Plant and Soil 222: 51–58, 2000. © 2000 Kluwer Academic Publishers. Printed in the Netherlands.
51
Uptake and partitioning of cadmium by cultivars of peanut (Arachis hypogaea L.) M.J. McLaughlin1,∗, M.J. Bell2 , G.C. Wright2 and G.D. Cozens1 1 CSIRO
Land and Water, Glen Osmond, South Australia and 2 Queensland Department of Primary Industries, J Bjelke-Petersen Research Station, P.O. Box 23, Kingaroy Qld. 4610, Australia Received 28 April 1999. Accepted in revised form 21 February 2000
Key words: cadmium, Arachis hypogaea, genotypic variation, split pot, translocation
Abstract Cadmium has been found to accumulate in peanut (Arachis hypogaea) kernels to levels exceeding the current maximum permitted concentration in Australia of 0.1 mg kg−1 . Little is known of the mechanisms of Cd uptake into kernels by cultivars of peanut, so the aims of the experiments reported here were to determine if Cd is absorbed directly through the pod wall or via the main root system, and if differences exist between cultivars in this respect. Split-pot soil and sand/nutrient solution experiments were performed with two cultivars of peanut (cv. NC7 and Streeton) known to accumulate Cd to different levels in the kernel. The growth medium was separated into pod and root zones with Cd concentrations in each zone varied. In confirmation of previous field trial results, cv. NC7 had higher concentrations of Cd in kernels, given the same Cd levels in the external medium (solution or soil). Despite total Cd uptake by cv. NC7 being similar to cv. Streeton, cv. NC7 appeared to retain more Cd in the roots and translocate less Cd to shoots. Results from both soil and sand/solution culture indicated that the dominant path of Cd uptake by peanut was via the main root system, with direct pod uptake contributing less than 5% of the total Cd in the kernel. There was little difference between cultivars in this characteristic. This indicates that unlike Ca nutrition of peanuts, agronomic techniques to manage Cd uptake will require modification of soil to the full depth of root exploration, rather than just the surface strata where pods develop. Cadmium concentrations in testa were up to an order of magnitude higher than in the kernel, indicating that blanching of kernels would be effective in reducing Cd in the marketed product.
Introduction Of all the heavy metals, cadmium (Cd) is recognised to be the metal posing the most threat to agricultural food quality, due to its mobility in the soil-plant system (Chaney and Oliver, 1996). Cadmium is added to soils in Australia principally through addition of phosphatic fertilizers containing Cd as an impurity (McLaughlin et al., 1996). While there have been significant reductions in amounts of Cd added to soils from this source over the last 10 years, Cd concentrations in most fertilized soils are still slowly increasing with time. ∗ FAX No: 8 8303 8565.
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Concentrations of Cd in food commodities are monitored through the National Residue Survey (Anon, 1992) and the Australian Market Basket Survey (Stenhouse, 1992), and food Cd concentrations are regulated through standards produced by the Australia–New Zealand Food Authority (ANZFA). Recently Bell et al. (1997) identified peanuts as accumulating significant concentrations of Cd on soils in new production areas in coastal Queensland, Australia. Currently, the maximum permitted concentration (MPC) for Cd in peanuts (Arachis hypogaea) is 0.1 mg kg−1 on a ‘food as consumed’ basis. In their studies, Bell et al. (1997) found Cd concentrations in kernels of up to 0.67 mg kg−1 . Understanding of Cd uptake mechanisms by peanuts is therefore an im-
52 portant prerequisite to designing effective agronomic control strategies. At present, little is known of the Cd uptake characteristics of peanuts. From analysis of plants growing under field conditions Bell et al. (1997) showed that significant differences exist between cultivars of peanut in terms of Cd accumulation in kernels. These authors also found that peanut shoots contained concentrations of Cd four to five times higher than concentrations in kernels, with up to half of the Cd in the kernel contained in the testa. From comparisons of Cd accumulation by peanuts and other grain legumes grown in field and glasshouse conditions, Bell et al. (1997) speculated that peanuts may be accessing Cd from deeper layers in the soil profile. By contrast, Bledsoe et al. (1949) convincingly demonstrated that calcium (Ca) enters the peanut kernel mainly through direct uptake by root hairs on the pods, and Zharare et al. (1993) presented data which suggested some zinc (Zn) uptake can occur in a similar fashion. This study was undertaken to address the hypothesis that peanuts take up Cd mainly through the true root system, deeper in the soil profile. Materials and methods Split-pot soil experiment A pot study using field soils was undertaken to investigate the zone of uptake of Cd in the profile, and the relative bioavailability of Cd in different soils cropped to peanuts with the root zone split into ‘pod’ and ‘root’ compartments similar to Wright (1989). Soils with varying Cd contents and Cd bioavailabilities were used in either the pod or root zones, with extra Cd applied using diammonium phosphate (DAP) fertiliser containing varying levels of Cd (see below). Three soils were chosen on the basis of their differences in phytoavailable Cd concentrations; ‘low’, ‘medium’ and ‘high’ (Table 1). Acid-washed sand was used as a very low total and bioavailable Cd medium in podding zones only (‘zero’ treatment). Two split-pot experiments using soils were performed using cv. Streeton. The first (Experiment A) examined the effect of soil type on Cd concentrations in kernels with no stratification of the pod/root zone, to confirm that the Cd availability assessed by chemical extraction was valid. The second experiment (Experiment B) examined various combinations of root and pod zone materials to determine whether Cd uptake was principally via the root or the pod (Table 2).
Amounts of (air dry) soil used in the root zone varied from 11.0–12.5 kg depending on soil type, with pod zones having 2.2 to 2.8 kg soil. All pod and root zones were treated with DAP at a rate equivalent to 37.3 mg P kg−1 soil and contained either low (<32.5 mg Cd kg−1 P) or high (375 mg Cd kg−1 P) levels of Cd, with the high and low Cd treatments designated as ‘with’ or ‘without’ added Cd, respectively. All pod zones received an application of analytical grade CaSO4 at a rate of 1.6 g kg−1 to ensure adequate calcium availability for kernel development, while all root zones received an application of analytical grade KCl to provide 12.5 mg K kg−1. Plants were harvested after 120 days growth and mature pods removed from the soil for analysis. Sand/nutrient solution experiment To enable further control of the Cd supply to various sections of the peanut root system, plants were grown in a sand/nutrient solution culture system, with the root zone split into pod and root compartments as detailed above. Quartz sand was repeatedly washed in 1.0 M HNO3 to remove clay and silt-sized materials and to remove any trace elements from the supporting growth medium. After acid washing the material was rinsed with deionised water, dried at 40 ◦ C in a forced air oven and sieved <2 mm over a stainless steel sieve. Free draining pots were filled with 18 kg sand and the sand leached with four litres of a nutrient solution containing calcium (Ca) 1 mM, magnesium (Mg) 0.2 mM, potassium (K) 2.0 mM, sodium (Na) 20 µM, nitrogen (N) 1.2 mM, sulfur (S) 1.0 mM, phosphorus (P) 1 µM, boron (B) 100 µM, copper (Cu) 1 µM, cobalt (Co) 0.4 µM, iron (Fe) 100 µM, manganese (Mn) 1.0 µM, molybdenum (Mo) 0.2 µM and Zn 5.0 µM. This pot comprised the ‘root’ zone. Two seeds of either cv. Streeton or NC7 were planted in the centre of the pot, and the pots placed in a naturally lit greenhouse on 26th September 1995. Pots were watered with deionised water once, and after seeds had germinated and emerged, seedlings were thinned to one per pot. Eight days after planting, a plastic pot with a hole in the centre was placed over the emerging seedling, the hole sealed and 3.5 kg sand placed in the upper pot covered with a layer of alkathene beads (‘pod’ zone). The pod zone was wetted to −10 kPa with nutrient solution treatments, while the root zone was flooded with nutrient solution.
53 Table 1. Soil classification and selected chemical characteristics of soils and acid-washed sand. Soil OrderA
Soil (Cd level) High Medium Low Zero
Alfisol Alfisol Oxisol Acid washed sand
pH
Org. CB
Clay
CECC
%
%
%
cmol+ kg−1
Extractable PD mg kg−1
15 4 65 <0.1
5.1 3.2 17.9 <0.2
37 31 20 <1
6.0 0.6 6.1 0.6 5.9 1.3 5.6 <0.1
CaCl2 CdE µg kg−1 5 3 <1.25 <1.25
EDTA CdF µg kg−1
Total CdG µg kg−1
EDTA ZnF mg kg−1
38.7 22.5 58.7 <5
43.6 31.8 67.4 <5
1.1 0.7 27.9 <5
A Soil Survey Staff (1992). B Walkeley and Black method (Rayment and Higginson, 1994). C 1.0 mol L−1 ammonium acetate at pH 7.0 (Rayment and Higginson, 1994). D Extracted by 0.5 M NaHCO (Colwell, 1963). 3 E 0.1 mol/L CaCl , 2 h extraction, 1:2.5 soil:solution ratio. 2 F Clayton and Tiller (1975), modified to 4 h extraction period. G Digestion using conc. HNO /HCl. 3
Table 2. Treatments used in split-pot soil experiments. +Cd signifies the DAP added to these pots had a high Cd concentration (see text) Treatment Experiment A Oxisol Alfisol Alfisol Experiment B 1 2 3 4 5 6 7 8 9 10
Pod zone soil
Root zone soil
Low Medium High
Low Medium High
Zero Zero+Cd Zero Zero+Cd Low Low Low+Cd High High High+Cd
Low Low High High Low Low+Cd Low High High+Cd High
Treatments consisted of control solutions (no Cd) or Cd added to solutions at a rate of 250 nM, in factorial combination to pod and root zones. GEOCHEM-PC (Parker et al., 1995) was used to determine activities of metals in the nutrient solution and ensure no precipitation of metal ions from solution occurred. All treatments were replicated fourfold. Treatment design was therefore a randomised block with two cultivars×four root zone treatments in each block. The high Cd concentration chosen represents the upper limit of Cd concentrations found in soil solutions in Australian agricultural soils (McLaughlin et
al., 1997). This high concentration was also chosen as we envisaged that uptake of Cd through pods would be small. Hence, higher Cd concentrations in solution were required to enable calculation of relative contribution of the two zones to Cd uptake by shoots and kernels. The root zone of each pot was leached with nutrient solution twice daily initially, increasing to three times daily 60 days after planting. Pod zones were kept moist using deionised water (as much of the water loss was due to evaporation and not uptake of water by the developing pods). Plants were sprayed with pyrethrum after 35 days to control whitefly, and at 114 and 120 days with Pictrin and at 127 days with RogorTM to control mites. Plants were harvested 130 days after transplanting and separated into shoots, roots, pegs (gynophores), pods and kernels. Plant shoot material and kernels were rinsed in a solution of 0.1% DeconTM , deionised water and then dried at 60 ◦ C in a forced draught oven. Roots were washed from the sand using deionised water. No attempt was made to desorb extracellular Cd bound in the apoplastic space, as we suspected there may have been differences between cultivars in the ability to bind Cd extracellularly, and possibly to affect Cd uptake. Cultivar differences in testa Cd concentrations Differences between cultivars in the concentrations of Cd retained in the testa and in the kernel were investigated by analysing Cd concentrations in these tissues for 12 cultivars of peanut. Pods obtained through a previous cultivar evaluation experiment (Bell et al.,
54 1997) were separated into kernel and testa, and Cd concentrations in each determined as outlined below.
Table 3. Pod weight and Cd and Mn concentrations in kernels of cv. Streeton in the three soils (Experiment A) Treatment
Pod weight (g pot−1 )
Kernel Cd (mg kg−1 )
Kernel Mn (mg kg−1 )
Low (Oxisol) Medium (Alfisol) High (Alfisol)
84.3 62.7 20.3
0.007 0.094 0.185
18.9 20.3 87.9
8.1
0.062
21.5
Soil and plant analyses Plant material (tops) was ground using a stainless steel grinder. Samples were totally digested in a concentrated solution of HNO3 /H2 O2 , after which the solution Cd concentration was determined by graphite furnace atomic absorption spectrophotometry (GFAAS). Analysis of standard reference materials gave Cd concentrations not significantly different from certified values (see McLaughlin et al., 1994 for details). In the case of analyses of peanut kernel, whole kernels (with testa intact) were analysed except in the instance where the relative Cd contents of testa and seed were determined. All plant Cd concentrations were expressed on a dry weight basis, while those of seeds were on an ‘as received’ basis, with moisture contents ranging from 2 to 5%. Soil pH, electrical conductivity (EC) and extractable Cl were determined in a water suspension of soil using a 1:5 soil:solution ratio (Rayment and Higginson, 1992). Chloride in the filtered solution was determined using an automated ferricyanide method (APHA, 1992). Organic C was determined using the Walkeley–Black procedure (Rayment and Higginson, 1992). EDTA-extractable Cd was determined by shaking soils for 4 h in 0.05 mol L−1 EDTA (pH 6.0) using a soil:solution ratio of 1:5 (modified Clayton and Tiller, 1979). DTPA-extractable Cd was determined by shaking soils for 2 h in 0.005 mol L−1 DTPA using a soil:solution ratio of 1:2 (Lindsay and Norvell, 1978). EDTA- and DTPA-extractable Cd represent strongly and moderately strongly surface-bound Cd, respectively. CaCl2 -extractable Cd (weakly-bound surface Cd) was determined by extracting soils for 2 h in 0.1 mol L−1 CaCl2 solution using a soil:solution ratio of 1:2.5 (modified Sauerbeck and Styperek, 1985). Concentrations of Cd in extracts were determined using flame or graphite furnace AAS using deuterium background correction. Statistical analysis Treatment effects were assessed by linear regression analyses or ANOVA using a completely randomised design.
LSD (P·0.05)
Results Split-pot soil experiments Results of Experiment A are shown in Table 3. Cadmium concentrations in peanut kernels were lowest in the Oxisol and greatest in the high-Cd Alfisol, which was in line with concentrations of Cd extracted from these soils by 0.1 M CaCl2 (Table 1). Yields of kernels were very low in the high-Cd Alfisol, and symptoms indicative of manganese (Mn) toxicity appeared on plants grown in this soil. While Mn concentrations in shoots were not determined, Mn concentrations in kernels grown on this soil were very high. In Experiment B, investigating stratification of the growing medium, significant differences were observed in pod yields and in kernel Cd concentrations, depending on both the soil type and the location of Cd in the pot (Table 4). The high Cd Alfisol again produced plants with symptoms of Mn toxicity and Mn concentrations in kernels were three- to four-fold those in other treatments. Cadmium concentrations in kernels were very low in the pots containing the Oxisol, either in the pod or root zone, and irrespective of high Cd DAP being added (Table 4). There was some indication that small amounts of Cd could be taken up by pods directly in the treatments with acid-washed sand in the pod zone, with and without high Cd DAP added. However, much larger increases in kernel Cd concentration were observed when Cd was added to the root zone, rather than the pod zone. Sand/nutrient solution experiment There were no significant effects of Cd treatments or cultivar on shoot or kernel weights. Mean values for shoot, root and kernel dry weights were 94.6, 26.9 and 19.7 g pot−1 , respectively. Cadmium concentrations in
55
Table 4. Pod weights and kernel Cd and Mn concentrations in cv. Streeton in relation to soil type and stratification treatments (Experiment B) Pod zone treatment
Root zone treatment
Pod weight (g pot−1 )
Kernel Cd (mg kg−1 )
Kernel Mn (mg kg−1 )
Zero Zero+Cd Zero Zero+Cd Low Low Low+Cd High High High+Cd
Low Low High High Low Low+Cd Low High High +Cd High
80.1 87.4 22.7 51.9 84.3 87.8 84.5 20.3 22.2 46.4
0.013 0.067 0.240 0.188 0.007 0.008 0.007 0.185 0.306 0.178
21.3 21.9 34.1 34.1 18.7 18.8 19.2 87.9 77.3 71.6
16.1
0.063
23.6
LSD (P≤0.05)
Table 5. Concentrations of Cd in plant parts from sand/nutrient solution experiment. Treatments are ++=Cd added to both pod and root zones, +−=Cd added to pod zone only, −+=Cd added to root zone only and −−=no Cd added to either zone. Means followed by the same letter are not significantly different (P≤0.05) Treatment
++
+−
−+
−−
Significant Treatments (P≤0.05)A
mg kg−1 Shoots Streeton NC7
9.98b 8.87b
0.08a 0.12a
10.07b 9.55b
0.15a 0.08a
Zone
Roots Streeton NC7
9.13b 12.96c
0.03a 0.05a
9.93b 10.64bc
0.02a 0.04a
Zone, Cultivar
Pegs Streeton NC7
4.50d 4.01cd
0.04b 0.04b
3.76c 3.82cd
0.02a 0.02a
Zone
Pods Streeton NC7
2.31d 2.86e
0.12b 0.11b
1.84c 2.59de
0.04a 0.03a
Zone, Cultivar, Zone×Cultivar
Kernels Streeton NC7
2.52cd 3.09e
0.06b 0.06b
2.33c 3.03de
0.02a 0.03a
Zone, Cultivar
A Data log transformed for analysis.
56 Table 6. Analysis of variance results for percentage of total Cd in plant found in shoots, roots and kernels in sand/nutrient solution experiment. Treatments are ++=Cd added to both pod and root zones, +−=Cd added to pod zone only, −+=Cd added to root zone only and −−=no Cd added to either zone. Means followed by the same letter are not significantly different (P≤0.05) Treatment
++
+−
−+
−−
Significant Treatments (P≤0.05)A
Shoots Streeton NC7
74.6ab 65.5a
78.2b 75.4ab
73.8ab 73.9ab
91.3c 74.9ab
Zone, Cultivar
Roots Streeton NC7
22.3cd 28.6d
7.2a 11.5ab
23.0cd 22.1cd
6.1a 18.9bc
Zone, Cultivar
Kernels Streeton NC7
3.2a 5.8a
14.6b 13.1b
3.3a 4.0a
2.5a 6.1a
Zone
A Data log transformed for analysis.
Table 7. Distribution of Cd between kernel and testa in relation to testa weight for several cultivars Cultivar
Testa wt.
Whole kernel Cd
Testa Cd
Testa Cd/total Cd
A140L31 55-437 RMP91 A166L17 B57 P5 1 B57 P4 1 New Mexico Valencia C NC7 Southern Runner Florunner Q24168 Streeton
(% of kernel) 3.39 3.03 2.79 2.90 3.10 3.10 2.32 3.40 2.47 2.25 2.61 2.60
mg/kg 0.48 0.46 0.36 0.42 0.34 0.39 0.77 0.61 0.36 0.52 0.41 0.46
mg/kg 3.50 2.98 2.41 3.62 2.74 2.92 2.83 3.87 2.27 2.13 3.17 2.56
% 24.0 18.7 18.1 25.2 24.8 23.3 9.1 21.4 16.3 9.5 19.6 14.5
Mean
2.83
0.47
2.92
17.3
plant material are shown in Table 5. At high levels of Cd supply in the root zone, cv. NC7 had significantly (P≤0.01) higher concentrations of Cd in both pods and kernels than cv. Streeton. There were no significant cultivar differences at low levels of Cd supply in the root zone. Shoot Cd concentrations were similar between the cultivars and other differences were not consistent across treatments. In relative terms, Cd concentrations in plant parts were in the order roots = shoots > pegs ≥ pods = kernels
In absolute terms, Cd concentrations in kernels in the Cd-treated pots were high, about 50 times higher than those found in field-grown plants (Bell et al., 1997). In the pots with no Cd added to the root zone, Cd concentrations in kernels were less than half those found under field conditions, normally 0.02 to 0.1 mg Cd kg−1 . In terms of total Cd uptake (µg pot−1 ), there were no significant differences (P≤0.05) between the cultivars (data not shown). As expected, Cd uptake was higher in the +Cd treatments. However, there were significant cultivar differences in terms of Cd distribution in plants. Cultivar NC7 retained a significantly
57
Figure 1. Relationship between percentage kernel weight in testa and percentage kernel Cd in testa. Fitted line is Y=24.44−3765∗0.088X , R 2 =0.77.
(P≤0.05) greater percentage of the total plant Cd in the roots than cv. Streeton, and a smaller percentage (P≤0.05) was translocated to shoots (Table 6). Cultivar differences in testa Cd concentrations Data for Cd distribution in kernels and testa are shown in Table 7. Cadmium concentrations in the testa were significantly higher than in the kernel for all cultivars. Across cultivars, Cd concentrations in the testa appear to be related to the relative weight of the testa, with thicker testa retaining more Cd (Figure 1).
Discussion Knowledge of the actual mechanisms of Cd uptake by peanut plants is an important prerequisite to designing agronomic management strategies to minimise Cd accumulation in kernels. If Cd is predominantly taken up directly through the pod, as is Ca, then management of Cd accumulation will involve modification of the chemistry of the surface layers of soil in which the pods develop (i.e. the top 10–15 cm). If, on the other hand, Cd uptake is via the main root system deeper in the profile, then agronomic management techniques to modify the profile to depth will be required. From the data presented here, it would appear that Cd uptake by both peanut cultivars studied was predominantly through the main root system and not through the pods. Cadmium uptake into kernels in both the splitpot soil experiment and in the sand/solution culture experiment were consistent in that Cd uptake was always greater where the main root system was exposed to Cd. From the data in Table 5 we estimate that only between 1–3% of the total kernel Cd is taken up directly by the pods, and the data from the split-pot soil
experiment support this conclusion. These data therefore suggest that management of Cd uptake by peanuts in the field will need to consider modification of the full rooting depth of the plant, rather than just the zone of pegging and pod development. These results agree with those of Popelka et al. (1996), who demonstrated that Cd uptake by peanut was predominantly through the root system. However, these authors suggested that 11% of the kernel Cd was sourced through the pod wall, a value somewhat higher than our estimate. Popelka et al. (1996) also found that Cd concentrations in roots were similar to shoots, at around 2.0 mg kg−1 . These values are lower than the concentrations which we measured in plant shoot and roots at the high level of Cd supply. One reason is likely to be the lower Cd concentration used in their solutions (100 nM). Cadmium concentrations in roots in our study included extracellularly-bound Cd (in the apoplast and on the root surface), because to investigate cultivar differences in uptake we deliberately did not desorb this fraction from the roots prior to analysis. In other nutrient solution experiments examining Cd uptake by plants, root Cd concentrations have generally been found to be much greater than shoot Cd concentrations (Jarvis et al., 1976; Tyler and McBride, 1982; Wong et al., 1988; Smolders and McLaughlin, 1996a, b), even when extracellular Cd has been desorbed (Smolders and McLaughlin, 1996a, b). Peanuts are evidently efficient in transporting Cd from roots to shoots compared to other species. Concentrations of Cd used in the sand/solution culture experiment were deliberately high so that measurable differences in Cd uptake from the pod zone could be determined. There are concerns from using such high Cd concentrations. One is that the level of Cd in solution is sufficiently high to cause toxicity to the plants (Page et al., 1972). However, there were no differences in shoot growth or pod weights between the minus Cd and plus Cd treatments (data not shown), suggesting Cd was not at phytotoxic levels. A second concern may be that the plant response and Cd partitioning is different at low versus high solution Cd concentrations. The data for Cd distribution in Table 6 indicate no interaction between cultivar effects and Cd (Zone) treatments. However, differential partitioning of Cd appeared to be more pronounced at low levels of Cd supply in both pod and root zones. Cultivar NC7 had higher Cd concentrations in kernels than cv. Streeton, in agreement with data from a field cultivar evaluation trial (Bell et al., 1997). Interesting differences in Cd distribution within the plant
58 were noted between the two cultivars. It would appear that cv. NC7 retained less of the accumulated Cd in the shoots and more in/on the roots, especially at low levels of Cd supply (Table 6). Differential translocation of Cd within the plant has been suggested as a principal mechanism for cultivar differences in Cd accumulation by maize (Zea mays L.) (Florijn et al., 1993). The possibility that this mechanism is linked to the ability of peanut plants to exclude Cd from the kernel requires investigation. Cadmium concentrations were significantly higher in the testa compared to the kernel, by up to one order of magnitude. Loading of nutrients into the kernel occurs through the testa, which requires an active transport mechanism (Periasamy and Sampoornam, 1984). The testa may therefore act as a barrier to Cd transport to the developing kernel. However, the data in Figure 1 imply that there are differences in efficiency of Cd retention in the testa (across cultivars) and the relationship between relative testa weight (to whole kernel weight) and relative testa Cd content was not linear. The practical significance of this result is that blanching of kernels, which removes the testa, is an effective management strategy to mininise Cd concentrations in the product, but that the efficiency will vary with cultivar. Acknowledgements Partial support from the Peanut Company of Australia and the Grains Research and Development Corporation is gratefully acknowledged. References Anon 1992 Report on the national residue survey, 1989–1990 Results. Bureau of Rural Resources, Australian Government Printing Office, Canberra. APHA – American Public Health Association 1992 Standard Methods for the Examination of Water and Wastewater, 18th edn. APHA, Washington, DC. Bell M J, McLaughlin M J, Wright G C and Cruickshank A 1997 Inter- and intra-specific variation in accumulation of cadmium by peanut, soybean and navybean. Aust J. Agric. Res. 48, 1151– 1160. Bledsoe R W, Comar C L and Harris H W 1949 Absorption of radioactive calcium by the peanut fruit. Science 109, 329–330. Chaney R L and Oliver D P 1996 Sources, potential adverse effects and remediation of agricultural soil contaminants. In Contaminants in the Soil Environment in the Australasia–Pacific Region. Eds R Naidu, R Kookana, D P Oliver, S R Rogers and M J McLaughlin. pp 456–478. Kluwer Academic Publishers, Dordrecht, The Netherlands. Clayton P M and Tiller K G 1979 A chemical method for the determination of heavy metal content of soils in environmental studies. CSIRO Aust. Div. Soils, Tech. Paper No. 41. 17 pp. Colwell J D 1963 The estimation of the phosphorus fertilizer requirements of wheat in southern New South Wales by soil analysis. Aust. J. Expt. Agric. An. Husb. 3, 100–107.
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