Who Standard); Values in Bold Indicate Levels > 0.4 MCG KG<Sup>-1</Sup> (Fda Standard); Values in Bold Underlined Indicate That the Average Is > 0.4 MCG KG<Sup>-1</Sup>

Table 11 Heavy Metal Concentration (MCG KG -1) of Brown Rice in Chang-Hwa Region, 2 ND Crop 2005. Italic Values Indicate Levels > 0.2 MCG KG -1 (Who Standard); Values in Bold Indicate Levels > 0.4 MCG KG -1 (Fda Standard); Values in Bold Underlined Indicate That the Average Is > 0.4 MCG KG -1

Table 12 Heavy Metal Concentration of Brown Rice in Hsin-Chu Plots, 1<Sup>ST</Sup> Crop, 2006. Italic Values Indicate Levels > 0.2 MCG KG<Sup>-1</Sup> (Who Standard); Values in Bold Indicate Levels > 0.4 MCG KG<Sup>-1</Sup> (Fda Standard); Values in Bold Underlined Indicate That the

Table 12 Heavy Metal Concentration of Brown Rice in Hsin-Chu Plots, 1 ST Crop, 2006. Italic Values Indicate Levels > 0.2 MCG KG -1 (Who Standard); Values in Bold Indicate Levels > 0.4 MCG KG -1 (Fda Standard); Values in Bold Underlined Indicate That the

Table 13 Heavy Metal Concentration of Brown Rice in Tou-Yuan Plots, 1<Sup>ST</Sup> Crop, 2006. Italic Values Indicate Levels > 0.2 MCG KG<Sup>-1</Sup> (Who Standard); Values in Bold Indicate Levels > 0.4 MCG KG<Sup>-1</Sup> (Fda Standard); Values in Bold Underlined Indicate That the Average Is > 0.4 MCG KG<Sup>-1</Sup>. </Ol> <Menu>

Table 13 Heavy Metal Concentration of Brown Rice in Tou-Yuan Plots, 1 ST Crop, 2006. Italic Values Indicate Levels > 0.2 MCG KG -1 (Who Standard); Values in Bold Indicate Levels > 0.4 MCG KG -1 (Fda Standard); Values in Bold Underlined Indicate That the Average Is > 0.4 MCG KG -1.

    Table 14 Cross Correlation of Cadmium Levels in Roots, Stems, Leaves, Rice Husk and Brown Rice.

    Table 14 Cross Correlation of Cadmium Levels in Roots, Stems, Leaves, Rice Husk and Brown Rice.

    Table 15 Cross Correlation of Cadmium in Rice Tissue and Soil Extractable Cadmium Extractions.

    Table 15 Cross Correlation of Cadmium in Rice Tissue and Soil Extractable Cadmium Extractions.

    Table 16 Coefficients of the Regression Equation to Predict Cadmium in Brown Rice from Soil Properties and Cadmium in Soil (According to Equation 1)

    Table 16 Coefficients of the Regression Equation to Predict Cadmium in Brown Rice from Soil Properties and Cadmium in Soil (According to Equation 1)

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