Cadmium in plants on polluted soils: Effects of soil

Geoderma 137 (2006) 19 – 32 www.elsevier.com/locate/geoderma

Review

Cadmium in plants on polluted soils: Effects of soil factors, hyperaccumulation, and amendments M.B. Kirkham ⁎ Department of Agronomy, 2004 Throckmorton Hall, Kansas State University, Manhattan, Kansas 66506-5501, USA Received 13 September 2005; received in revised form 25 July 2006; accepted 20 August 2006 Available online 27 September 2006

Abstract Cadmium (Cd) is a heavy metal that is of great concern in the environment, because of its toxicity to animals and humans. This article reviews recent papers showing how soil factors (such as pH, phosphate, zinc, and organic matter), Cd hyperaccumulation, and soil amendments affect Cd availability. The studies confirm that the pH of the soil is usually the most important factor that controls uptake, with low pH favoring Cd accumulation, and that phosphate and zinc decrease Cd uptake. The work reveals that the availability of Cd is increased by the application of chloride and reduced by application of silicon. The most striking result of this review is the elevated levels of Cd in plants that are being reported in recent studies. Data for concentrations of Cd in soils and plants under variously polluted conditions are presented in a table and show that all plants have Cd concentrations ≥ 0.1 mg/kg, the normal concentration in plants. Concentrations ranged from two low concentrations of 0.1 mg/kg Cd (in grain of corn, Zea mays, on an abandoned sludge disposal site that had not received sludge for 10 years, and in roots of hybrid poplar, Populus deltoides x P. nigra, at a 25-year old active sludge farm) to 380 mg/kg Cd in leaves of penny-cress (Thlaspi caerulescens). Plants that hyperaccumulate Cd (i.e., have 100 mg/kg Cd in the tissue or more) belong to the genus Thalspi, the only known Cd hyperaccumulator. Of particular concern for humans are the high concentrations of Cd in rice grain and tobacco leaves. Even if Cd availability is decreased by adding amendments, it is still in the soil and a potential hazard. The best solution for maintaining non-contaminated soils and plants is to remove the sources of Cd in the environment. Given that that is essentially impossible at this time, further research needs to determine how soil and plant factors affect Cd availability on polluted soils. © 2006 Elsevier B.V. All rights reserved. Keywords: Cadmium; Phytoremediation; Bioavailability; Soil pH; Amendments; Chelators; Hyperaccumulators

Contents 1. 2. 3. 4.

5.

Cadmium in the environment . . . . . . . . . . . . . . . . . . . . . . . . Soil factors that control Cd bioavailability . . . . . . . . . . . . . . . . . Phytoremediation by hyperaccumulator and non-hyperaccumulator plants Analysis of data for Cd in plants grown on polluted soils . . . . . . . . . 4.1. One. Concentrations . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Two. Soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Three. Cd hyperaccumulator. . . . . . . . . . . . . . . . . . . . . Amendments to control Cd availability . . . . . . . . . . . . . . . . . . . 5.1. Phosphorus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Industrial by-products . . . . . . . . . . . . . . . . . . . . . . . . 5.3. Muck . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4. Silicon . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.5. Zinc . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

⁎ Tel.: +1 785 532 0422; fax: +1 785 532 6094. E-mail address: [email protected]. 0016-7061/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.geoderma.2006.08.024

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5.6. Chloride 6. Future research Acknowledgements . References . . . . .

M.B. Kirkham / Geoderma 137 (2006) 19–32

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1. Cadmium in the environment Cadmium is a heavy metal that is of great concern in the environment, because of its toxicity to animals and humans. Concentrations of Cd can accumulate in plants that are not toxic to them, yet are toxic to the animals eating the plants. Cadmium toxicity especially affects humans rather than animals, because of their longevity and the accumulation of Cd in their organs by eating Cd-contaminated food (Tudoreanu and Phillips, 2004). Anthropogenic pathways by which Cd enters the environment are through industrial waste from processes such as electroplating, manufacturing of plastics, mining, paint pigments, alloy preparation, and batteries that contain cadmium (Adriano, 2001, p. 264; Cordero et al., 2004). Household appliances, automobiles and trucks, agricultural implements, airplane parts, industrial tools, hand tools, and fasteners of all kinds (e.g., nuts, bolts, screws, nails) are commonly Cd coated. Cadmium is also used for luminescent dials, in photography, rubber curing, and as fungicides (Adriano, 2001, p. 264). Tobacco concentrates Cd, leading to human exposure to this carcinogenic metal through smoking (Lugon-Moulin et al., 2004). Heavy metals enter soils through addition of sludge, composts, or fertilizers. Even with the strictest source control, domestic sewage sludge contains heavy metals because they are present in items washed down drains or toilets. For example, Cd is in cigarette butts flushed down toilets. Cadmium is given off from rubber when car tires run over streets, and after a rain, the Cd is washed into sewage systems where it collects in the sludge. Composted sludge can contain high levels of Cd. The composted sludge from Topeka, Kansas, which is applied to crop land, contains 4.2 mg/kg Cd (Liphadzi and Kirkham, 2006). Phosphate fertilizers are contaminated with Cd. Zarcinas et al. (2004) attributed elevated levels of Cd in soil and excessive concentrations of Cd in cocoa (Theobroma cacao) in Peninsular Malaysia to input from phosphate fertilizers. People who smoke counterfeit cigarettes, which are packaged in the Far East or the Balkans and made to mimic legitimate brands, are exposed to increased concentrations of Cd. The most likely origin of the excess Cd is from heavy applications of cheap, contaminated phosphate fertilizers (Booth, 2005; Stephens and Calder, 2005). Cadmium accumulates in animals, especially in the kidney, liver, and reproductive organs. Sheep in New Zealand are allowed to graze only a short period of time on pasturelands that have elevated Cd concentrations due to repeated applications of Cd-rich superphosphate fertilizer (Granel et al., 2002). The meat then has Cd levels that are allowed in export. Elevated levels of Cd in humans can cause kidney damage, and low levels of Cd in the diet are linked renal dysfunction. Other diseases associated

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29 29 30 30

with Cd exposure are pulmonary emphysema and the notorious Itai–Itai (“ouch–ouch”) disease (Yeung and Hsu, 2005). It results in painful bone demineralization (osteoporosis), because Cd replaces calcium in the bones. Cadmium poisoning has occurred worldwide. For example, it caused more than 100 deaths in Japan from 1922 to 1965 (Yeung and Hsu, 2005). Cadmium is one of the metals under scrutiny by the U.S. Environmental Protection Agency (EPA) (Hogue, 2004), and contamination from it occurs in more than 8% of hazardous waste sites in the United States (Yeung and Hsu, 2005). It renders hectares of valuable farmland in Taiwan non-arable. Therefore, effective and economical techniques are needed to remediate Cd-contaminated soils. This article reviews how soil factors, hyperaccumulation, and soil amendments affect Cd availability. The review is divided into five parts: 1) soil factors that control Cd bioavailability; 2) phytoremediation by hyperaccumulator and nonhyperaccumulator plants; 3) analysis of data for Cd in plants grown on polluted soils; 4) amendments to control Cd availability; and 5) future research. 2. Soil factors that control Cd bioavailability Different definitions of bioavailability exist (Semple et al., 2004). Adriano (2001, p. 188) defines “availability” and “bioavailability.” “Availability” refers to (1) the rate and extent at which a chemical is released from a medium of concern or (2) the bioavailability of the chemical to living receptors (e.g., plant roots) through direct contact or uptake. In other words, a chemical's bioavailability can be used to express its availability, and the two terms are often used interchangeably, as they are in this review. Metal availability in soil, rather than total metal concentration, is of main concern, because it is assumed that the available concentration is an indication of the amount available for plant uptake. Therefore, in any study, both the available and the total concentration of a heavy metal in soil should be determined. One of the most commonly used methods to determine plant availability of heavy metals, including the essential ones (copper, iron, manganese, and zinc), is the DTPA (diethylenetriaminepentaacetic acid) test, a non-equilibrium extraction developed by Lindsay and Novell (1978). It is the standard method in many soil testing laboratories in the USA (Whitney, 1998). The test also has been shown to be useful in monitoring Cd, Ni, and Pb in soils that have received sludge applications (Whitney, 1998). As the following section tells, there are many factors that control availability and new tests, other than the one developed by Lindsay and Novell (1978), have been developed to determine available concentration. pH and organic matter are two of the most important soil factors that control Cd availability (Barančiková et al., 2004).

M.B. Kirkham / Geoderma 137 (2006) 19–32

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Table 1 Cadmium concentration in plants grown on various soils† Plant name Common and Latin

Soil type

pH

Source of pollution

Field (F) or greenhouse (G)

Total soil Cd mg/kg

Corn Zea mays

Non-mined and strip-mined

pH kept at 6.5 or higher, by law

Chicago sludge applied, 1974–1984

F

50

1985–1987 Leaf Grain 1995–1997 Leaf Grain Indian mustard Brassica juncea Shoot Root Lettuce Lactuca sativa Leaves

Penny-cress Thlaspi caerulescens Leaves Non metal tolerant Population 1 Population 2 Metal Tolerant Population 1 Population 2 Rice Oryza sativa Grain

Granato et al., 2004

5.6 0.1 Paddy soil; clay loam

7.40

Cadmium nitrate salt added

G

190

Jiang et al., 2003

160 240 Silt loam

Arable

Limed to different pHs 5.8 6.4 6.9 Not given

Cadmium chloride salt added

Cadmium sulfate salt added

G 1.1 1.3 1.3 G

Kuo et al., 2004 14 9.5 80 Dechamps et al., 2005

380 280 260 160 Two south China soil Typic Hapludults

Cadmim chloride salt added

G

2.0

Li et al., 2005

4.95 0.623 0.407

Typic Hapluqept

6.54

Paddy soil (loam) Two soils

6.0

Sandy

4.6

Long term irrigation with sewage (since before 1974) Cadmium sulfate added

F

0.70–6.24

G

17.6

Roots Stems Leaves Fruit

0.528 0.250 0.44– 3.87

Xiong et al., 2004 Treder and Cieslinski, 2005

32.83 47.77 25.60 0.958 Sandy clay loam

Roots Steams Leaves Fruit Sunflower Helianthus annuus Roots Leaves Tall fescue Festuca arundinaceae Leaves Taro Colocasia esculente Roots Stems

Reference

10 0.2

Cultivar A Cultivar B

Cultivar A Cultivar B Rice Oryza sativa Grain in 1990 Strawberry Fragaria chilensis Var. ananassa

Plant Cd mg/kg

4.9 28.80 18.42 8.83 0.418

Silty–clay loam

5.51

Cadmium chloride salt added

G

30

Turgut et al., 2004 90 20

Soil in Joplin, Missouri USA

7.15

Contaminated with smelter emission

F

24.64

Garden

8.0

Cadmium nitrate salt added

G

250

Brown et al., 2004 3.38 Patel et al., 2005 200 12 (continued on next page)

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M.B. Kirkham / Geoderma 137 (2006) 19–32

Table 1 (continued) Plant name Common and Latin Leaves Tobacco Nicotiana tabacum Leaves (non-transgenic)

Tobacco Nicotiana tabacum Leaves

Soil type

pH

Source of pollution

Field (F) or greenhouse (G)

Sandy loam

Limed to different pHs 5.8 6.5 7.0 Limited to different pHs 5.1

Naturally polluted; near a former smelter

G

Typic Haploxeralf

Cadmium naturally in soil

5 2.5 1.5

F

Tsadilas et al., 2005 0.14 (extractable) 0.15 (extractable) 0.13 (extractable) 17.33

Loam

7.2

Cadmium sulfate salt added

F

Two soils

Various

Long-term sewage sludge dispsal sites

F

Loamy sand

6.1

0.14–1.07

Sandy loam

6.6

0.14–2.70

Sandy; typic Haplumbrept

Various

3.75 3.13 2.45 Evangelou et al., 2004 32 Adams et al., 2004

Grain

Wheat Triticum aestivum Leaves—1998 Leaves—1999 Sugar beet Beta vulgaris Leaves—1998 Leaves—1999 Potato Solanum tuberosum Leaves—1998 Leaves—1999 Two crops

Reference

Sappin-Didier et al., 2005 2.4 2.6 2.3

5.8

Grain Three crops

Plant Cd mg/kg 1

5.3

Tobacco Nicotiana tabacum Leaves Wheat Triticm aestivum

Total soil Cd mg/kg

0.2 0.2

Very fine sandy loam

40 years irrigated with waste water

F

0.36

Ingwersen and Streck, 2005

5.9 5.7

0.26 0.18

5.3 5.7

0.29 0.23

5.5 5.5 8.1

0.14 0.29 25-year-old sludge farm

Hybrid poplar Populus deltoides x P. nigra Roots Stems Leaves Sunflower Helianthus annuus Roots Stems Leaves

F

0.8

Liphadzi et al., 2003

0.1 1.9 5.5

1.1 0.2 2.2

†

Maximum concentration of Cd in plants, under non-polluted conditions, is 0.20 mg/kg (Kirkham, 1977). Normal level is 0.1 mg/kg (Brooks, 1998b). If special treatments have been given other than the ones listed in the table (e.g., a chelate has been added to the soil), these special treatments are not listed. Only values for the control treatments are given. The data in the table are from 16 papers published between January, 2003, and July, 2005, in which the concentration of Cd was given in both the soil and the plant.

Recent papers confirm earlier observations (Kirkham, 1977) that pH is one of the most important factors, if not the most important factor (Kukier et al., 2004), controlling uptake of heavy metals (Seuntjens et al., 2004; Amini et al., 2005; Basta et al., 2005). Table 1 has been constructed to show the uptake of Cd by plants grown on various soils with different types of pollution. A polluted soil is here defined to be a soil that has been impacted by anthropogenic activities—e.g., sludge disposal. Some soils naturally have high Cd concentrations

(Adriano, 2001, p. 266), but these soils will not be considered, except for the soil studied by Tsadilas et al. (2005), which had only natural levels of Cd. In Table 1, pH is given, if documented in the original paper. One can see, for example in the studies by Kuo et al. (2004), Sappin-Didier et al., 2005, and Tsadilas et al. (2005) that, as pH decreases, the amount of Cd in the plants increases. There is a linear trend between soil pH and Cd uptake by plants (Tudoreanu and Phillips, 2004, p. 145). Because speciation varies with pH, the concentration of free metal ion

M.B. Kirkham / Geoderma 137 (2006) 19–32

concentration exerting a given level of toxic effect can be expressed as a function of pH alone (Lofts et al., 2004). Multiple regression analysis showed that soil total Cd and pH were the significant factors influencing grain Cd concentrations in a meta-analysis of 162 wheat (Triticum aestivum) and 215 barley (Hordeum vulgare) grain samples (Adams et al., 2004, Table 1). Domestic sewage sludge contains Cd in varying amounts and is a source of Cd pollution when applied to land for disposal. Because of nitrification and the microbial production of carbon dioxide, sewage sludge often lowers the pH of soils. Liming of sludge-disposal sites is recommended to keep heavy metals less available. McLaren et al. (2004) applied Cd-spiked sludge to five different soils from New Zealand: three forest soils and two pasture soils. Metal leaching from the soils was monitored continuously over a three-year period. The pH of the leachate from the soils without sludge was higher than the pH of the leachate from the soils with sludge. Leachate pH values from control lysimeters fluctuated mainly around pH 6.0–6.5, whereas pH values of leachates from sludge-treated lysimeters fell to around pH 5.0 or below. Conditions for metal leaching were enhanced by the decreased pH resulting from sludge treatment. The amount of Cd leached from four of the five soils was higher in the sludged soils than in the control soils (one pasture soil was an exception). More Cd leached out of the forest soils than the pasture soils, and this was expected from the acidic forest soils. Sludge was surface applied to the forest soils and incorporated in the top 10 cm in the pasture soils (McLaren et al., 2005). After three years, there was little movement of Cd below the level of incorporation in the pasture soils, while in the three forest soils the metal penetrated to 0.25 m from the top. The results indicated potential for the long-term and sustained leaching of metals from forest soils. Bergkvist and Jarvis (2004) described a model to help resolve uncertainly over the long-term consequences of sludge applications to arable land. Model simulations were compared with measured changes in Cd contents in a clay loam soil following 41 years of sludge application. The most important parameters affecting leaching and crop uptake were the Cd loading, the partition coefficient for sludge-derived inorganic material, and the factor regulating the effect of pH on sorption. The model adequately reproduced the data, although discrepancies in the vertical distribution of Cd were attributed to the effects of macropore transport and root-uptake driven recirculation. A problem in parts of China is the uptake of Cd by rice (Oryza sativa) grown on the acidic red soils of southern China (Li et al., 2005). Human exposure to toxic heavy metals via dietary intake is of increasing concern. A pot experiment was conducted to elucidate the relative significance of soil types and rice genotypes on the bioavailability of Cd. Two cultivars were grown on two soils. One was a Typic Hapludults with a pH of 4.95 and one was a Typic Haplaquept with a pH of 6.54 (Table 1). On both soil types, Cd in the rice grain exceeded the Chinese food guideline limit of 0.2 mg/kg. Values of Cd in the grain ranged from 0.250 to 0.623 mg/kg. Li et al. (2005) concluded that “great care must be taken in cultivar selection when cultivating rice in areas where inherent soil characteristics result in the presence of a high proportion of total soil Cd in a

23

readily available form.” They “strongly recommended” that “the cultivation of high Cd cultivars on acid soils be avoided.” Li et al. (2005) spiked soil in pots with a salt (cadmium chloride), and the availability of Cd under field conditions might be less than that observed in the greenhouse experiment. Nevertheless, Cd uptake by rice in China is of concern not only on the acidic red soils of southern China but also on the rich, black soils of northeast China. Rice on these soils can contain as much as 3 mg/kg (3 ppm) of the heavy metal, exceeding the World Health Organization's recommendations of less than 0.2 mg/kg (0.2 ppm) (Schnoor, 2004). There is urgent need for costeffective solutions to reduce the 2 million hectares of China's land that are polluted by heavy metals (Schnoor, 2004). While agricultural soils can be maintained close to neutral pH by application of lime and base-rich fertilizers to limit heavy metal uptake, forest soils are often acidic and poorly buffered. Yet forest soils are often exposed to atmospheric heavy-metal pollution. They also are sites for sludge-disposal, because the plants growing in forests are not part of the human food chain. However, forested soils may be relevant for Cd transfer to humans, if they consume internal organs like liver and kidney of hunted deer. In forest soils, natural layering can be important when considering the effect of pH on metal uptake. Menon et al. (2005) investigated the influence of two types of uncontaminated subsoil, one acidic and one calcareous, on forest vegetation. The topsoil was polluted with 10 mg/kg Cd in filter dust from a non-ferrous metal smelter. It was mixed into the upper 15 cm of soil, which was a silty loam with a pH of 6.5. The vegetation was Norway spruce (Picea abies), willow (Salix viminalis), poplar (Populus tremula), and birch (Betula pendula) trees and a variety of herbaceous understorey plants. They were grown for three years in lysimeters in open top chambers. Evapotranspiration and root growth were reduced in metal contaminated treatments, independent of the subsoil type. Soil water potentials indicated that the increasing water consumption over the years was fed primarily by intensified extraction of water from the topsoil with acidic subsoil. Lower depths became strongly exploited in the lysimeters with the calcareous subsoil. The results showed that the uncontaminated subsoil offered a possibility to compensate for the reduction in root water extraction in the topsoil under metal stress. It must be noted that the work of Menon et al. (2005) showed that the pH and organic matter of surface, contaminated soil do not control the uptake of Cd, when roots can grow into uncontaminated subsoil. In contrast to many studies that show pH is the most important factor in determining availability of Cd, two studies, both done in Canada, point out the importance of organic matter. Sauvé et al. (2003) found that for organic forest soils in Canada, pH and total metal contents were not consistent predictors of metal partitioning between the solid and liquid phases of the soil. The soils showed high sorption affinity of organic matter for Cd, which was as much as 30 times higher than mineral soil for sorbing Cd. This study indicates that the quality of soil organic matter may play an important role for the ability to bind and accumulate Cd. This is a topic deserving of more research. Another study done in Canada (Ge and Hendershot, 2005) showed that organic matter is the primary sorbent for heavy

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M.B. Kirkham / Geoderma 137 (2006) 19–32

metals in the boreal temperate regions such as the Canadian Shield. Soils in this region often possess podzolic characteristics due to the acidic soil environment and the alluviation process. Organic matter usually accumulates in the surface and subsurface layers of the soil profile, present as either bulk materials or coating on particular matter. Organic matter is an important reactive component in such soils capable of retaining the metal cations. In some studies involving metal adsorption in mineral-humic mixtures, it was shown that the amount of bound metals was increased compared to the metal binding on the mineral alone. Degryse et al. (2004) studied extraction of the “labile Cd pool,” a term they used, which probably is the weakly sorbed/ exchanged Cd. They used 1 M CaCl2, because the labile Cd is solubilized through complexation by Cl−and competition for surface sites by Ca2+. Degryse et al. (2004) said that it is unlikely that fixed Cd (occluded in minerals) will be dissolved by CaCl2. Sequential extraction schemes have been proposed to assess the availability of heavy metals in soils. But, according to Degryse et al. (2004), although sequential extractions may give useful information about the associations of the metals in the soil, the results are difficult to interpret in terms of availability. They suggested that the isotopically exchangeable pool of metals, also called the ‘E’ value, may best represent the fraction of metals that is in dynamic equilibrium with metals in the solution phase. To determine the E value, a small quantity of suitable radioisotope is added to a water or dilute salt extract, and the specific activity of the metal is measured after a set equilibration time. The ratio of the E value to the total metal content (%E value) denotes the fraction of metals that is labile. Degryse et al. (2004) found that soils polluted with Cd had %E values ranging from 9% to 92% (mean 61%) for Cd. There was a strong negative correlation between pH and %E in soils enriched with metals in soluble form (e.g., metal salts). In soils where Cd was added in a less soluble form, no such correlation was found, and %E values were generally less than in soils spiked with metal salts, which suggested that the source of the contamination controls the labile fractions of Cd. Gray et al. (2004) also found that the isotopically exchangeable kinetics technique is a useful tool to provide information on Cd availability in soils. In addition to E values by isotope dilution, another new way to determine bioavailability of heavy metals is the diffusive gradients in thin films (DGT) technique. In the DGT method, ions are dynamically removed by their diffusion through a gel to a binding resin, while E values represent the isotopically exchangeable (labile) metal pools. Nolan et al. (2005) found that the kinetically labile solid-phase pool of metal, which is included in the DGT measurement, played an important role in Cd uptake by wheat (Triticum aestivum) along with the labile metal in soil solution. Concentration of Cd in plants was highly related to the effective metal concentration (the concentration available for plant uptake), as measured by the DGT technique, while other measures of metal availability, such as the soluble metal and E values measured by isotope dilution, were not as well related. The nutrient level also affects bioavailability. Pearson and Kirkham (1981) grew wheat (Triticum aestivum) in one of three solutions: distilled water; half the normal strength of Hoagland's

nutrient solution; and five times the normal strength of Hoagland's nutrient solution. Half of the solutions had 1 mg/kg Cd, added as CdSO4, and the other half had no added Cd. Cadmium apparently increased the permeability of membranes to ions and water, because osmotic potentials were usually lower, and turgor potentials higher, with Cd than without. Plants which grew in 5X nutrient solution with Cd had a higher turgor potential and a higher dry weight than those which grew in 5X nutrient solution without Cd. Göthberg et al. (2004) grew the aquatic macrophyte water spinach (Ipomoea aquatica), which is a widely used vegetable in southeast Asia, in Hoagland's solution with different strengths (1, 10, 25, 50, 100%). Cadmium was added as cadmium sulfate to the nutrient solutions (0, 0.9, 9, 27, 45 μM Cd). They measured Cd in the leaves, stems, and roots. Uptake of Cd depended upon the strength of the nutrient solution. They found that the lower the nutrient strength in the medium was, the higher the metal concentrations that accumulated in the different plant parts. However, contrary to this main finding, Cd concentrations in the leaves, stems, and roots of untreated plants were higher at the high rather than the low strength of nutrient solution. Gothberg et al. (2004) conclude that “the strength of the external nutrient solution is of importance for the accumulation and toxicity of heavy metals in water spinach.” Aging is a factor that affects availability. As a result of longterm chemical processes, the bioavailability of metals in soils can decrease with time, with little or no reduction in the total metal concentration (Lock and Janssen, 2003). However, it is difficult to assess the rate and extent of metal aging because environmental parameters affect the aging process simultaneously, such as temperature, repeated drying and rewetting, soil moisture content, pH, and total metal concentration. pH is probably the most important parameter influencing the aging process. Lock and Janssen (2003) said it should be possible to estimate the influence of aging on metal availability for a given soil by calculating the difference between the metal fraction sorbed immediately after spiking and the fraction predicted to be sorbed after aging on the basis of the pH. For example, in acidic soils, the sorbed metal fraction will remain constant over time after spiking because metals stay in solution at a low pH. In contrast, in soils with a high pH, the influence of aging on metal availability will be high if the initial sorption is low, but smaller when the initial sorption is already high. To work out the foregoing hypothesis in more detail, it would be interesting to collect contaminated and uncontaminated field soils with the same soil properties and subsequently spike the uncontaminated soils with the same metal concentrations as the contaminated soils. In this way, it would be possible to quantify the effect of aging and to monitor metal availability as a function of time (Lock and Janssen, 2003). At the long-term sludge-disposal site of Chicago in Fulton County, Illinois, USA, Cd in sludge-amended soil was measured right after the cessation of a 10-year application of sludge to the land (1974–1984) and then 10 years later (Granato et al., 2004; Table 1). In 1985–1987, Cd concentrations in soil, corn (Zea mays) leaves, and corn grain at the site were 53, 10, and 0.2 mg/ kg, respectively. By 1995–1997, these concentrations were 50, 5.6, and 0.1 mg/kg. The change in total soil Cd concentration from

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53 to 50 mg/kg was small. The available concentration of Cd in the soil was not measured. But the fact that the concentration of Cd in the leaves and roots fell by about half indicates that the available amount of Cd in the soil decreased with time, even though the total amount hardly changed. In a long-term wastewater disposal site (40 years) on a sandy soil in Germany, still in use, there was a linear relationship between Cd content of potato (Solanum tuberosum), sugar beet (Beta vulgaris), and winter wheat (Triticum aestivum) and the Cd concentration in the soil solution (Ingwersen and Streck, 2005; Table 1). Comparison between the studies of Granato et al. (2004) and Ingwersen and Streck (2005) cannot be made, because in one study (Granato et al., 2004), total Cd in the soil was studied, and in the other (Ingwersen and Streck, 2005), Cd in solution was studied. Pedotransfer functions are now being used to study heavy metal movement and availability in soil. They have been used to understand hydraulic characteristics of the soil since 1989, when Bouma (1989) proposed their use. He suggested that key measures of the soil's characteristics could be used to infer other traits that are more difficult to measure directly. For this process, he defined “pedotransfer functions,” which allow existing knowledge to be transferred to deduce something that is unknown or difficult to determine (Clothier et al., 2004). More specifically, pedotransfer functions are regression equations that are used to predict difficult-to-obtain parameters from more easily measured soil properties (Perfect, 2003). They have been widely used to predict input parameters for soil hydrological models from basic soil physical properties such as particle size distribution and bulk density (Pachepsky and Rawls, 2004; Martin et al., 2005). Gonçalves et al. (2001) and Perfect (2003) have applied this approach to estimate the input parameters for solute transport models. Springob et al. (2001) used pedotransfer frunctions to assess the bioavailability of Cd. In particular, they used pedotransfer functions to estimate parameters in the Freundlich equation (isotherm) to predict Cd concentrations in soil solution. The Freundlich equation is: S ¼ CCdM

ð1Þ

where S is the sorbed fraction, CCd is the Cd concentration in the soil solution, and k (slope) and M (shape) are the Freundlich parameters. CCd for an individual soil can be derived if S, k, and M are known. If a number of different soils are considered, M is not closely correlated with basic soil properties, and average values around 0.8 have been frequently used (Springob et al., 2001). The more important parameter k is determined by soil properties and thus can be derived by multiple regression techniques. Springob et al. (2001) extended the basic Freundlich function as follows: S ¼ k ⁎x1a x2b ::: xnz CCdM

ð2Þ

The factors x1 to xn represent the soil variables that predict k. The constant k⁎ contains the unpredictable factors and might not be required in all cases. The exponents a, b … z are used to allow a nonlinear contribution of each independent variable. In the log domain, Eq. (2) can be fitted to data by

25

the procedures of multiple linear regression analysis (Springob et al., 2001): S ¼ k ⁎ þ alogx1 þ blogx2 ::: þ zlogxn þ M logCCd

ð3Þ

Such operational models, based on easily available, general soil properties as pH, CEC, organic carbon, and dissolved organic carbon, are parameterized. Springob et al. (2001) determined Cd sorption isotherms for 225 soil samples from sandy, northern German arable and forested soils. From these they derived the Freundlich parameters k and M. The average value of parameter M was 0.815. There was some correlation of M with pH. Samples above pH 6 had an average M of only 0.730. The main information about the sorption properties of the soils was contained in k, which could be predicted by multiple regressions from pH, organic carbon, and clay content for one subset of Ap horizons (r2 = 0.96). They used the Freundlich equation to predict Cd concentrations in the soil solutions (CCd) of the 225 sites, both for the current load of Cd and assuming higher contamination, for example, after additions of sewage sludge. They pointed out that the approach appears to be promising, but there are still some deficiencies concerning the prediction of the Freundlich exponent M and the influence on k of DOC, time, temperature, and the contents of clay or oxides. Booltink et al. (1998) used a pedotransfer function to predict the time of initial breakthrough of a solute (a dye) in soil columns. Using the pedotransfer function, they were able to identify macropore flow. Their pedotransfer function estimated the time for initial breakthrough, and this value was incorporated into a model to calculate the rate of propagation of the waterfront in macropores. The method might be used to determine the Cd front, if Cd is in the soil solution. Calculations made with pedotransfer functions might be compared to measurements of penetration of the solute front using the method of Duwig et al. (1997). They inserted TDR probes horizontally into columns with soil from Maré in the Loyalty Islands of New Caledonia to measure the relative velocity of the wet front and solute front using bromide as a tracer. The soil was a ferralitic oxisol derived from weathered volcanic ejecta and ash. Even though the soil was volcanic, it had some anion exchange capacity that acted to retard the leaching of anions like nitrate. The method of Duwig et al. (1997) depends upon the ion being mobile in the soil solution.

3. Phytoremediation by hyperaccumulator and nonhyperaccumulator plants Phytoremediation is the use green plants to detoxify a degraded or polluted environment (Brooks, 1998a). It is divided into the following topics (Salt et al., 1998): phytoextraction, phytodegradation, rhizofiltration, phytostabilization, phytovolatilization, and use of plants to remove pollutants from air. The main advantages of phytoremediation are that the procedure is carried out in situ and it is inexpensive compared to other technologies for remediation (Brooks, 1998a), such as capping or removal and disposal of the contaminated material. Many of these engineering techniques are subject to economic and

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logistic restrictions and prevent restoration of environment (Illera et al., 2004). Another important advantage of phytoremediation is that soils retain their fertility after metal removal. Phytoextraction is the method usually used to remediate metal-contaminated soils. Heavy metals are a target for phytoextraction. The technology relies on plants that translocate heavy metals into their aboveground parts (Robinson et al., 2000). The plant biomass is removed from the field and can be burned to reduce its volume. It is then disposed in an appropriate area, such as a contained landfill. Hyperaccumlator plants are species able to accumulate high amounts of heavy metals in their tissues, at concentrations 10 to 100 times higher than tolerated by crop plants (Kukier et al., 2004). A hyperaccumulator for Cd has 100 mg/kg Cd in its tissue, compared to a normal level for most plants of 0.1 mg/kg (Brooks, 1998b). Higher concentrations of a heavy metal are found in the shoots than the roots of hyperaccumulators. This is opposite to non-accumulator species, which concentrate metals in their roots when exposed to high soil metal concentrations. For non-accumulators, exclusion of metals from shoots and/or roots and retention of metals in root cell walls and vacuoles is a defense minimizing metal phytotoxicity. In contrast, metal accumulation in shoots of hyperaccumulator plants is believed to provide a unique method of self-defense against microbial infection and larval feeding on leaves, giving these species an advantage on metal-rich soils (Kukier et al., 2004). Thalspi caerulescens is a known accumulator of Zn (Brooks, 1998b), but it also accumulates Cd (Wang et al., 2006). It is the only hyperaccumulator known to accumulate Cd (McGrath, 1998), and many studies show it to be a Cd hyperaccumulator (e.g., Baker and Whiting, 2002; Cosio et al., 2005). One of its common names is penny-cress. Not all Thlaspi ecotypes are Cd hyperaccumulators. Dechamps et al. (2005) compared two ecotypes of T. caerulescens on Cd-contaminated soil (Table 1). One ecotype (T. caerulescens subsp. Calaminare) came from a metal polluted site in Belgium (MET); the other ecotype (T. caerulescens subsp. Caerulescens) came from a nonpolluted site in Luxembourg (NMET). The MET population had a higher biomass and a higher root:shoot ratio compared to the NMET population. The shoot mass of the MET and NMET populations were 1.1 g and 0.7 g, respectively; the root mass of the MET and NMET populations were 0.8 g and 0.2 g, respectively. These values corresponded to root:shoot ratios for the MET and NMET populations of 0.63 and 0.25, respectively. Vogel-Mikuš et al. (2005) found hyperaccumulation of Cd by Thlaspi praecox from a polluted area in Solvenia. It had a maximum shoot concentration of 5960 mg/kg Cd. No arbuscular mycorrhizal fungi colonization was observed on the most polluted plots. However, low to moderate levels of mycorrhizal frequency (F = 20% to 30%) were observed on less and non-polluted plots. To their knowledge, this was the first report of Cd hyperaccumulation and mycorrhizal colonization in metal hyperaccumulating T. praecox. Brassicaceae are generally considered not to be mycorrhized, so the result of Vogel-Mikuš et al. (2005) is interesting. Vogel-Mikuš et al. (2006) did a greenhouse experiment in which they inoculated the hyperaccumulator T. praecox with arbuscular mycorrhizal

fungi. Colonized plants showed improved nutrient uptake and a decreased Cd uptake, thus confirming the usefulness of the symbiosis, but negating its benefit for phytoremediation. More studies are needed to determine the extent of mycorrrhizal fungi on the Cd hyperaccumulator and its effect on Cd accumulation. Even though the high metal concentration is supposed to be a defense in hyperaccumulators, a high Ni mirid bug (Melanotrichus boydi) has been found on a California Ni hyperaccumulator, Streptanthus polygaloides. This specialist insect, found only on this hyperaccumulator species, was unknown to science prior to insect surveys, illustrating the potential of studies of hyperaccumulator ecology to yield unique discoveries (Boyd, 2004). Patel et al. (2005) investigated taro (Colocasia esculenta) as a potential Cd hyperaccumulator (Table 1). It is a species of tropical Asia and Polynesia and grown for its edible tubers. The authors grew the plants in pots containing different concentrations of Cd. Cadmium depressed dry matter production of the plant up to 33%. The plants accumulated a larger portion of the heavy metal in the roots followed by stem and leaf. Taro does not appear to be a hyperaccumulator useful in phytoremediation. Hyperaccumulating plants can be found in naturally occurring metal-rich sites. However, these plants are not ideal for phytoremediation, because they are small and have a low biomass production, like penny-cress. In contrast, plants with good growth usually show low metal accumulation as well as low tolerance to heavy metals. An ideal plant for phytoremediation is one with high biomass production, easily harvestable, and with superior capacity for heavy-metal tolerance and accumulation (Sappin-Didier et al., 2005). This underpins the need for alternative phytoremediation options such as transgenic approaches. Combining the genomes of a hyperaccumulator and a related, high-biomass, non-accumulator species, might become a promising alternative. Hence Sappin-Didier et al. (2005) investigated metal-uptake capacity of transgenic tobaccos (Nicotiniana tabacum) overexpressing ferritin in plastids (P6) or in cytoplasm (C5) and a control tobacco (A) (Table 1). They grew the plants in three polluted soils (designated 8b2, 8b3, S11) from the same soil series, with a similar Cd content, but having pHs from 5.8 to 7. Differences in dry leaf weight were not significant among the three tobaccos. Only the P6 tobacco growing in the S11 soil accumulated slightly more Cd compared to A and C5 tobaccos, but its increase was small; A and C5 accumulated 2 μg Cd and P6 accumulated 2.5 μg Cd. The results indicated that genetic engineering was not effective in increasing Cd uptake. In contrast to genetic engineering to enhance metal uptake, chelates are added to soil with the goal of making large biomass plants into hyperaccumulators. For efficient phytoremediation, the process needs good biomass yields and metal hyperaccumulation (McGrath and Zhao, 2003), and chelates are added to try and accomplish both. The synthetic chelator, ethylenediaminetetraacetic acid (EDTA), is often used since it is an effective chelating agent (Gwo and Jardine, 2005). EDTA is not known to be particularly toxic per se in the environment. Its capacity to mobilize toxic metals in combination with its persistence is what is of environmental concern. As a result of complexation of Cd

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and EDTA, the mobility of Cd is increased. It is important to add a chelate when the plant is at its maximum growth with maximum root area, because, once the plant takes up the solubilized metal, it usually dies. If the plant dies upon treatment, this indicates that the increase in metal uptake was not a physiological response. Hence, such an effect cannot be termed “hyperaccumulation.” Chen and Cutright (2002) found that EDTA increased the shoot concentration of Cd from 34.2 mg/kg to 115 mg/kg in sunflower (Helianthus annuus). However, the total biomass of plants was drastically decreased by 50 to 60%. Turgut et al. (2004; Table 1) also found that the chelate citric acid was severely phytotoxic to sunflower. The concentration of the chelate also determines whether or not the plant will take up a metal. Vassil et al. (1998) studied the role of EDTA in Pb transport and accumulation by Indian mustard (Brassica juncea). They showed that a threshold concentration of EDTA was required to stimulate Pb accumulation. They speculated that at the threshold concentration synthetic chelators destroy the physiological barrier in roots, which normally function to control uptake and translocation of solutes, by removing stabilizing Zn2+ and Ca2+ from the plasma membrane. Without this barrier, metal-ligands in soil solution could equilibrate rapidly with the xylem sap. Once in the xylem, metal-ligands follow the transpiration stream and accumulate in shoots. Adding chelating agents to soil to increase the bioavailability of heavy metals to induce hyperaccumulation in normal plants may produce undesirable environmental risks, grave if the groundwater is polluted, because half of the population in the USA uses groundwater as a source of drinking water. To decrease the chance of groundwater pollution with metals during chelate-facilitated phytoremediation (Jiang et al., 2003; Table 1), protective strategies have been suggested, such as using a dual-pipe subirrigation-drainage system (Madrid et al., 2003), increasing sorption (increasing field capacity) of soils by adding acrylamide hydrogels (Kos and Leštan, 2003), addition of physical barriers (e.g., vermiculite and apatitie mixture) (Kos and Leštan, 2004), minimizing the concentration of chelate used, dosage splitting (Schmidt, 2003), use of biodegradable synthetic chelating agents (Kos and Leštan, 2004; Tandy et al., 2004), and use of less-toxic natural chelators, like humic acids (Evangelou et al., 2004; Table 1) and biosurfactants generated by bacteria and yeast (Wang and Mulligan, 2004). Keller et al. (2005) showed that thermal treatment of Cdenriched plants may be a feasible option for evaporatively separating Cd from plant residues. Between 90% and 100% of the Cd was volatilized from willow (S. viminalis) and the Cd hyperaccumulator, Thlaspi caerulescens. The authors suggested that this Cd could be recovered and recycled and that the bottom ash could be recycled as a fertilizer free of Cd.

27

et al., 2004; Sappin-Didier et al., 2005) or by having Cd salts added to the soil (Jiang et al., 2003; Kuo et al., 2004; Turgut et al., 2004; Evangelou et al., 2004; Dechamps et al., 2005; Li et al., 2005; Treder and Cieslinski, 2005; Patel et al., 2005;). The only study in Table 1 that reports Cd naturally in the soil is in the one by Tsadilas et al. (2005), who grew tobacco with no added Cd. Three conclusions can be drawn from Table 1. 4.1. One. Concentrations Most of the concentrations of Cd in the plant parts are above the maximum concentration observed under non-polluted conditions (0.2 mg/kg in plants) and all are equal to or above the normal level in plants (0.1 mg/kg in plants; Brooks, 1998b). If we ignore the greenhouse studies in which the soil has been artificially polluted with Cd salt and focus on the field studies, we can see that Cd in the environment is a cause for concern and does need careful regulation (Renella et al., 2004). The high Cd in rice grain is particularly worrisome in China (Xiong et al., 2004; Schnoor, 2004; Li et al., 2005). The tobacco companies do need to be concerned about the high level of Cd in tobacco (Lugon-Moulin et al., 2004). Long-term sludge and wastewater disposal sites do have plants with higher-than-normal concentrations of Cd that are eaten by humans or animals (Liphadzi et al., 2003; Adams et al., 2004; Granato et al., 2004; Ingwersen and Streck, 2005). 4.2. Two. Soils More papers need to define the soils on which the studies are done. Most of the 16 papers cited in Table 1 did not give the taxonomic name of the soil, and, in some cases not even a general soil type was given. If we are to learn how soil properties affect Cd uptake, we need to know the soils. 4.3. Three. Cd hyperaccumulator The data in Table 1 confirm that the Cd hyperaccumulator, penny-cress (T. caerulescens), does accumulate high concentrations of Cd. It has the highest concentrations of Cd of any plant listed in Table 1. Indian mustard (B. juncea) also has high concentrations of Cd as a result of the high level of Cd salt added (Jiang et al., 2003). 5. Amendments to control Cd availability Because the data in Table 1 show that Cd pollution of soil is of concern, we need to consider methods to reduce the Cd availability. Various amendments have been added to soil to prevent or enhance Cd uptake.

4. Analysis of data for Cd in plants grown on polluted soils 5.1. Phosphorus Table 1 shows studies in which the Cd concentration has been given in both the soil and the plant. Soils have been polluted with Cd by application of sludge (Liphadzi et al., 2003; Granato et al., 2004; Adams et al., 2004) or wastewater (Xiong et al., 2004; Ingwersen and Streck, 2005); by being near a smelter (Brown

One of the most common amendments added to soil to tie up heavy metals is phosphate. It is generally felt that phosphate essentially does not move downward in most soils. However, considerable phosphate leaching has been observed in connection

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with preferential flow, e.g., in tile-drained soils. Addition of phosphorus to soil is the basis of a patented process to reduce bioavailability of metals (Pierzynski and Hettiarachchi, 2002). The patent also describes the mixing of an oxide of manganese into soil to reduce metal bioavailability. The patent states that preferred phosphorus sources are phosphate rock, alkali and alkaline earth metal phosphates, ammonium phosphates, ammonium orthophosphates, orthophosphoric acid, and superphosphates. The patent gives data for bioavailability of Pb in polluted soil treated with phosphate rock or triple superphosphate, and the results show that both forms of phosphate are equally effective in reducing bioavailability. The study by Brown et al. (2004) showed that phosphate reduces Cd availability. They established a study near a former Zn and Pb smelter in Joplin, Missouri, USA, to test the ability of soil amendments containing phosphorus to reduce the availability of Pb, Zn, and Cd in situ (Table 1). Soil collected from the field was amended in the laboratory with phosphorus added in different ways, including as 1% PH3PO4, a high-Fe by-product +P-triple superphosphate (TSP) (2.5% Fe + 1% P-TSP), 1% P-TSP, 3.2% P-TSP, 1% Pphosphate rock, sludge compost at 10% + 0.32% P-TSP, and sludge compost at 10% + 1% P-TSP. Sludge compost also was added at 10% with no P. The soil with no amendment had a pH of 7.15, and the amendments had little effect on the pH. Availability of heavy metals was assessed in different ways, including uptake by tall fescue (Festuca arundinaceae), which grew in the field. As was observed for both plant Pb and Zn, concentrations of plant Cd in the 3.2% P-TSP were lowest overall. The 1% P-TSP and 1% P-H3PO4 treatments also resulted in decreased plant Cd compared with the control treatment. Phosphate rock addition had no effect on plant Cd concentrations. Combining P with compost did not have any effect on plant Cd concentrations. Compost added alone was the most effective of the compost treatments at reducing plant Cd and was similar in efficacy to the most effective P treatments. The results showed that both sludge compost or triple superphosphate were effective in tying up Cd and making it unavailable to tall fescue. They indicated that, in combination, the effects of phosphorus and compost on Cd availability cancelled each other. The authors gave no explanation for this, and research is needed to determine the reason for this observation.

that an agricultural-based approach to remediation using these soil amendments is realistic and cost-effective for polluted industrial sites and surrounding rural land. These in situ treatments provide no actual reduction in heavy metal concentrations. Rather, they enhance the soil's natural attenuation mechanisms that control metal mobility and bioavailability, thus reducing the potential toxicity of metals to humans. Although not industrial by-products, amendments used to remove Cd from wastewaters, such as the dried brown marine macroalga, Fucus spiralis (Cordero et al., 2004), might be tried on polluted agricultural land, too, to tie up Cd. 5.3. Muck Estuaries and canals that were constructed for urban and agricultural development have contributed to the accumulation of black fine-grained organic sediment, commonly called muck. Increased muck sediment loading into estuaries and canals has caused deleterious effects on the benthic biological community and water quality. Consequently, mucks are being removed from them to improve the habitat. The muck is disposed on land. There is a concern over potential leachability of heavy metals from agricultural soils following muck application. In an experiment with 30-cm long columns with no plants, Zhang et al. (2004) added muck at different rates to the surface of sandy soils, sampled at the 0- to 30-cm depth from two commercial citrus orchards in Florida, an acidic sand and a calcareous sand. They applied daily 57 mm water and collected leachates and analyzed them for elemental concentrations, including Cd. They found that most heavy metals in the muck sediments predominantly occurred in weakly mobile or nonbioavailable forms. Concentrations of heavy metals in the leachates were below drinking water limits. At the maximum loading rate of muck of 300 kg/ha, the highest concentrations of Cd leached from muck-amended soil columns were 0.002 and 0.0006 μg/mL, for the acidic and calcareous sands, respectively, below the drinking water standard for Cd of 0.01 μg/mL. However, the experimental design of Zhang et al. (2004) was not suited to study long-term leaching of heavy metals after muck application. Field trials are needed to determine if mucks can be disposed of on land without polluting the groundwater with heavy metals.

5.2. Industrial by-products 5.4. Silicon Illera et al. (2004) investigated the potential of three industrial by-products (phosphogypsum, red gypsum, and dolomitic residue) for increasing the heavy metal sorption capacity of an agricultural acid soil developed from Pliocene–Quaternary aged formations in Cáceres, Spain, and classified as Plinthic Acrisol. The three by-products increased the retention of Cd on the solid components of the soil. The dolomitic residue increased the metal retention capacity of the soil horizons through the precipitation of laurionite-type minerals as well as Cd hydroxyl-chlorides. Scanning electron microscopy showed that Cd was found to be associated with organic matter in the Ap horizon treated with the three by-products and to be associated with undissolved dolomitic residue particles. They concluded

Silicon (Si) has been shown to increase resistance of some plant species to toxic metals, including Cd. Shi et al. (2005) grew rice seedlings hydroponically under toxic levels of Cd in a growth chamber to investigate the effects of Si on the distribution of Cd in the plants. Silicon alleviated the toxicity of Cd and partly overcame the reduction in growth due to Cd. This amelioration was correlated with a reduction in Cd uptake. Silicon increased Cd accumulation in the roots and restricted the transport of Cd from roots to shoots, where the distribution of Cd in the shoots decreased by 33%. Cadmium was mainly deposited in the vicinity of the endodermis of the root. Shi et al. (2005) said that Si, like lignin, plays an

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important role as a structural component of the cell walls. By using fluorescent tracers, they found that the Si was mainly deposited in the cell walls of the endodermis, and not the cell walls of the epidermis. Its deposition in the endodermis may account for the reduction in apoplastic transport. The heavy deposition of silica revealed by energy-dispersive X-ray analysis (EDX) in the vicinity of the endodermis strengthened this view. Mineral nutrients are blocked by the endodermis and must be actively taken up by plant roots, when they reach the endodermis. Perhaps Cd is blocked at the endodermis by Si, but the nutrients required for growth still can be taken up actively to allow for plant growth. Treder and Cieslinski (2005) applied Si as potassium silicate to strawberry plants (Fragaria chiloensis Var. ananassa) either by spraying it on the leaves or incorporating it directly into the soil, to determine if it would decrease Cd uptake and alleviate its toxic effects (Table 1). Plants were grown in a greenhouse in two soils, a sandy soil and a sandy clay–loam soil, contaminated with five different Cd levels. As expected, Cd uptake by the strawberry plants increased with the initial level of this element in the soil. However, plants grown on sandy soil had a higher concentration of Cd in all organs compared with plants grown on sandy clay–loam soil. Silicon used as soil amendment prior to planting was effective in preventing excessive Cd uptake by strawberry plants grown on the sandy soil. They postulated that Si enhances the tightness and stiffness of cell walls and is a natural mechanical obstacle for Cd ions as they are transported through cells. The precipitation of Si and Cd complexes in the cell walls and in the intercellular spaces restricts the translocation of Cd from the roots to shoots. Treder and Cieslinski (2005) suggested that an effective way to prevent excessive Cd uptake by strawberries grown on light soils would be to apply Si directly to the soil using fertilizers that contain Si. If Si makes a natural mechanical barrier for Cd ions, it may also hinder the movement of other metals. It is known that Al toxicity is alleviated by Si (Wang et al., 2004). Aluminum is a metal, but not a heavy metal. Studies need to be done to see if Si reduces the toxicity of heavy metals other than Cd. 5.5. Zinc Cadmium and Zn are chemically similar (Mengel and Kirkby, 2001, p. 670). Cadmium is thus able to mimic the behavior of the essential element Zn in its uptake. It has been known for decades that Zn is a competing ion for Cd (Hawf and Schmid, 1967; Chaney, 1973) and depresses Cd uptake (Mengel and Kirkby, 2001, p. 671). Uptake of Cd depends upon the content of Zn in the soil, and plants generally take up more Cd if the Zn content is low. Homma and Hirata (1984) found that Cd uptake rates by rice seedlings were as high as the uptake rates of Zn, if the concentration of both ion species were lower than 1.0 mmol/m 3 . At higher concentrations, Zn uptake rates were more than twice as those of Cd when both ion species were present in equal concentrations in the nutrient solution. The antagonism between Zn and Cd offers a method to reduce Cd uptake by plants. Zinc could be added to soil con-

29

taminated with Cd to help reduce Cd in food crops. In fact, Green et al. (2003) did an experiment which indicated that it might be possible to reduce Cd in wheat by adding Zn. They studied the effect of Cd and Zn levels on Cd uptake and translocation of wheat (Triticum aestivum). Genotypes of wheat can tranloscate high enough levels of Cd from uncontaminated soils to exceed the regulatory limits, which the Food and Agricultural Organization of the United Nations (FAO) suggests ought to be 0.1 mg Cd kg− 1 for cereal grains (Green et al., 2003). They found that the level of Cd did not affect the uptake and translocation of Zn in the roots and shoots. But when Zn activity was varied from 10− 7.6 to 10− 5.2 M, shoot:root Cd concentration ratio in wheat decreased from 0.20 to 0.03. The results indicated that Zn is effective in regulating Cd uptake and translocation in wheat. 5.6. Chloride Chloride anions are known to reduce soil sorption of Cd, and an increase in Cl concentration in the soil or soil solution has been shown to increase Cd concentration in plants (Smolders et al., 1997; Weggler-Beaton et al., 2000). However, because previous experiments have not distinguished between the effect of carbon on sludge-borne Cd compared with soil-borne Cd, Weggler et al. (2004) did a pot experiment with sludge application rates of 0, 20, 40, and 80 g sludge/kg soil (an Alfisol with pH 6.3) and chloride concentration in soil solution ranging from 1 to 160 mM chloride. The Cd uptake of wheat (Triticum aestivum) was measured and cations and anions in the soil solution were determined. The Cd concentration in shoots and soil solution increased with sludge application rates up to 40 g/ kg, but decreased slightly in the 80 g/kg sludge treatment. Across sludge application rates, the Cd concentration in the soil solution and plant shoots was positively correlated with the chloride concentration in the soil solution. They suggested that sludge-borne Cd is also mobilized by chloride ligands in the soil solution. Organically complexed Cd increased with the increase in sludge rate and increases in dissolved organic carbon levels. However, those levels were low in absolute terms and further decreased with increasing Cl levels (Weggler et al., 2004). They concluded that chloro-complexation of Cd increases the phytoavailability of sludge-borne Cd. 6. Future research The most striking result of this review is the elevated levels of Cd in plants that are being reported in recent studies (Table 1). The best solution for maintaining non-contaminated soils and plants is to remove the sources of Cd in the environment. Given that that is essentially impossible at this time, further research needs to determine how soil and plant factors affect Cd availability on polluted soils. The review indicates that plants are limited in the amount of Cd that they can accumulate, even when chelates are used to solubilize the Cd for uptake. Consequently, phytoremediation will be of limited use in removing Cd from the soil. Hence, further research needs to be done to determine how Cd can be tied

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up in the soil and made less available. Pierzynski and Hettiarachchi (2002) listed several forms of phosphorus that could be used to tie up heavy metals. Which form is the best one to use? Other questions raised by the review are the following: Why does one plant accumulate more Cd than another plant? Indian grass, a non-hyperaccumulator, accumulated high amounts of Cd when Cd was added as a salt (Jiang et al., 2003, Table 1). It had about 10 times more Cd in its leaves than the other nonhyperaccumulators in Table 1. It had as much Cd as the Cd hyperaccumulator, penny-cress. Can we identify other hyperaccumulators of Cd? Can we find Cd hyperaccumulators that have high biomass, and therefore, will take up large amounts of Cd? As analytical and microscopic techniques become more sensitive, small concentrations of Cd can be measured and their location in a cell can be determined. How important is adsorption of Cd or Si (Shi et al., 2005) onto the surface of a root epidermal cell wall or endodermal cell wall in controlling the uptake of Cd? What is the mechanism of the Cd–Si interaction? Is inhibition of Cd uptake by Si the result of the physical barrier that Si makes or is there a chemical reaction between Cd and Si? How is adsorption onto the root surface affected by soil type? Few studies report Cd concentrations in roots, because of the difficulty in excavating them. It is also difficult to separate soil factors that control Cd availability (e.g., an organic soil adhering to a root) from root factors (e.g., root exudates). More studies need to be done to distinguish Cd adsorption versus Cd absorption at the root. How much Cd is only adsorbed onto the surface of a root and how much is taken up into the root? What factors favor absorption over adsorption? Acknowledgements I thank Geoderma for inviting this review. I thank two anonymous reviewers for reviewing the original paper and two subsequent revisions. Their comments have improved the paper. This is Contribution No. 06-66-J from the Kansas Agricultural Experiment Station, Manhattan, Kansas 66506 USA. References Adams, M.L., Zhao, F.J., McGrath, S.P., Nicholson, F.A., Chambers, B.J., 2004. Predicting cadmium concentrations in wheat and barley grain using soil properties. Journal of Environmental Quality 33, 532–541. Adriano, D.C., 2001. Trace Elements in Terrestrial Environments. Biogeochemistry, Bioavailability, and Risks of Metals. Springer-Verlag, New York. 867 pp. Amini, M., Khademi, H., Afyuni, M., Abbaspour, K.C., 2005. Variability of available cadmium in relation to soil properties and landuse in an arid region in central Iran. Water, Air, and Soil Pollution 162, 205–218. Baker, A.J.M., Whiting, S.N., 2002. In search of the Holy Grail — a further step in understanding metal hyperaccumulation? New Phytologist 155, 1–7. Barančíková, G., Madaras, M., Rybár, O., 2004. Crop contamination by selected trace elements. Journal of Soils and Sediments 4, 37–42. Basta, N.T., Ryan, J.A., Chaney, R.L., 2005. Trace element chemistry in residual-treated soils: key concepts and metal bioavailability. Journal of Environmental Quality 34, 49–63.

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