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Journal of Environmental Quality 30:869-877 (2001)
© 2001 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America

TECHNICAL REPORT
Heavy Metals in the Environment

Plant Uptake of Cadmium-109 and Zinc-65 at Different Temperature and Organic Matter Levels

Å.R. Almås and B.R. Singh

Agricultural Univ. of Norway, Department of Soil and Water Sciences, PB 5028, 1432 Aas, Norway

Corresponding author (asgeir.almas{at}ijvf.nlh.no)

Received for publication September 30, 1999.

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSION
 REFERENCES
 
The uptake of 109Cd and 65Zn and their stable isotopes by ryegrass (Lolium multiflorum Lam.), grown on two different soil types, was investigated in climatically controlled growth chambers at 9 and 21°C. The soils were treated with 0 and 4% organic matter (pig [Sus scrofa] manure) and spiked with 109Cd and 65Zn before sowing. The organic matter addition resulted in increased uptake of the 109Cd, Cd, and Zn by ryegrass, but the uptake of 65Zn was decreased. The latter effect was ascribed to isotopic dilution of 65Zn as the amount of stable Zn in the plant tissues increased with the organic matter addition. The effect of temperature was more pronounced than that of organic matter addition, and the uptake of both 109Cd and 65Zn and their stable isotopes was higher in ryegrass grown at 21°C than that grown at 9°C. Results from fractionation and speciation analysis of soil cadmium and zinc were correlated with plant uptake, and there was a good consistency between observed plant uptake and the physico–chemical forms of cadmium and zinc in soil and soil solution presumed to be plant available.

Abbreviations: ASV, anodic stripping voltammetry • DM, dry matter


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSION
 REFERENCES
 
INTERACTIONS of trace metals with the solid phase soil include chemisorption on minerals, precipitation with different anions, coprecipitation in minerals, and complexation with organic matter (McBride, 1989). By using modern analytical methods, most heavy metals can be detected in soil solutions and dilute extracts of soils even at low concentrations, which is important for the assessment of bioavailability. Since plants and soil organisms are highly active in the processes controlling solubility, mobility, and uptake of elements from the soil solution (McLaughlin et al., 1998), vital information may be lacking in the assessment of trace metal bioavailability, if the results are based only on laboratory experiments with soils. It has, for instance, been shown that trace metal uptake is controlled not only by the soil types and soil conditions, but also by plant species (Singh et al., 1995). Toxicity of trace metals and their biological uptake by living organisms have been shown to be best correlated with the free ion or labile metal form in waters (Florence, 1986; Neal and Sposito, 1986) and soil solutions (Sauve et al., 1996). This is in agreement with the free metal ion hypothesis, which states that the bioavailability of trace metals is related to the activity of the free aquo ion (Lund, 1990). But this hypothesis may not be valid in all situations. McLaughlin et al. (1997) found, for instance, that the uptake of Cd and Zn by lettuce grown in a ligand-buffered nutrient solution was increased in the presence of organic ligands. This was ascribed to either the metal–ligand complexes being taken up intact by the roots or the complex formation affecting the diffusional limitations to free metal uptake in the unstirred root zone and in the apoplast. Mench and Martin (1991) reported that root exudates of Nicotina spp. enhanced the solubility of Cd, and this resulted also in increased bioavailability of Cd to the three Nicotina species used as test crops. The solubility of Zn was not, however, affected by the content of root exudates in the extracting solution in that experiment.

Organic matter seems to have quite a different effect on the trace metal uptake by crops, depending upon whether it is in soluble or insoluble form. The uptake of Cu2+ and Pb2+ was, for instance, effectively inhibited by formation of stable complexes with insoluble organics (McBride et al., 1997a; Sauve et al., 1998), and the complexed metals were thereby prevented from diffusing to roots. Soluble organics may, on the other hand, raise the carrying capacity of soil solution for trace metals by the formation of soluble organo–metallic complexes (Almås et al., 2000a; Dunnivant et al., 1992; Francis et al., 1992; McBride et al., 1997b; McBride et al., 1998; Mench and Martin, 1991; Naidu and Harter, 1998; Neal and Sposito, 1986; Sauve et al., 1998), and high concentrations of dissolved organics may promote trace metal adsorption to the root surfaces (McBride, 1995). The mobilization of Cd by naturally occurring dissolved organic carbon (DOC) was evaluated by Dunnivant et al. (1992). They reported that the mobility of Cd was increased as solution DOC concentration increased from 0 to 58 mg DOC L-1, and this was explained as cotransportation of Cd with DOC.

According to Nor and Cheng (1986), plant roots are able to liberate trace metals from dissolved organo–metallic complexes once they are associated in the root zone. The stability of these metal–organic complexes is, however, attributed to the heavy metal's affinity for organic matter. This may consequently affect the bioavailability of the metals in soil solution. Typically, Cu and Pb form very stable complexes with dissolved organic matter, and only a very small fraction of these metals exists as free hydrated metal ions, when soil pH is not strongly acid (Aualiitia and Pickering, 1986; Christensen, 1984; Sauve et al., 1997, 1998). Since Cd and Zn are less prone to form such stable complexes with soil organic matter (Aualiitia and Pickering, 1986; Holm et al., 1995; Pinheiro et al., 1994), a larger fraction of these metals is usually recovered as free hydrated metal ions.

Increasing temperature has been shown to increase both the rate and the amount of trace metal sorption by soil particles (Almås et al., 2000b; Barrow, 1992). At the same time, trace metal uptake by plants is reported to increase with increasing temperature (Hooda and Alloway, 1994; Pinamonti, 1998), indicating that a temperature-induced retention of metals in soil is not necessarily limiting the plant uptake. This can partly be explained by the fact that the root growth is often limited by low (suboptimal) and high (supraoptimal) soil temperatures. Hence, as soil temperature increases toward optimal, the root activity of the crop itself increases with temperature (Macay and Barber, 1984; Moorby and Nye, 1984). Huang et al. (1991a)(b) reported that the optimal temperature for the root growth of winter wheat was 25°C, resulting in reduced growth both below and above this temperature. Increased root growth becomes important for the trace metal uptake by plants since it increases the root surface for trace metal absorption, and the uptake is thus expected to increase accordingly (Singh and Subramaniam, 1997).

The amount and activity of soil microorganisms is also expected to increase with temperature, and the increased microbial activity in the rhizosphere is suggested to assist the metal uptake by plant roots in two ways. First, metals inaccessible for root uptake may be liberated through microbial decomposition of large organo–metallic complexes. Second, complexing agents exuded by the roots can enhance uptake of contaminants (McLaughlin et al., 1998). Since the excretion of organic compounds into the rhizosphere has been found to increase under conditions where microorganisms are present (Barber and Martin, 1976), metal uptake is expected to increase.

From a pollution point of view, heavy metal accumulation in soil is either of diffuse character (atmospheric deposition, application of phosphate fertilizers, accumulation in sediments, etc.) or concentrated at a specific site (spills, deposition, mine tails, amendments with sewage sludge or other wastes, etc.). Even though there may be no immediate danger of exposure to living organisms, long-term exposure or sudden changes in environmental conditions may result in undesired effects. Generally, according to the conclusions of Kabata-Pendias (1993), metals from anthropogenic sources are potentially more mobile than those ultimately inherited from the geological material. It has been reported that the potential mobility and bioavailability of metals is influenced by whether the metals are added anthropogenically or present naturally in the soil (Ma and Rao, 1997; Narwal et al., 1999). Several investigations about trace metal–contaminated Norwegian soils have shown that Cd and Zn of anthropogenic origin were more bioavailable than the naturally existing soil metals (Singh and Steinnes, 1994).

The purpose of this study was to investigate the effects of organic matter addition and increasing temperature on plant uptake of Cd and Zn recently added to two soil types. Tracers of Cd and Zn were therefore used to identify the metals recently added (109Cd and 65Zn do not exist in natural soils) from those naturally existing (stable Cd and Zn). Thus, the normal temperature gradient across Norway from south to north during the growth season can be evaluated in terms of significance on mobility of Cd and Zn from anthropogenic sources. The use of farmyard manure in grass production necessitates the use of organic matter addition to soil as a treatment factor, since organic matter plays an important role in the solubility control of trace metals in the soil–plant system as stated above. The trace technique method is very precise and the gamma emission from the radioactive metals (109Cd and 65Zn) enables detection of extremely low metal concentrations (Salbu, 1987). In previous studies, subsamples were withdrawn from one of the soils, a soil weathered in situ from alum shales, at increasing contact time between 109Cd and 65Zn and the soil. These subsamples were used for sequential extraction (Almås et al., 1999). These results showed that the mobility of the recently added 109Cd and 65Zn decreased during the experimental period (0.5 to 8760 h), indicating an aging effect, and that increasing temperature facilitated the reduction of mobility of these isotopes. Results from the sequential extractions and investigations of the chemical lability of Cd and Zn (using anodic stripping voltammetry, ASV) in a dilute salt extract (0.01 M KNO3) of the two soils used showed that addition of organic matter increased the mobility of both the stable soil Cd and Zn (Almås et al., 2000a) and the radioactive 109Cd and 65Zn (Almås et al., 1999). Because the interaction between plants and the physico–chemical properties in the root zone is vital for metal uptake, this study was aimed at: (i) studying the plant uptake of the recently added 109Cd and 65Zn and their naturally existing counterparts, as influenced by temperature and organic matter addition to soil, and (ii) investigating the correlation between the physico–chemical forms of Cd and Zn in the soil and soil solution with their uptake by plants.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSION
 REFERENCES
 
Soils and Organic Matter Used
A pot experiment was conducted with two soils of different origins in a phytotron (climate-controlled growth chambers) at 9 and 21°C. These soils were amended with organic matter at the rates of 0 and 4% (w/w) and spiked with 109Cd and 65Zn. The source of organic matter was pig manure. Both soil types were placed under each temperature (9 and 21°C). For each soil, the experiment was run once at each temperature. All treatment combinations of soils, temperature, and organic matter were run in triplicates and placed in a randomized design. The experimental period was 1 yr. Ryegrass was sown in every pot and harvested twice. Subsamples of soil were collected from every pot at time intervals ranging from 0.5 h to 1 yr (8760 h) of contact time between 109Cd and 65Zn and the soils. Detailed description of the different experimental steps follows below.

One of the soils (Soil A) was a saprolite of alum shale bedrocks, collected from the Jønsberg Agricultural School farm in southeastern Norway. The alum shales are sulfide-bearing rocks formed in the Cambric era, and contain naturally high levels of a number of trace elements. Detailed mineralogical and chemical compositions of this soil are given in Jeng and Bergseth (1992). The other soil (Soil B) was a marine deposit soil of mixed mineralogy (dominated by Illite) of granitic and gneissic origin. This soil was collected from an uncultivated site at the Agricultural University of Norway farm, southeastern Norway. Some of the most relevant properties of these two soils are presented in Table 1. Soil A is classified as a Typic Cryoboroll and Soil B as a Humaquept (Soil Taxonomy, 1992). The total concentrations of Cd and Zn, and the relative amounts of the respective metals added to soil through the manure, are also presented in Table 1.


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  		Table 1. Important soil properties and the composition of organic matter added.

 
Pot Experiment
All nutrients were added on a soil volume basis to eliminate the variation in soil weight caused by the organic matter addition. The doses of N, P, K, Mg, Fe, Cu, Mn, B, and Mo were 120, 30, 120, 18.5, 10, 6.4, 8.1, 0.27, and 0.26 mg L-1 soil, respectively. The sources of N, P, and K were Ca(NO3)2 · 4H2O, Ca(H2PO4)2 · H2O, and KCl, respectively. For Mg, Fe, Cu, and Mn, their sulfate salts, Na2B4O7 · 10H2O (for B) and (NH4)6 Mo7O24 · H2O (for Mo), were used. All the fertilizers were applied in liquid form, and the required amounts of fertilizer solutions were thoroughly mixed with the soil of each pot. At the same time, the soils were also spiked and thoroughly mixed with a tracer solution of 109Cd2+ (specific activity: 1.24 x 105 kBq kg-1) and 65Zn2+ (specific activity: 1.45 x 105 kBq kg-1) (DuPont, Mechelen, Belgium), which were diluted with MilliQ water (Millipore, Bedford, MA) to 25 mL, added to the total soil volume of about 2.2 L (soil volume in pot), and the soil was moistened immediately after to 60% of field capacity (0.33 bar suction). The 25-mL spike was acidified to pH 2 to prevent adsorption of the tracers to the equipment surfaces, but this did not result in any noticeable change in soil pH. The addition of 109Cd and 65Zn was equivalent to 4 x 10-6 mg kg-1 soil, and the specific activity of 109Cd and 65Zn was estimated to be 500 and 600 kBq kg-1 soil, respectively. Except from the content of Cd and Zn in the organic matter source used (the pig manure, Table 1), no further application of Cd and Zn (e.g., as inorganic salts) was done.

In each pot, 0.4 g ryegrass seed was sown. The soil was watered with double distilled water to raise the moisture level to 60% of field capacity, and this level was maintained throughout the growing period by weighing the pots at regular time intervals and adding double distilled water equivalent to the loss of water. The aboveground parts of the whole ryegrass plants were harvested two times just before the flowering stage, and the harvested plant material was dried at 65°C and weighed prior to grinding it in a stainless steel mill.

Tension lysimeters were installed only in pots filled with Soil A at both temperatures (9 and 21°C) and organic treatment levels (0 and 4%). Soil solution was collected from these pots 8 mo after initiation of the experiment, and the gamma emission activity from 109Cd and 65Zn in the soil solution was determined by a Packard (Downers Grove, IL) Minaxi 3'' thorough-hole NaI Gamma Counter, 5000 Series.

Plant Sample Analysis
The activity of 109Cd and 65Zn in the ground plant samples was measured by a Packard Minaxi 3'' through-hole NaI Gamma Counter, 5000 Series. The total Cd and Zn concentrations were determined by graphite furnace atomic absorption spectrometry (AAS) and inductively coupled plasma (ICP), respectively, after digesting the plant material. The digestion was done by dry-ashing the plant samples at 450°C and treating them with a 1:2 concentrated HCl–HNO3 mixture. The heating and acid digestion step was done twice and the residue was then dissolved in 5 mL of 1:1 HNO3 and diluted to 50 mL by double distilled water. The presented data are all on a dry-matter basis (oven-dried overnight at 105°C).

Soil Analysis
Sequential Extractions
The soils used in this study were analyzed for a number of parameters, and the detailed descriptions of the analytical procedures and model setup are presented in previous publications (Almås et al., 1999; Almås et al., 2000b). However, a brief overview of the soil analysis is necessary for the following discussions. Sequential extractions were performed after the soils were spiked with 109Cd and 65Zn. Three-gram moist subsamples of soil were withdrawn from the pots at time intervals ranging from 0.5 h to 1 yr (8760 h) of contact time between the tracers and the soils. Each of these subsamples was extracted sequentially by H2O (F1), 1 M NH4OAc at soil pH (F2), 1 M NH4OAc at pH 5 (F3), 0.04 M NH2OH · HCl (F4), 30% H2O2 (F5), and finally by 7 M HNO3 (F6). This is a fractionation procedure developed by Salbu et al. (1998), which is modified from that described by Tessier et al. (1979). Soil samples for sequential extractions of Soil B were withdrawn only after 1 yr of contact time, because this soil was not used for studying the kinetics of 109Cd and 65Zn interactions with soil (Almås et al., 2000a). The initial fractions from sequential extractions can be used to assess the potential short-term biological uptake of soil metals, and the fraction of metals that is readily displaced from the reversible sorption phases (physical and electrostatic sorption) can thus be regarded as the mobile fraction. Metals associated with the three first fractions, recovered by H2O (F1) or by exchange reactions (F2 and F3), are referred to as mobile. The immobile fractions refer to those fractions where dissolution of the ligand by redox agents and strong acids was necessary to liberate the metals (F4, F5, and F6). The change in partitioning of 109Cd and 65Zn during the experimental period between the water-soluble (F1), the reversibly sorbed fractions (F2 and F3), and the irreversibly sorbed fractions (F4–F6) was used in a three-component model to calculate the rate of 109Cd and 65Zn transfer among the three components as influenced by the organic matter content and temperature change (Almås et al., 2000b). A Packard Minaxi 3'' thorough-hole NaI Gamma Counter, 5000 Series, was used for the analysis of 109Cd and 65Zn in the extracts. Stable Cd and Zn concentrations in the same extracts were also determined, but only in extracts from Soil A, by using graphite furnace atomic absorption spectrometry (AAS) and inductively coupled plasma (ICP), respectively.

All funnels and containers used during the analysis were of polycarbonate, and the equipment was soaked in 10% HCl and thoroughly rinsed in MilliQ water prior to use.

Reproducibility of Results and Presentation of Data
Every treatment combination was run in triplicate, and plant samples were harvested twice from each of them. Possible contamination from the equipment used and the surroundings during digestion and analysis were corrected for by the use of blanks. Analysis of variance and paired t-tests were done using JMP 3.1 (SAS Institute, 1995), and the level of significance was 95%. Graphical presentations were performed by Origin 5.0 (Microcal Software, 1997).


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSION
 REFERENCES
 
Reactions in Soils and Metal Uptake
It was shown in the sequential extraction experiment that soil sorption of the spiked 109Cd and 65Zn was rapid. After 0.5 h contact time between 109Cd and 65Zn and the soils, <1% of the total 109Cd and 65Zn was recovered in the F1 fraction, and <10% and <5% of 109Cd and 65Zn, respectively, were recovered in the F2 fraction (Almås et al., 1999). The investigations about the kinetics of reactions related to the geochemical partitioning of 109Cd and 65Zn added to Soil A used, indicated that the reversible sorption (the transfer of 109Cd and 65Zn from F1 to F2 and F3) of the tracers occurred rapidly, and the pseudoequilibrium was attained within 0.5 h, while the transfer of reversibly sorbed 109Cd and 65Zn (F2 and F3) into the irreversibly sorbed (F4–F6) fractions was a significantly slower process. The addition of organic matter reduced that rate of 109Cd and 65Zn transfer into the irreversibly sorbed fractions, whereas the transfer rate increased with increasing temperature (Almås et al., 2000b). At the start of the experimental period, the relative amount (in percent of total) of stable Cd and Zn in the mobile fractions (F1–F3) was 15 and 20% lower than that of 109Cd and 65Zn. However, this difference was reduced to only 8 and 9%, respectively, after 1 yr. This implies that, until equilibrium or at least pseudoequilibrium has been reached, Cd and Zn added to soil as inorganic ions may have a higher potential bioavailability then the corresponding metals naturally existing in soil.

The metal uptake by ryegrass from both soil types as affected by soil type, temperature, and organic matter addition, was tested by analysis of variance within each temperature and within each soil type. The test showed that soil type was the most significant factor affecting the metal uptake. The effect of temperature was also significant, whereas the addition of organic matter was significant only for the uptake of zinc. Interaction effect was found to be significant between soil type and organic matter addition for 65Zn (kBq kg-1 dry matter [DM] plant). The concentration of 65Zn was higher in plants grown in Soil B than those grown in Soil A, but the addition of 4% organic matter (OM) reduced the 65Zn tissue concentrations. More discussion about the main effects found to be significant is presented below under the effects of temperature and organic matter. The total plant uptake of 109Cd, Cd, 65Zn, and Zn from the two soils at different temperatures and organic matter levels is shown in Figs. 1 and 2. The concentrations of 109Cd and 65Zn (kBq kg-1 DM) as well as Cd and Zn (mg kg-1 DM) in the harvested ryegrass at different temperatures and organic matter levels are presented in Table 2.



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  		Fig. 1. Uptake of 109Cd (kBq pot-1) and Cd (µg pot-1) in ryegrass grown in two different soils as affected by temperature (9 and 21°C) and organic matter (OM) addition to the soils (0 and 4%). Each "corner" in the three-dimensional surface diagrams represents the mean of n = 6.

 


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  		Fig. 2. Uptake of 65Zn (kBq pot-1) and Zn (µg pot-1) in ryegrass grown in two different soils as affected by temperature (9 and 21°C) and organic matter (OM) addition to the soils (0 and 4%). Each "corner" in the three-dimensional surface diagrams represents the mean of n = 6.

 

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  		Table 2. The concentration of 109Cd, 65Zn, Cd, and Zn in ryegrass harvested at different temperatures and organic matter (OM) levels (n = 6).

 
Effect of Temperature
The uptake of 109Cd and 65Zn (Bq pot-1) and Cd and Zn (µg pot-1) in the aboveground plant parts increased with increasing temperature (Fig. 1 and 2), but this effect was significant only for the tissue metal concentrations, shown in Table 2. Although the DM yield was reduced significantly at 21°C as compared with that at 9°C (20–40% reduction, Table 3), no effect of isotopic dilution (109Cd and 65Zn) by the increased uptake of Cd and Zn with the higher temperature was noticed. Previous investigations on the mobility of 109Cd and 65Zn in Soil A, and analysis of 109Cd and 65Zn concentration in the soil solution collected (Fig. 3) showed that increasing temperature reduced the mobility and the soil solution concentration of these metal isotopes. This pot experiment thus indicates that the uptake of 109Cd and 65Zn is controlled not only by the extractability of 109Cd and 65Zn in the soil, but even more by the effect of temperature treatment on plant growth. It is expected that the conditions for plant uptake of Cd and Zn were more optimal at 21°C than at 9°C. Since the DM yield did not increase with temperature, the increased uptake of the investigated metals may have been due to improved root development. The lower DM yield (Table 3) at the higher temperature may be explained by the faster plant growth and higher evapotranspiration followed by higher moisture content in plant cells. It is expected that a higher rate of water flow through the plants result in higher concentration of cadmium and zinc in the plant tissue. A highly significant correlation between mass flow of Cd and Zn in soil (a soil weathered from alum shales) and evapotranspiration by plants (oat, radish, and spinach) was reported by Kashem and Singh (unpublished data, 2000).


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  		Table 3. The ryegrass yield (g pot-1) of the two harvests from both temperature (9 and 21°C) and organic matter (OM) treatment levels (0 and 4%).

 


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  		Fig. 3. Concentrations of 109Cd and 65Zn (Bq mL-1) in soil solution extracted by tension lysimeters in the untreated and the organic matter–treated Soil A at 9 and 21°C. Each bar represents the mean of n = 3.

 
Organic Matter
The addition of organic matter increased the Cd and 109Cd uptake from both soils (Fig. 1) and similar effects of organic matter addition were also observed for the Zn uptake, except for the reduced uptake of Zn in Soil A at 9°C (Fig. 2). Reduced DM yield in the organic matter–treated soil seems to reduce the uptake of Zn at 9°C in Soil A. The Zn uptake (mg kg-1 DM), being the product of Zn concentration and DM yield, was thus reduced accordingly. No such effect of organic matter addition on DM yield was found in the other treatment combinations. The uptake of 65Zn from both soils and at both temperatures was, however, reduced by the organic matter addition. This is probably the result of isotopic dilution of 65Zn as the amount of stable Zn in plant tissues in general increased with the organic matter treatment.

Although the uptake of Cd and Zn in general increased with organic matter addition, the effect was found to be significant only in Soil B. Soil A is originally rich in organic matter (5% total organic carbon), and the addition of 4% organic matter may thus only have increased the metal uptake to a limited extent. These two soils have, in a parallel experiment, been treated with 0.01 M KNO3, and due to low soil pH in Soil B, the concentrations of Cd and Zn were many times higher in the 0.01 M KNO3 extracts from this soil than in those of Soil A (Almås et al., 2000a). The addition of organic matter to Soil B may thus have increased the uptake in two ways. First, the addition of soluble organic acids may have competed with other reversible sorption phases for the metals, thereby increasing the potential mobility of the investigated metals by formation of soluble organo–metallic complexes. Second, the addition of fresh pig manure, which was the organic matter source used, improved the growth conditions through the additional nutrients provided and, by this practice, increased the uptake of Cd and Zn. Although the organic matter source provided contained Cd and Zn, the addition of these metals was relatively small as compared with the amount of naturally present metals in Soil A. The corresponding addition of metals through the organic matter was in the range of 2 and 9% for Cd and Zn, respectively, in Soil B (Table 1). Statistical analysis of total Cd and Zn in both soils (paired t-tests) showed that only Cd was significantly increased (by 7%) in the organic matter–treated soils as compared with the untreated soils. The total Zn concentrations were not changed significantly. It is unlikely that the entire amounts of Cd and Zn in the added organic material were liberated to the soil solution. It is, for instance, noteworthy that the increased Zn uptake in a crop grown in the organic matter–treated loam soil as compared with that grown in the untreated soil was in the range of 60 and 70% at 9 and 21°C, respectively.

Characterization of Mobility and Lability
Detailed investigations of Soil A (Almås et al., 1999), the soil weathered from alum shales, showed that the addition of organic matter not only increased the 109Cd and 65Zn concentrations in the mobile fractions (recovered in the F1–F3 fractions, Table 4) and in the soil solution (Fig. 3) but also the total organic carbon (TOC) concentrations in the water extracts (Almås et al., 1999). These two soils were in a parallel experiment treated with ultrapure 0.01 M KNO3, and the concentrations of labile Cd and Zn ions in the extracts were detected by the use of differential pulse anodic stripping voltammetry (Almås et al., 2000a). The concentrations of Cd and Zn ions detected by the electrode are defined as being ASV-labile. These analyses indicated that the addition of organic matter not only lead to increased concentrations of soluble Cd (from 0.043 to 0.093 and from 0.13 to 0.14 µmol kg-1 soil in 0.01 M KNO3 extracts of Soil A and Soil B, respectively), but also the concentration of the ASV-labile Cd fraction was increased (from 0.0044 to 0.0089 and from 0.026 to 0.043 µmol kg-1 soil in extracts of Soil A and Soil B, respectively). The concentration of soluble Zn increased correspondingly with the organic matter addition (from 1.69 to 5.76 and from 22.83 to 23.93 µmol kg-1 soil in extracts of Soil A and Soil B, respectively), but the ASV lability of Zn was reduced significantly (from 0.71 to 0.39 and from 4.97 to 4.21 µmol kg-1 soil in extracts of Soil A and Soil B, respectively). It was assumed that the non-ASV-labile fraction of the total soluble Cd and Zn was complexed with dissolved organic matter. Since the uptake and solubility of Zn in these soils was increased by the organic matter addition, while the ASV-labile fraction was decreased in the same soil types as used in this pot experiment, it is possible that a fraction of the inert metal–organic complexes was available to plants. It seems that Zn was liberated at the root surface to a greater extent than that predicted by the diffusion of Zn into the mercury electrode (the reacting electrode of the differential pulse ASV instrumentation), and hence the ASV-labile Zn fraction did not predict the bioavailable Zn fraction satisfactorily. Alternatively, the metal–organic complexes were taken up more or less intact by the plant roots. Evidence for uptake of metal complexes by plants is found for both Cd (McLaughlin et al., 1997) and Zn (von Wiren et al., 1996). Thus, one may speculate that the uptake of Zn, and possibly also Cd, was facilitated by the formation of metal–organic complexes.


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  		Table 4. Relative distribution (% of total recovered in all fractions, F1–F6) of 109Cd and 65Zn recovered in the F1, F2, and the F3 extracts from Soil A and Soil B as affected by temperature and addition of organic matter (OM). The values shown are mean values ± standard deviation (n = 3).

 
Effect of Soil Types and Properties
Although the concentration of stable Cd and Zn was higher in the F1 extracts from Soil B, the uptake of these elements was not higher in the crop grown in this soil as compared with Soil A. Rather, the opposite was true: the uptake of Cd and Zn was in fact significantly higher in plants grown in Soil A. In spite of the fact that the extractability of Cd and Zn was higher in the acidic loam soil, the total concentrations of these metals in soil were significantly higher in Soil A (Table 1), and consequently also the Cd and Zn uptake. It has been reported by Eriksson et al. (1996) from a survey of Swedish field investigations, that soil pH, but even more the Cd level in soil, were the most important factors controlling the uptake. The uptake of the recently added 109Cd and 65Zn was, on the other hand, significantly higher in the crop grown in Soil B as compared with that grown in Soil A. Since the radioactive elements are nonexistent in the natural soil environment, there is no large solid-phase pool providing the soil solution and the plant roots with 109Cd and 65Zn over time, thus the lower content of soil organic matter is more important at the substantially lower soil pH (Table 1) of Soil B. This most likely explains the higher solubility and uptake of 109Cd and 65Zn by the ryegrass in this soil. It is known that soil solution pH has a distinct effect on total concentrations of trace metals in the soil solution, due to its effect on surface charges and the hydrolysis of metal cations (McBride, 1989).

Pickering (1998) stated that the early stages in a multistep extraction sequence could provide information comparable with those obtained from a single extraction method. Taking this into consideration, the correlation between plant uptake and the concentrations of 109Cd and 65Zn in the three mobile fractions (F1–F3) was worked out. The results showed that the uptake of 109Cd and 65Zn was positively and significantly correlated with the F1, F2, and F3 fractions in the soils, with a few exceptions. The correlations were improved by correcting for temperature treatment differences. Although the metal concentrations in these soil fractions (F1–F3) were better correlated with the uptake of 109Cd (r2 ranging from 0.69 to 0.91) than with that of 65Zn (r2 ranging from 0.21 to 0.52), the correlations were significant for both metals. Among the soil fractions tested, the F2 fraction was generally best correlated with plant uptake. These statistical tests were made on the data obtained from the soil samples withdrawn after 1 mo (only alum shale soil) and 1 yr (both soils) of contact time between 109Cd and 65Zn and the soils (Table 4), and by using the plant uptake data from both harvests.


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSION
REFERENCES
 
The plant uptake of recently added 109Cd and 65Zn and aged Cd and Zn (naturally existing) from two mineral soils was significantly affected by temperature (9 or 21°C) and addition of organic matter (4% w/w) to soils. The solubility of both the recently added metals and the natural existing Cd and Zn was highest in extract of the marine-deposited soil (Soil B), due to the substantially lower pH and organic matter content of that soil. The uptake of 109Cd and 65Zn was also highest from Soil B, whereas the uptake of the natural existing Cd and Zn was influenced even more by the total metal concentrations of the soil, hence the uptake of Cd and Zn was much higher from the alum shale–weathered soil (Soil A) containing about 10 times as much Cd and Zn as Soil B. It implies that the added metals (109Cd and 65Zn) had not attained equal distribution in the soil fractions (F1–F6) as the natural existing metals, thus temporarily being more mobile. This also suggests that the uptake of newly added metals is more controlled by the soil solution properties (like pH and total organic carbon concentration) than the existing metals. The uptake of the latter is influenced by soil pH, but even more by the total metal concentration in the soil (Eriksson et al., 1996).

Increasing temperature increased the retention of 109Cd and 65Zn in soil, but since the plant uptake also increased, it is suggested that the temperature effect on plant growth controls the uptake more than the slight reduction of 109Cd and 65Zn extractability detected.

The organic matter addition lead to increased mobility of 109Cd, Cd, 65Zn, and Zn in soil, and their uptake by plants was also increased. Since the uptake and extractability of Zn in these soils was increased by the addition of organic matter, while the fraction of ASV-labile Zn was decreased, it is suggested that a fraction of the dissolved inert metal–organic complexes was available to plants. Due to the fact that the mobile fractions (F1, F2, and F3) of 109Cd and 65Zn in the soils were significantly correlated with the uptake in ryegrass, fractionation of solid phases and speciation of metals in soil solution can provide valuable information about their bioavailability.


   ACKNOWLEDGMENTS
 
The Research Counsel of Norway supported the research through a fellowship to the senior author, and this assistance is gratefully acknowledged. The first author wishes to thank professor Brit Salbu and her personnel at the Dep. of Chemistry and Biotechnology for valuable assistance during the laboratory experiments.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSION
 REFERENCES
 





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