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Australian Journal of Soil Research Volume 38, 2000 © CSIRO 2000

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Aust. J. Soil Res., 2000, 38, 991–1004

Speciation and phytoavailability of cadmium in selected surface soils of South Australia G. S. R. KrishnamurtiA and R. Naidu CSIRO Land and Water, PMB 2, Glen Osmond, SA 5064, Australia. A Corresponding author; email: [email protected]

Abstract A modified sequential extraction scheme was developed for partitioning the particulate-bound cadmium (Cd) into 9 fractions: exchangeable, carbonate-bound/specifically adsorbed, metal–fulvic acid-complexbound, metal–humic acid-complex-bound, easily reducible metal oxide-bound, organic-bound, amorphous mineral colloid-bound, crystalline Fe oxide-bound, and detrital (bound to mineral lattices). Results on 11 surface soils showed that Cd in these soils was predominantly present in detrital form, bound to the mineral lattices, accounting for 15.8–61.9%, with an average of 33.4%, of the total Cd in the soils. The average relative abundance of Cd bound to the different particulate forms in the soils is in the order: detrital (0.077 mg/kg) > specifically adsorbed/carbonate-bound (0.066 mg/kg) > organic-bound (0.033 mg/kg) > metal–fulvic acid-complex-bound (0.031 mg/kg) > easily reducible metal oxide-bound (0.019 mg/kg) > exchangeable (0.013 mg/kg) > metal–humic acid-complex-bound (0.011 mg/kg) > crystalline Fe oxide-bound (0.001 mg/kg) ≥ amorphous mineral colloid-bound (0.001 mg/kg). The phytoavailable Cd content was determined as Cd concentration in the shoot and leaf of durum wheat plants grown on the soils in a greenhouse study. Statistical treatment of the data showed that the exchangeable Cd (r = 0.735, P = 0.01) and the metal–fulvic acid-complex-bound Cd (r = 0.824, P = 0.002) correlated significantly with the plant-available Cd, compared with other species. The exchangeable and fulvic acid fraction of the metal–organic-complex-bound Cd contents, together, could explain 91.5% of the variation in plant-available Cd, determined as Cd concentration in leaf and stem of the durum wheat plants (r = 0.956, P = 0.0001). The significance of metal–fulvic acid complexes on Cd phytoavailability has not been reported so far and needs in-depth research in explaining the toxicity and food chain contamination of Cd in the environment. Additional keywords: metal–fulvic acid complexes, availability, wheat.

Introduction Toxic metal contamination of soil poses a major environmental and human health concern. The specific form and reactivity of their association with the reactive components of the soil determine the ecotoxicological significance of the environmental impact of heavy metals in soils. Estimation of plant transfer and prediction of long-term effects on soil solution and ground water quality should therefore be based on the proportion of the potentially ‘active species’ of the heavy metals. Qualitative assessment of these fractions involves speciation of both the soil solution and the particulate-bound species of the soils. The distribution of trace elements among soil components such as organic matter or hydrous metal oxides is important for assessing the potential of soil to supply sufficient micronutrients for plant growth and to retain toxic quantities of trace metals, and for determination of amelioration procedures for soils at risk of causing trace metal contamination. Metal cations may be soluble, readily exchangeable, complexed with organic matter or hydrous oxides, substituted in stoichiometric compounds, or occluded in © CSIRO 2000

10.1071/SR99129 0004-9573/00/050991

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G. S. R. Krishnamurti and R. Naidu

mineral structures. Delineating the speciation of metals in soils is considered essential for understanding the mobility, bioavailability, and toxicity of the metals, and for developing useful environmental guidelines for potential toxic hazards (Davies 1980, 1992). The procedure used extensively by environmental researchers for the speciation of particulate-bound heavy metals in soils is that of Tessier et al. (1979), with minor variations (reviews by Ross 1994; Sheppard and Stephenson 1997). Krishnamurti et al. (1995) proposed a modified sequential extraction speciation scheme, which delineated the species as: exchangeable; specifically adsorbed; bound to metal–organic complexes, easily reducible metal oxides, organics, amorphous mineral colloids, and crystalline Fe oxides; and residual. Following the sequential extraction scheme of Krishnamurti et al. (1995), the cadmium (Cd) in selected temperate soils of southern Saskatchewan, Canada (Krishnamurti et al. 1995, 1997), and tropical soils of Kenya (Onyatta and Huang 1999) was reported to be predominantly the metal–organic-complex-bound species. The importance of the metal–organic-complex-bound Cd species in determining the Cd bioavailability index of the temperate soils of Saskatchewan was shown by Krishnamurti et al. (1995). Cadmium uptake by the plant is a dynamic process. As the plant takes up Cd, the equilibrium Cd concentration in the soil solution is maintained from the input of Cd from the particulate-bound species. Thus, the Cd concentration in soil solution is controlled by the nature of particulate-bound Cd species in the soils. The speciation of particulatebound Cd in soils of Australia, developed under a Mediterranean climate, is a neglected area of study. The objectives of this paper were (i) to report the solid-state speciation of Cd in a few typical soils of South Australia, with a wide range of chemical and physicochemical properties, following a scheme similar to that of Krishnamurti et al. (1995); and (ii) to investigate the relative importance of the Cd species in influencing the Cd uptake by the plant. Materials and Methods Characteristics of the soils Selected characteristics of the soils used in the study are presented in Table 1. The soils selected are representative of typical soils encountered in South Australia and are not contaminated with known anthropogenic inputs. The soil samples, collected from the surface horizon (0–15 cm), were air-dried and ground to pass through a 2-mm sieve, homogenised, and stored for subsequent analysis. The pH of the soils in water (1 : 2) was measured using an Orion Model 720 A pH meter (Orion Research Inc., Boston, MA). The electrical conductivity (EC) of the soil–water suspensions (1 : 5) was measured using an Orion Model 160 conductivity meter (Orion Research Inc., Boston, MA). Mechanical analysis of the soils was carried out by gravity sedimentation (Jackson 1979) after dispersion of the soils with 5% sodium hexametaphosphate. Total C and inorganic C contents of the soils were determined using a Leco CNS2000 analyser (Leco Corp., St Joseph, MI) and following the method of Loveday and Reeve (1974), respectively. The organic C content was deduced from the difference between the two values. The free Fe and ‘amorphous’ Fe contents of the soils were determined following the methods of Mehra and Jackson (1960) and Schwertmann (1964), respectively. The mineralogy of the clay ( easily reducible metal oxide-bound (0.019 mg/kg) > exchangeable (0.013 mg/kg) > metal–humic acid-complex-bound (0.011 mg/kg) > crystalline Fe oxide-bound (0.001

0

50

100

150

200

Amount of particulate-bound Cd species (µg/kg)

Fig. 1. Distribution of particulate-bound Cd species in the soils studied, following the modified sequential extraction scheme.

Speciation and phytoavailability of Cd

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mg/kg) ≥ amorphous mineral colloid-bound (0.001mg/kg). The average percent distribution of the particulate-bound Cd species in the soils studied is presented in Fig. 2. The Cd bound to the amorphous mineral colloids and to the crystalline Fe oxides was, together, less than 1% of the total Cd, and hence was not shown in the figures. In this study, the exchangeable Cd content was, on an average, approximately 5.8% of the total Cd in the soils. The exchangeable Cd content in the temperate soils of Canada (Krishnamurti et al. 1995) and the tropical soils of Kenya (Onyatta and Huang 1999) was reported to be negligible. This may be due to the differences in the weathering regime and the parent material, which have a profound influence on the formation of the soils and in the distribution of Cd amongst different reactive components. The Cd in the surface horizons of the temperate soils of Canada (Krishnamurti et al. 1997) and the tropical soils of Kenya (Onyatta and Huang 1999) was reported to be present mainly in the metal–organic-complex-bound form. The Cd in the soils used in the present study, however, is predominantly present in the detrital fraction, bound to the mineral lattices, accounting for 15.8–61.9%, with an average of 33.4%, of the total Cd present in the soils, and is considered as not readily available. Cadmium present as metal–organic-complex-bound species in these soils, ranging between 0.016 and 0.098 mg/kg, was predominantly bound to the fulvic acid fraction of the organic matter, accounting for 48.3–95.2%, with an average of 72.9% of the species. Speciation and phytoavailability The Cd species contributing most towards the phytoavailable Cd was identified using correlation analysis of the data. The exchangeable Cd (r = 0.735, P = 1.0 × 10–2) and the fulvic acid fraction of the metal–organic-complex-bound Cd (r = 0.824, P = 1.8 ×10–3) correlated significantly with the plant-available Cd, compared with other species (Table 4). Fulvic acid-bound Cd correlated (r = 0.824, P = 1.8 × 10–3) at least 2 orders of magnitude better than humic acid-bound Cd (r = 0.168, P = 6.2 × 10–1) with the plantavailable Cd, determined as Cd concentration in leaf and stem of durum wheat plants

Fig. 2. Average percent distribution of particulate-bound Cd species in the soils studied following the modified sequential extraction scheme.

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Table 4.

Data on the multiple regression analysis between plant-available Cd (Cd concentration in leaf and stem of the plant) and the particulate-bound Cd species of the soils (following the method of Krishnamurti et al. 1995 as modified) The values in parentheses under the correlation coefficients are the levels of significance

Simple correlation analysis:

Plant-available Cd

Metal–organic complex-bound 0.761 (6.5 × 10–3)

Exchangeable

Detrital

0.735 (1 × 10–2)

0.446 (1.7 ×10–1)

Fulvic acid bound 0.824 (1.8 × 10–3)

Humic acid bound 0.168 (6.2 × 10–1)

Easily reducible metal oxide-bound –0.239 (4.8 × 10–1)

Specifically adsorbed –0.219 (5.2 × 10–1)

Organic-bound –0.453 (1.6 × 10–1)

Multiple regression analysis: Plant-available Cd = 0.0004 + 3.5676. Exchangeable Cd + 2.6500. Fulvic acid-bound Cd

(Eqn 1) (Eqn 2)


Plant-available Cd (Y) = 0.0645 + 2.8734. Exchangeable Cd + 2.5746. Fulvic acid-bound Cd - 0.0079 pH

R2 = 0.915 (P = 0.0001) R2 = 0.919 (P = 0.0003)


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0.30

Calculated leaf Cd concentration (mg/kg)

0.25

0.20

0.15

0.10

0.05 y = 0.010 + 0.917x

0.00 0.00

0.05

0.10

0.15

0.20

r 2 = 0.917

0.25

0.30

Observed leaf Cd concentration (mg/kg)

Fig. 3. Relationship between the observed and calculated concentration of Cd in the leaf and stem of durum wheat crop plants.

(Table 4). The importance of the fulvic acid-bound Cd fraction of the metal–organic complex-bound Cd species in assessing the plant-available Cd was earlier suggested by Krishnamurti and Huang (1999) based on the 13C CPMAS NMR and ESR spectroscopic analysis of the fulvic acid fraction, in the temperate soils of Saskatchewan, Canada. The Cd associated with the simple organic C molecules in the fulvic acid fraction of the metal–organic complexes is apparently more mobile and easily available to the plant than the Cd associated with the high molecular weight humic acid fraction (Cabrera et al. 1988; Krishnamurti and Huang 1999). The role of fulvic–metal complexes in Cd phytoavailability has not been established so far. The relative role of the pH and the particulate-bound Cd species on the plant-available Cd in these soils was assessed using multiple regression analysis of the data. The exchangeable and fulvic acid fraction of the metal–organic-complex-bound Cd contents, together, could explain 91.5% of the variation in plant-available Cd, determined as Cd concentration in leaf and stem of the durum wheat plants (r = 0.956, P = 1 × 10–4) (Eqn 1, Table 4). Inclusion of pH in the regression analysis did not significantly improve the coefficient of determination (r = 0.959, P = 3 × 10–4) (Eqn 2, Table 4). Further, the step-wise regression analysis of the speciation data, together with pH, had also shown that only the fulvic acid fraction of the metal–organic-complex-bound Cd and exchangeable Cd are significant in controlling the leaf Cd concentration. The leaf Cd concentration calculated using the regression equation (Eqn 1, Table 4) was highly significantly correlated (r2 = 0.917, P < 0.00001) with the observed leaf Cd

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concentrations (Fig. 3). The analysis showed that the leaf Cd concentration could be assessed using the data on the amounts of the exchangeable Cd and the fulvic acid fraction of the metal–organic-complex-bound Cd species. The significance of metal–fulvic acid complexes on Cd phytoavailability has not been reported so far and needs in-depth research in explaining the toxicity and food chain contamination of Cd in the environment. Conclusions The total Cd content of the soils used in the present study varied between 0.117 and 0.365 mg Cd/kg soil. About 77% of the variation in total Cd content of the soils can be explained satisfactorily by using the soil factors free Fe and organic C contents, and soil pH. Data on the speciation of particulate-bound Cd in the soils obtained using the modified sequential extraction scheme developed in this study, on 11 surface Mediterranean soils of South Australia, showed that Cd in these soils was predominantly present in the detrital form bound to the alumino-silicate lattice minerals, accounting for 33.4% of the total Cd, and can be considered as not readily available to the plant. Cadmium present as metal–organic-complex-bound species in these soils, ranging between 0.016 and 0.098 mg/kg, was predominantly bound to the fulvic acid fraction of the organic matter, accounting for 48.3–95.2%, with an average of 72.9% of the species. The plant-available Cd content was determined as Cd concentration in the shoot and leaf of durum wheat plants grown on the soils in the greenhouse study. Statistical treatment of the speciation and plant-uptake data showed that the exchangeable Cd (r = 0.735, P = 0.01) and the fulvic acid fraction of the metal–organic-complex-bound Cd (r = 0.824, P = 0.0018) correlated significantly with the plant-available Cd, compared with other species. The exchangeable and fulvic acid fraction of the metal–organiccomplex-bound Cd contents, together, could explain 91.5% of the variation in plantavailable Cd, determined as Cd concentration in leaf and stem of the durum wheat plants (r = 0.956, P = 0.0001). The significance of metal–fulvic acid complexes on Cd phytoavailability has not been reported so far and needs in-depth research in explaining the toxicity and food chain contamination of Cd in the environment. Acknowledgments The financial assistance provided by the Grains Research and Development Corporation during the course of this study is gratefully acknowledged. References Brady NC (1974) ‘The nature and properties of soils.’ 8th edn. pp. 71–110. (Macmillan: New York) Cabrera D, Young SD, Rowell DL (1988) The toxicity of cadmium to barley plants as affected by complex formation with humic acid. Plant and Soil 105, 195–204. Cieslinski G, Van Rees KCJ, Huang PM, Kozak LM, Rostad HPW, Knott DR (1994) Cadmium uptake and bioaccumulation in selected cultivars of durum wheat and flax as affected by soil type. Plant and Soil 182, 115–124. Davies BE (1980) Trace element pollution. In ‘Applied soil trace elements’. (Ed. BE Davies) pp. 287–351. (John Wiley: Chichester) Davies BE (1992) Trace elements in the environment: retrospect and prospect. In ‘Biogeochemistry of trace metals’. (Ed. DC Adriano) pp. 1–17. (Lewis Publishers: Boca Raton, FL) Florijn PJ, Van Beusichem MJ (1993) Uptake and distribution of cadmium in maize inbred lines. Plant and Soil 150, 25–32. Gardiner J (1974) The chemistry of cadmium in natural water—I. A study of cadmium complex formation using cadmium specific ion electrode. Water Research 8, 23–30.


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Manuscript received 10 November 1999, accepted 27 March 2000

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