Environ. Sci. Technol. 2008, 42, 450–455
Differential Uptake, Partitioning and Transfer of Cd and Zn in the Soil-Pea Plant-Aphid System I A I N D . G R E E N * ,† A N D M A R K T I B B E T T ‡ The School of Conservation Sciences, Bournemouth University, Talbot Campus, Poole, Dorset, BH12 5BB, U.K., and Centre for Land Rehabilitation, School of Earth and Geographical Sciences, Faculty of Natural and Agricultural Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia
Received August 10, 2007. Revised manuscript received September 27, 2007. Accepted November 2, 2007.
The biomagnification of trace metals during transfer from contaminated soil to higher trophic levels may potentially result in the exposure of predatory arthropods to toxic concentrations of these elements. This study examined the transfer of Cd and Zn in a soil-plant-arthropod system grown in series of field plots that had received two annual applications of municipal biosolids with elevated levels of Cd and Zn. Results showed thatbiosolidsamendmentsignificantlyincreasedtheconcentration of Cd in the soil and the shoots of pea plants and the concentration of Zn in the soil, pea roots, shoots, and pods. In addition, the ratio of Cd to Zn concentration showed that Zn was preferentially transferred compared to Cd through all parts of the system. As a consequence, Zn was biomagnified by the system whereas Cd was biominimized. Cd and Zn are considered to exhibit similar behaviors in biological systems. However, the Cd/Zn ratios demonstrated that in this system, Cd is much less labile in the root-shoot-pod and shoot-aphid pathways than Zn.
Introduction The trace metals Cd and Zn possess similar chemical properties, which may result in similar behavior in biological systems (1). Both elements are among the most labile trace metals in the soil-plant system (2) and may, therefore, be readily transferred to higher trophic levels. However, they differ in an important way as Zn is an essential element for plants (3) and animals (4), while Cd has no known essential function in metazoan organisms. Moreover, work in potbased experimental systems has suggested that that there are important differences in the way the two metals are transferred from the soil to the shoots of graminoid crops (5, 6). The biomagnification of trace metals during transfer through arthropod food chains is of much concern due to the potential for this process to concentrate benign levels of contamination into toxic levels within higher trophic levels (7–9). Within agroecosystems, biomagnification may pose a risk to the successful use of biological control measures against invertebrate crop pests (10, 11). Deposition from the * Corresponding author tel: +44 (0)1202 965009; fax: +44 (0)1202 965046; e-mail:
[email protected]. † Bournemouth University. ‡ The University of Western Australia. 450
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atmosphere and the use of many agricultural materials, such as biosolids, can contaminate agricultural soils with Cd and Zn (12). Trace metals from contaminated soil may be taken up by crop plants and it has been shown that Cd and Zn can be biomagnified in aphids feeding on them (6, 8, 10). Aphid outbreaks can cause economic damage to crops, but a large range of species predate aphids and can be used as an environmentally and economically effective method of control (13). However, our knowledge of the multitrophic transfer of trace metals is not sufficient to determine the magnitude of the threat posed by biomagnification to aphid predators and hence the impact on biological control. The quantity of trace metals transferred from the soil to aphid predators is highly likely to vary within the crop rotation as it is well established that large differences in metal accumulation exist between crop species. Aphids are generally specialist herbivores and therefore different species of aphids are found on different crops. The efficiency of trace metal regulating physiology within arthropods is species specific and can vary significantly, even between closely related species (14, 15). Thus, the trace metal accumulation characteristics of the crop plant and its associated aphid species may combine to have an antagonistic or synergistic effect on the transfer of trace metal from the soil to the predator trophic level. The concentrations of trace metals extracted from soils by neutral salt solutions are widely used to predict concentrations of trace metals in plants and may also be useful in predicting concentrations in higher trophic levels (16). Consequently, this technique may be a useful tool to predict the concentration and therefore ecotoxicological effects of trace metals in higher trophic levels, including aphids and their predators. However, due to the scarcity of reports concerning the power of this technique to predict concentrations in the herbivore trophic level, the efficacy of this technique needs further elucidation. Given the paucity of knowledge of multitrophic transfer in the soil-plant-arthropod system, the aims of this present study are 3-fold: (1) to determine the uptake and partitioning of Cd and Zn in the soil-pea plant-aphid system; this has not been investigated previously in this respect; (2) to investigate the relative transfer of Cd and Zn in the system; and (3) to determine if Cd and Zn concentration in various components of the system can be more readily predicted from the concentration extracted from the soil by a neutral salt extraction (0.1 M Ca Cl2) than total metal concentration in the soil.
Materials and Methods A field trial was established on a freely draining sandy loam soil of the Fyfied series (a typic plaggenthrept). Thirty six experimental plots of 9 m2 were established and randomly assigned one of six biosolid treatment rates equivalent to 0, 5, 7.5, 10, 15, or 20 t (dry solids) ha-1. Each treatment rate was applied to six plots. Treatments, in the form of a dewatered biosolids “cake”, were incorporated into the plow layer of the soil with a rotavator. Plots were amended again the following year using identical amendment rates and biosolids from the same municipal source as used in the first amendment. The cumulative application rates were therefore 0, 10, 15, 20, 30, and 40 t ha-1. Total metal concentrations in the biosolids used for the first amendment were 11.3 and 610 mg kg-1 for Cd and Zn, respectively, while the cognate values for the second amendment were 2.4 and 724.6 mg kg-1for Cd and Zn, respectively. 10.1021/es071992c CCC: $40.75
2008 American Chemical Society
Published on Web 12/12/2007
TABLE 1. Mean (± 1SE) Total and Available (0.1 M CaCl2 Extractable) Concentrations of Cd and Zn (mg kg-1), pH, and % Loss on Ignition (LOI) after the Amendment of Soil with Biosolids (Significance Determined by ANOVA) total concn.
extractable concn.
amendment
Cd
Zn
Cd
Zn
pH
LOI
ha-1
0.14 ( 0.01 0.15 ( 0.01 0.16 ( 0.01 0.17 ( 0.01 0.17 ( 0.01 0.19 ( 0.01
30.9 ( 0.59 32.5 ( 0.94 32.5 ( 1.48 33.8 ( 0.91 35.3 ( 0.44 35.9 ( 1.18
0.08 ( 0.00 0.08 ( 0.00 0.08 ( 0.00 0.09 ( 0.01 0.10 ( 0.01 0.09 ( 0.01
2.14 ( 0.14 2.34 ( 0.14 2.70 ( 0.18 3.04 ( 0.21 3.43 ( 0.11 3.81 ( 0.13
4.60 ( 0.07 4.59 ( 0.06 4.59 ( 0.06 4.54 ( 0.04 4.49 ( 0.02 4.50 ( 0.04
5.9 ( 0.34 6.2 ( 0.25 6.8 ( 0.17 6.5 ( 0.22 6.7 ( 0.22 6.7 ( 0.21
significance
F(5,30) ) 5.7 P ) 0.004
F(5,30) ) 3.4 P ) 0.01
F(5,30) ) 3.4 P ) 0.015
F(5,30) ) 17 P < 0.001
F(5,30) ) 1.1 P ) 0.39
F(5,30) ) 2.1 P ) 0.09
0t 10 t 15 t 20 t 30 t 40 t
ha-1 ha-1 ha-1 ha-1 ha-1
For the first four years of cultivation, winter wheat was grown on the plots. In the fifth year, field peas (Pisum sativum L. cv. Elan) were grown as a break crop. A seeding rate calculated to result in a density of 70 plants m-2 was used and the crop was fertilized with an N, P, K fertilizer applied at a rate of 90 kg ha-1. Pea aphids (Acyrthosiphon pisum Harr.) were allowed to infest pea plants naturally. Plots were sampled 72 d after seeding. Five soil samples were taken from the top 15 cm of each plot and bulked into one composite sample for each plot. Six pea plants were selected at random in each plot and were dug out by hand, ensuring the roots were sampled to the third order lateral. Aphid samples were collected by hand brushing them into plastic tubes. Chemical Analysis. Analysis of the soil sampled from the plots was conducted in triplicate on a fine earth fraction prepared from the bulk samples. Soil pH was determined in a 2.5:1 water/soil suspension and organic matter content of the soil was estimated by loss on ignition. Total Cd and Zn concentrations in soil were determined by refluxing a 0.5 g subsample in concentrated nitric acid (10). Extractable metal concentrations were determined by shaking 10 g of soil with 50 mL of 0.1 M CaCl2 for 16 h (17). Washed roots, shoots, and pods of plants were dried to constant weight at 70 °C. Subsamples of finely ground root and shoot material (0.25 g) were digested in triplicate in 10 mL of concentrated nitric acid (10). Root samples were cut into 0.5 cm strips and duplicate subsamples of ca. 0.1 g were digested as per other plant samples. Aphid samples were washed and dried as described for the plant material, before subsamples of ca. 40 mg were digested in 2 mL of nitric acid in sealed glass vessels at a temperature of 80 °C. The clear residue was then diluted to volume (5 mL) using deionized–distilled water. Concentrations of Cd and Zn in samples were determined with flame (Zn) and electro-thermal (Cd) atomic absorption spectrometry (ATI Unicam Solaar 939). Analytical quality was ensured by the digestion of relevant certified reference materials (BCR 143R or BCR 281) and reagent blanks in each batch of samples were digested and analyzed. Data Analysis. Statistical analysis was conducted with SPSS (Version 11). Transfer coefficients were calculated by dividing the concentration in one component of the system by the concentration in the component below it, e.g. concentration in the shoot divided by the concentration in the root. Due to the non-normal distribution of derived variables, the differences among treatments in transfer coefficients or Cd/Zn ratios were determined nonparametrically by the Kruskal–Wallis (K-W) test (18). All other data sets were analyzed for homogeneity of variance and for normality with Levene’s test and the Shapiro-Wilk test, respectively. Subsequently, differences among treatments were tested for statistical significance by one-way analysis of variance (ANOVA). Additional checks for linearity and
homoscedasticity were conducted on data sets prior to regression analysis. When assumptions were not met, data were inversely transformed in order to meet them.
Results Metal Accumulation and Transfer Coefficients. The amendment of the soil with biosolids significantly elevated the total concentrations of both metals in the soil (Table 1). The concentration of 0.1 M CaCl2 extractable Cd in the soil showed a small, but statistically significant increase due to biosolids amendment (Table 1). The extractable Zn concentrations in the soil also differed significantly among the treatments and were elevated compared to the control in all the biosolids amended plots. The pH of the amended soils was generally lower than that of the control, while loss on ignition values were higher. However, neither parameter was found to be significantly affected by biosolids amendment (Table 1). Cadmium concentrations within the plant decreased in the order roots > shoots> pods in all treatments (Figures 1 and 2). The concentration of Cd showed no evident relationship with biosolids amendment in the roots or pods of pea plants and ANOVA showed there were no significant differences among treatments for either plant part (F(5,30) ) 0.44, P ) 0.82 and F(5,30) ) 2.1, P ) 0.10 for roots and shoots, respectively). However, biosolids amendment had a significant effect on the Cd concentration in shoots, which showed a pattern of increase with the size of the amendment (F(5,30) ) 5.7, P ) 0.001). Transfer coefficients showed that Cd concentrations in the roots were 3.6–4.6 times higher than the total concentration in the soil and 7-9 times higher than in the extractable fraction of the soil (Table 2). By contrast, transfer coefficients between the root and shoot were all below 0.4, demonstrating a substantial deconcentration of Cd. Transfer coefficients showed that a further deconcentration, of a similar magnitude, also occurred in the transfer of Cd from the shoots to the pods. The Kruskal–Wallis test showed that only the transfer coefficients for the transfer of Cd from the roots to the shoots were significantly affected by biosolids amendment (Table 2). The concentration of Cd in pea aphids showed no clear pattern as the size of the biosolids amendment changed (Figure 2), and differences among treatments were not significant (data inversely transformed, F(5,30) ) 2.0, P ) 0.11). Furthermore, transfer coefficients between the aphids and the shoots on which they fed demonstrated considerable biominimization of Cd, especially in the three highest biosolids amendments. This change in transfer coefficients as biosolids amendment increased was significant (Table 2). Zinc concentrations within the different parts of the pea plants decreased in the order roots > shoots> pods in the control and the lowest three biosolids amendments. However, this order changed to shoots > roots > pods in the plants subject to the two highest biosolids amendment (Figure 2). Each increase in VOL. 42, NO. 2, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 1. Mean concentration of Cd in roots, shoots, and pods of pea plants and the pea aphids feeding on them after the amendment of soil with biosolids (error bars ( 1SE).
FIGURE 2. Mean concentration of Zn in roots, shoots, and pods of pea plants and the pea aphids feeding on them after the amendment of soil with biosolids (error bars ( 1SE).
TABLE 2. Transfer Coefficients for the Transfer of Cd and Zn between Components of the Soil-Pea Plant-Pea Aphid System Following the Application of Biosolids (Significance Determined by K-W Test) total soil to root
extractable soil to root
root to shoot
shoot to pod
shoot to aphids
amendment
Cd
Zn
Cd
Zn
Cd
Zn
Cd
Zn
Cd
Zn
ha-1
4.49 3.98 4.48 4.54 4.14 3.65
2.45 2.43 2.68 2.56 2.55 2.57
8.04 7.50 9.34 8.39 7.23 7.37
35.41 33.94 32.54 28.91 26.53 24.34
0.22 0.38 0.22 0.32 0.29 0.41
0.75 0.87 0.80 0.93 1.04 1.16
0.39 0.35 0.30 0.30 0.25 0.32
0.95 0.81 0.82 0.72 0.80 0.74
0.50 0.41 0.43 0.16 0.17 0.15
2.10 1.81 1.97 1.84 1.78 1.33
1.9 0.86
2.1 0.83
2.7 0.75
15 0.01
7.9 0.02
17 0.01
10 0.07
11 0.06
19 0.002
11.5 0.04
0t 10 t 15 t 20 t 30 t 40 t
ha-1 ha-1 ha-1 ha-1 ha-1
H(5) ) P)
the biosolids amendment rate resulted in an increase in the mean concentration of Zn in the pea roots, but ANOVA showed that this was not statistically significant overall (F(5,30) ) 1.4, P ) 0.25). However, Zn concentration increased significantly with 452
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the biosolids amendment in pea shoots (F(5,30) ) 13.9, P < 0.001) and pods (F(5,30) ) 21.6, P < 0.001). Transfer coefficients between the total Zn concentration in the soil and the roots were remarkably consistent, ranging
TABLE 3. Cd/Zn Concentration Ratios (×10-3) Found in the Components of the Soil-Pea Plant-Pea Aphid System Following the Application of Biosolids (Significance Determined by K-W Test) amendment ha-1
soil (total)
soil (extrct.)
root
shoot
pod
aphid
0t 10 t ha-1 15 t ha-1 20 t ha-1 30 t ha-1 40 t ha-1
4.53 4.45 4.92 4.92 4.88 5.36
37.20 32.68 28.59 29.44 29.14 24.02
8.20 7.17 8.29 8.36 7.87 7.66
2.34 2.00 2.19 2.48 2.17 1.96
0.94 0.85 0.81 1.02 0.69 0.83
0.92 0.31 0.22 0.42 0.20 0.21
significance
H(5) ) 8.21 P ) 0.15
H(5) ) 13.1 P ) 0.022
H(5) ) 0.76 P ) 0.98
H(5) ) 5.67 P ) 0.34
H(5) ) 7.95 P ) 0.16
H(5) ) 11.2 P ) 0.047
TABLE 4. Regression Relationships between the Total or Extractable Concentration of Cd and Zn (mg kg-1) in Soil (S) and the Concentration (mg kg-1) in Pea Plant Roots (Pr), Shoots (Ps), Pods (Pp), and Aphids (A) total concn. in soil regression model
extractable concn. in soil r2
regression model Cadmium
Pr ) 0.40 + 1.68S Ps ) 0.014 + 0.96S Pp ) 0.02 + 0.19S A ) 0.13 + –0.54S
0.03 0.25** 0.14* 0.25**
Pr ) 51.02 + 1.0S PS ) -10.18 + 4.43S 1/Pp ) 0.034 + -0.001S A ) 97.73 + 0.97S
0.05 0.40*** 0.34*** 0.014
Zinc
between 2.4 and 2.7, and the Kruskal–Wallis test showed there was no significant variation with biosolids amendment (Table 2). Coefficients between extractable Zn concentration in the soil and in the roots were by far the highest coefficients found in the system, but showed a significant decline as biosolids amendment increased. Transfer coefficients between the roots and shoots followed the opposite pattern, rising significantly with biosolids treatment. Transfer coefficients between pea shoots and pods were all below 1, but no clear pattern was evident in the way these transfer coefficients changed with biosolids amendment and differences among treatments were not significant. Zinc concentrations in aphid populations from the biosolids amended plots were higher than the control (Figure 2). However, differences among treatments were not significant (F(5,30) ) 1.3, P ) 0.31). Transfer coefficients showed that Zn was biomagnified in aphids by a factor between 1.8 and 2.0 up to 30 t ha-1 (Table 2), but the low concentration of Zn in the aphid populations at the highest amendment rate was reflected in a low transfer coefficient for this treatment. Overall differences among treatments were statistically significant (Table 2). Cadmium/Zinc Ratios. Cadmium/zinc ratios decreased through the soil-plant-aphid system, starting from the extractable concentration in the soil (Table 3). This was consistent across all treatments. Ratios changed significantly with the size of biosolids amendment only for the extractable concentration in the soil and in aphid populations. In both cases, the ratio decreased as biosolids amendment increased. Predicting the Fate of Cd and Zn from the Extractable Soil Concentrations. Linear regression of the total and extractable concentration in the soil against the concentration in pea roots, shoots, and pods gave positive slopes for Cd, while a negative slope was found in the case of Cd in pea aphids (Table 4). Regression slopes significantly different from zero were found between the total Cd concentration in the soil and the concentration in the shoots and pods of pea plants and in the aphid populations. For the extractable
r2
Pr ) 0.07 + 7.14S PS ) 0.06 + 1.30S Pp ) 0.03 + 0.30S A ) 0.09 + -0.50S
0.21** 0.19** 0.14* 0.09
Pr ) 61.88 + 7.83S PS ) 15.49 + 21.53S Pp ) 26.21 + 12.02S A ) 118.28 + 4.11S
0.16* 0.54*** 0.59*** 0.015
concentration in the soil, regression slopes were significant in the case of roots, shoots, and pods of pea plants. Both the total and extractable concentrations of Zn in the soil showed positive relationships with the Zn concentrations in the roots, shoots, and pods of pea plants and in the aphid populations (Table 4). Regression slopes significantly different from zero were found between the total and extractable concentrations of Zn in the soil and the concentrations in pea shoots and pods. The extractable Zn concentration in the soil also showed an additional significant slope with the concentration in pea roots. Regression relationships were much stronger for Zn than for Cd and the discrimination between total (nitric acid digestible) and extractable (0.1 M CaCl2) metal concentration in the soil was much greater for Zn than for Cd.
Discussion Soil to Root Transfer. The concentration of Zn in both the biosolids was greater than the 50-percentile value of biosolids used in UK agriculture (19). The concentration of Cd in the biosolids was proportionally much higher, over three times the 90-percentile value of biosolids used in UK agriculture in the case of the first amendment (19). The lowest amendment rate of biosolids applied to the plots was equivalent to the typical application in the UK, while the highest rate was equivalent to 4 times this rate (19). Amendment at these rates resulted in a significant increase in the total and extractable concentration of Cd and Zn in the soil. However, total concentrations of both metals were well within the current limits for Cd and Zn in biosolids amended soils set in the EU and the United States (20, 21). Growing in the amended soils did not significantly affect the concentration of Cd or Zn in the pea roots. However, transfer coefficients demonstrated that the roots took up proportionally more Zn than Cd from the extractable fraction in the soil. There is evidence that ZRT1/IRT1-like proteins play a role in the trans-membrane uptake of Zn2+ by root cells and may function in the uptake of Cd2+, but at a lower VOL. 42, NO. 2, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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affinity (22, 23). Moreover, there is also indirect evidence that Cd2+ may enter plant cells via Ca2+ uptake channels, again at low affinity (22). Thus, the greater uptake of Zn can be explained by the higher affinity of uptake mechanisms for this metal. Nevertheless, Cd was still strongly accumulated in pea roots, a finding that agrees with other work (24). Root to Shoot Transfer. In the present study, both Cd and Zn concentrations in the pea roots showed no increase with increasing soil concentration, but shoot concentration was increased. This suggests that the pea plants took up more Cd and Zn as the concentration in the soil increased and that a large proportion of the additional metal taken up was translocated to the shoot. This was particularly evident in the case of Zn, where transfer coefficients between the extractable concentration in the soil and in the roots fell with increasing concentration in the soil, while the transfer coefficients between the root and shoot increased. Such a finding is consistent with the homeostatic regulation of Cd and Zn concentrations in the pea roots, which may possibly have been mediated through the physiological action of transmembrane proteins transporters responsible for the loading of the two metals into the xylem sap (25–27). The decrease in Cd/Zn ratio in the shoots compared to the roots indicated that Zn was translocated to the shoot to a much greater extent than Cd. Strong retention of Cd in the root and relatively free translocation of Zn from the root to the shoot has also been reported in other members of the Fabaceae (28, 29). This would suggest that the physiological mechanisms for sequestering Cd and Zn in the roots, such as binding to phytochelatins, were more efficient in the case of Cd than Zn (30, 31), depressing the supply of Cd2+ relative to Zn2+ to the mechanisms loading these cations into the xylem sap. Shoot to Pod Transfer. Cd and Zn are transported to developing seeds primarily via phloem-mediated retranslocation from the shoots (32, 33). However, in the present study elevated concentrations of Cd in the shoots were not transferred to the developing pods. Such exclusion of Cd from seed generating organs has been reported for other plant species (32–35). The very low transfer coefficients between shoots and pods found in the present study demonstrated the effectiveness of this exclusion mechanism and suggests that the quality of the final crop would not be affected by the equivalent of several years of biosolids application that was used in the present study. In contrast to Cd, Zn concentrations in the developing pods were significantly elevated by biosolids amendment of the soil. In addition, Cd/Zn ratios showed a marked fall in the pods when compared to the shoots. Both facts suggest that Zn was retranslocated from the shoot to the developing seeds to a much greater extent than Cd and is hence the more phloem mobile trace metal. This is consistent with reported results for other plant species (33, 36). The exclusion of Cd from seed generating organs appears to result from the constraint of Cd loading into the phloem stream (33, 36). Experimental evidence suggests that the protein transporters that drive the loading of Cd and Zn into the phloem do not differ in their affinity for the two metals (25, 27). Consequently, the mechanism excluding the loading of Cd into the phloem sap is likely to occur before transport over the plasma membrane, which suggests regulation of Cd2+ levels in the cytosol via cellular sequestration is the principle cause. Shoot to Aphid Transfer. The low mobility of Cd in phloem sap compared to Zn was reflected in the relatively high accumulation of Zn compared to Cd in the aphids. A similar result for the transfer of Cd and Zn from wheat plants to the cereal aphid Rhopalosiphum padi has also been reported (37). The concentrations of both metals in the aphids were not affected by biosolids amendment, despite the 454
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significant increase in shoot concentration. Invertebrates are thought to exert little control over the uptake of trace metals from their food and metal uptake is believed to be proportional to the concentration of the metal in an available form in the ingested food (38). In the case of aphids, the concentration of Cd and Zn in the shoots on which they have fed has been reported to be significantly related to the concentration in aphids themselves (6, 8, 37). This was not the case in the present study, which may indicate that physiological mechanisms have maintained homeostatic control over the metal concentration in the phloem sap in the case of Cd or within the aphid in the case of Zn. Concentrations of Cd and Zn in pea shoots were higher than those found in wheat shoots grown earlier in the crop rotation in the same plots, but the concentrations of both metals were lower in the pea aphids than in the grain aphids (Sitobion avenae) feeding on the wheat crop (10). In the Psyllidae (jumping plant lice), the concentration of trace metals has been reported to vary significantly among different species, even among those feeding on the same plant species (15). Psyllidae are phloem-feeding insects in the same suborder as aphids (the Sternorrhyncha). The difference in Cd and Zn concentration between pea and grain aphids could, therefore, be related to interspecific differences in trace metal regulation, but could equally be attributable to lower concentrations of Cd and Zn in the phloem sap of peas. In either case, the results of the present study demonstrated that considerable differences in Cd and Zn transfer from the soil to predatory arthropods can occur during the different phases of the crop rotation and this cannot be predicted from the concentration in the crop alone. Predicting Cd and Zn Accumulation from Extractable Soil Concentrations. There was no clear advantage to be gained from using the extractable over the total concentration of Cd in the soil to predict concentrations in the parts of pea plant or in the aphid populations feeding on them. Moreover, the predictive power of the regression models was low in all instances, which suggests that physiological mechanisms in the plant are more important in determining the concentration of Cd in the plant and hence herbivores than soil concentration. The extractable concentration of Zn in the soil had a clearly superior power to predict the concentration of Zn in the parts of pea plants, which agrees with other studies (17, 39). Nevertheless, only the variation in shoot and pod Zn concentration could be explained to any great extent by the extractable concentration in the soil. The lack of a significant relationship between the extractable concentration and the concentration in aphids found in the present study renders this technique unable to predict concentrations in trophic levels above the plant in this soil-plant-arthropod system.
Acknowledgments We acknowledge the contributions made by Dr. Linton Winder and Dr. Graham Merrington to the design and original setup of the plots and for the help provided by the numerous staff and students of the School of Conservation Sciences who contributed their time to help manage and sample the plots.
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