You are on page 1of 5

Environmental Pollution 158 (2010) 2659e2663

Contents lists available at ScienceDirect

Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

Heavy metal concentrations in plants and different harvestable parts: A soileplant equilibrium model
Sebastin D. Guala a, Flora A. Vega b, Emma F. Covelo b, *
a b

Instituto de Ciencias, Universidad Nacional de General Sarmiento, Gutirrez 1150, Los Polvorines, Buenos Aires, Argentina Departamento de Bioloxa Vexetal e Ciencia do Solo, Facultade de Bioloxia, Universidade de Vigo, Lagoas, Marcosende, 36310 Vigo, Pontevedra, Spain

The model proposed in this study makes possible to characterize the nonlinear behavior of the soileplant interaction with metal pollution.

a r t i c l e i n f o
Article history: Received 8 February 2010 Received in revised form 27 April 2010 Accepted 28 April 2010 Keywords: Soil pollution Metal uptake Interaction model Plant mortality

a b s t r a c t
A mathematical interaction model, validated by experimental results, was developed to modeling the metal uptake by plants and induced growth decrease, by knowing metal in soils. The model relates the dynamics of the uptake of metals from soil to plants. Also, two types of relationships are tested: total and available metal content. The model successfully tted the experimental data and made it possible to predict the threshold values of total mortality with a satisfactory approach. Data are taken from soils treated with Cd and Ni for ryegrass (Lolium perenne, L.) and oats (Avena sativa L.), respectively. Concentrations are measured in the aboveground biomass of plants. In the latter case, the concentration of metals in different parts of the plants (tillering, shooting and earing) is also modeled. At low concentrations, the effects of metals are moderate, and the dynamics appear to be linear. However, increasing concentrations show nonlinear behaviors. 2010 Elsevier Ltd. All rights reserved.

1. Introduction Increased attention has been focused on metals due to their harmful negative effect on the environment. In trace amounts, they are mostly necessary elements in living organisms; however, in higher concentrations they are toxic. Soil pollution by metals can be caused by fertilizers and pesticides. The use of industrial efuent and sewage sludge on agricultural soil has become a common practice in developing countries, as a result of which these toxic metals can be transferred and concentrated into plant tissues from the soil (Alloway, 1995). Industrial wastes are a major source of soil pollution from mining industries, chemical industries, metal processing industries, metallurgic operations, oil products and products of fossil fuel combustion (Van Assche and Clijsters, 1990; Kabata-Pendias, 2001). The mobility and bioavailability of these elements depend on soil characteristics such as pH, organic matter, cation-exchange capacity, and soil redox potential (Adriano, 1986). Soil management can also change its physical, chemical, and biological characteristics; therefore, a different response of biological activity to metals toxicity may be observed. The activities of microorganisms that

* Corresponding author. E-mail address: emmaf@uvigo.es (E.F. Covelo). 0269-7491/$ e see front matter 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2010.04.026

promote plant growth can be also altered as a result of high metal concentrations (Wani et al., 2007). At high concentrations, some metals have strong toxic effects and are regarded as environmental pollutants (Nedelkoska and Doran, 2000; Chehregani et al., 2005). Heavy metals are potentially toxic for plants. Phytotoxicity results in chlorosis, weak plant growth and yield depression, and may even be accompanied by reduced nutrient uptake, and disorders in plant metabolism (Dan et al., 2008). In soils polluted by metals, plant growth can be inhibited by metal absorption. However, some plant species are able to accumulate fairly large amounts of metals without showing stress, which represents a potential risk for animals and humans (Oliver, 1997). Metal uptake by crops growing in contaminated soil is a potential hazard to human health due to transmission in the food chain (Brun et al., 2001; Gincchio et al., 2002; Friesl et al., 2006). There is also concern with regard to metal transmission through natural ecosystems (MacFarlane and Burchett, 2002; Walker et al., 2003). Parameters connected with metal uptake have been used as sensitive indicators of metal toxicity (Wilke, 1991; Nannipieri et al., 1997). The toxicity of metals in soil varies signicantly according to the characteristics of the soil and the time elapsed after contamination by metals (Doelman and Haanstra, 1984; Speir et al., 1995). Data from studies on the toxic effect of metals on soils have been used to establish the concentrations at which metals affect soil biological processes for regulatory purposes (Giller et al., 1998).

2660

S.D. Guala et al. / Environmental Pollution 158 (2010) 2659e2663 Table 1 Ni concentration in the dry matter (mg kg1) of several parts of oats (Avena sativa L.) (Poulik, 1997). Ni total content (mg kg1) 0 14 28 56 84 168 Ni in tillering 0 11.81 20.26 27.26 35.73 e Ni in shooting 0 12.76 17.47 27.96 31.47 e Ni in earing 0.75 9.88 15.81 25.60 28.81 e

Although a large number of experimental studies have been carried out to analyze the negative effects of the accumulation of metals in plants, little has been done to model mathematical formulas that are capable of generally relating the concentration of metals in the liquid phase of a soil and the concentration of metals present in plants. In this study, we model the relationship between the concentration of metals in soil and plants and in parts of plants (tillering, shooting and earing) with different concentration levels. Finally, we validate this relationship using recently published experimental results. 2. Modeling It is widely accepted that the effects of metals on forest or agrosystem soils are complex, due to the fact that soil chemistry and its liquid phase involve a large number of reactions (Lindsay, 1979; Ulrich et al., 1980; Ulrich and Pankrath, 1983). We focus on the toxic effects of ions of metals, many of which become bioavailable in natural pH levels. De Leo et al. (1993) modeled the interaction between soil acidity and forest dynamics when aluminum is mobilized with acid deposition. Guala et al. (2009) simplied this model, in order to allow it to be validated experimentally. In this study we consider the model applicable to other metals in soil, modifying it in order to make it independent of acid deposition, assuming the mobility of other metals in natural pH levels in soil. The dominant reaction may be represented as:

0 0 0 0

BhB mS; aA hBS; fH bA aAB=p; fH=m n bH W =p

(2)

As signicant amounts of metals may be available under natural acidity conditions in the liquid phase of soil and absorbed by plants instead of being xed by the soil matrix, we may neglect the two last expressions of Equation (2) by focusing on the concentration of available metals A in the second equation of Equation (2). As a result, the system in equilibrium is expressed as:

0 BhB mS; 0 aA hBS:

(3)

MOHn nH /Mn nH2 O


In order to model the dynamic interaction, we have adapted the general mathematical expression of the model that describes the dynamics of soil acidity with respect to aluminum mobility and the characteristics of trees, according to the model proposed by De Leo et al. (1993), and modied by Guala et al. (2009). As a result, the new system gives us:
dB dt dS dt dA dt dH dt

BhB mS; aA hBS; fH bA aAB=p; fH=m n bH W =p (1)

where B is the biomass of trees (kg m2), n is the oxidative number of the metal, S is the metal concentration in trees (mg kg1), and A and H are the available concentrations of metal Mn (mg L1) and proton H (mg L1) in the soil solution, respectively. t is time, W is the proton ux to the soil during rainfall (mgm2 yr1), p is the available water for roots (mm) and a, b and 4 are the coefcients of absorption (Lkg1 yr1), leaching (yr1) and reaction (yr1), respectively. m is the atomic weight of the metal M. h(B) is the function of biomass net-growth and m(S) is the function of mortality or metabolic inefciency of trees due to the concentration of Mn they contain. While De Leo et al. (1993) used B to refer to the biomass of trees, Guala et al. (2009) showed that B may also indicate some other physiological characteristics, and that Equation (1) may also be applied to plants in general. Although Equation (1) was originally proposed to specically model the soileplant interaction under the condition of aluminum mobility by acidity, we can reformulate the conditions of the last two equations for any deposited metal Mn. In this case, we are not focusing directly on the mobility of aluminum due to the concentration of protons H as a result of acid deposition W, but on the availability of any deposited metal Mn plus soil acidity conditions. As a result, under equilibrium conditions, the reformulated Equation (1) could be rewritten as:

Using Equation (3), it is possible to calculate the relationship between the concentration of available metals in soil A and the concentration of metals in plants S. The expression yields: aA mSS The net-growth function was assumed by De Leo et al. (1993) to be of the form h(B) a/(1 bB), where coefcients a, b > 0 are constant; and the logistic form to be h(B) r(1B/k) as proposed by Guala et al. (2009). Although it does not appear explicitly after Equation (3), in Equation (1) the denition of h(B) mutually determines the functional form of m(S). Therefore, the functional form of growth h(B) should be considered. It is difcult to specify how metals in soils determine the metabolic inefciency. Despite the fact that the quantitative relationship between the concentration of metals in soils and biomass production has already been documented for some years, metals do not seem to cause a significant risk far below a certain survival threshold, although the effects on different organs of the plant are detected. In particular, the functional form of the metabolic inefciency and eventual mortality m(S) is assumed by De Leo et al. (1993) as:

mS

c fS eS

where in c; f ; e > 0; S 0; e, S e is the critical survival value. It does not mean that plants can resist until S e; this would be only possible if m(S) was 0 until S e, which would mean that plants are completely insensitive to any concentration below e. Obviously, it is crucial to choose the values of the parameters correctly.

Table 2 Cd concentration in the dry matter (mg kg1) of ryegrass (Lolium perenne, L.) in cultivated and uncultivated soil after 60 days (Moreno et al., 2006). Cd total content (mg kg1) 0 50 600 1000 2000 5000 Cd in uncultivated soil 0.1 25.3 201 329 778 1209 Cd in plant 5.8 63.0 87.4 130 228 e Cd in cultivated soil 0.1 24.3 125 242 468 1030 Cd in plant 25.6 53.8 174 198 386 721

S.D. Guala et al. / Environmental Pollution 158 (2010) 2659e2663 Table 3 Value of the 3 aggregate coefcients corresponding to the simplied polynomial formula (C1S2eC2S)/(SeC3) for the Ni experiment (Poulik, 1997). Coefcients C1 C2 C3 R2 Ni in tillering 2.61 1011 72.9 66.31 0.9896 Ni in shooting 0.9094 44.74 37.52 0.9960 Ni in earing 1.302 49.2 32.82 0.9978

2661

where E1, E2, E3 > 0. As a result, we can validate the model tting results that are shown either in terms of the available metal A or in terms of the total metal content T. For the sake of simplicity and due to the mathematical equivalence of Equation (5) and Equation (6), we will only use the coefcient C1, C2, C3 to refer to the tted results for both A and T.

According to the denition of m(S) given above, the concentration of available metal in soil A as a function of the concentration of metals in plants S is explicitly written as:

3. Results In order to validate the model, we used two studies that measured the dynamic interaction between metal levels in soil and the production of biomass and other physiological characteristics of plants (Poulik, 1997; Moreno et al., 2006). Table 1 and Table 2 show the results published by Poulik (1997) and Moreno et al. (2006), respectively. The corresponding coefcients of Equation (5) are shown in Table 3 and Table 4. Poulik (1997) suggests a linear relationship for dose-S. However, although the behavior can be linearly approached far below the threshold parameter e (equivalently, coefcients C3 of Table 3 and Table 4), linearity vanishes in the tted function for all of the experimental results when metal levels increase. Equation (5) and Equation (6) suggest a more complex interaction as the concentration of metals in plants S moves closer to e, the linear tting becomes ineffective, and nonlinear terms become relevant. These terms are important in order to reliably predict the parameter e. Please note we do not assume that plants survive up to S e. As mentioned, the threshold is not the death point of the plants. Metabolic problems and eventual mortality actually appear before this point. That is a referential value and indicates the limit after which no plant of the given species under given conditions is statistically expected to be found (De Leo et al., 1993; Guala et al., 2009). Some results in Tables 3 and 4 seem to indicate that the relevance of coefcient C1 is numerically negligible and should not be taken into account. This additional result would suggest that further revisions should be made to the model, when metal dose is considered, from the perspective of the economy of parameters. In this case, Guala et al. (2009) and De Leo et al. (1993) proposed different expressions for m(S) which vary slightly in mathematical terms, but reect a conceptually different approach towards the growth of plants h(B). Although h(B) does not explicitly appear after Equation (3), expressions of h(B) and m(S) are mutually dependent from the denition of Equation (1). Therefore, further denitions of h(B) and m(S) should be considered. Similar results appear to be provided by the comparative values of the threshold e estimated from metals in soil and metal dose for the same plant species, shown in Table 4. This would conrm the assumptions in the model, which encourages us to carry out more exhaustive analyses. Fig. 1 shows the results of the experimental tting according to the proposed model. As can be seen, the gure shows the threshold concentrations of metals e in plants and in parts of plants, which species the effects for different plant organs. These thresholds are represented by the coefcients C3 of Equation (5) and Equation (6). Table 1 shows that under experimental conditions (Poulik, 1997), the last registered concentrations of Ni (in mg kg1) in tillering,

    1 c f S c=a f =aS S S a e S e S

(4)

Signs of Equation (4) were inverted for simplifying the tting propose, but mathematically is perfectly equivalent. As we can see, the process of determining coefcients is difcult, and the known empirical methods yield widely varying results (De Leo et al., 1993; Guala et al., 2009). Therefore, the model needs to be written in a way whereby the relationship A-S may be inferred from tting Equation (4). However, the coefcients c/a, f/a and e can be tted by experimental results in order to establish the relationship between A and S. It should be noted that the relationship AeS is independent of the growth function h(B), which makes it possible to generalize the model to a wide range of plants. We can now test the model in order to verify whether Equation (4) provides us with reliable results when we introduce realistic values, in this case testing the model when referring particularly to different parts of plants. This is possible by writing Equation (4) in a general mathematical form, where the constant terms are put together in aggregate coefcients to be tted, giving us:

C2 S C1 S2 C3 S

(5)

where C1,C2,C3> 0. However, many studies do not compare the metal uptake to the available metal concentration in soil A, but instead to the total metal content of soil T (Poulik, 1997; Athar and Ahmad, 2002; Moreno et al., 2006; Ryser and Sauder, 2006). In this case, we can dene T as a proportional sum of the places where the metal is located: the metal uptake S, the available metal content in soil A and the metal adsorbed in the soil matrix (assuming a Freundlich linear relationship for the purpose of simplicity). In equilibrium this is T k1S A k2A, where k1, k2 are the corresponding proportional coefcients for uptake and Freundlich adsorption, respectively. A simple algebraic calculation shows that T can be written in terms of Equation (5):

T k1 S

C2 S C1 S2 C S C 1 S2 k2 2 C3 S C3 S

C3 k1 C2 1 k2 S k1 C1 1 k2 S2 C3 S E2 S E1 S2 E3 S

Now, as with Equation (5), we can aggregate terms to redene T:

(6)

Table 4 Value of the 5 aggregate coefcients corresponding to the simplied polynomial formulas (C1S2eC2S)/(SeC3) for Cd experiments (Moreno et al., 2006). Coefcients C1 C2 C3 R2 Cd in uncultivated soil 3.259 1013 675.9 425.1 0.9742 Cd in cultivated soil 2.859 1013 2074 2169 0.9920 Cd in uncultivated soil (total content) 3.388 1014 2672 529.7 0.9555 Cd in cultivated soil (total content) 6.718 107 6302 1629 0.9956

2662

S.D. Guala et al. / Environmental Pollution 158 (2010) 2659e2663

1000 900

1400 1200 1000 800 600 400 200

Cd in uncultivated soil (mg/kg)

800 700 600 500 400 300 200 100 0 0 50 100 150 200

a
250

Cd in cultivated soil (mg/kg)

0 0 100 200 300 400 500 600 700

b
800

Cd in plant (mg/kg)
2500 7000

Cd in plant (mg/kg)

Cd total content in uncultiv. soil (mg/kg)

Cd total content in cultiv. soil (mg/kg)

6000 5000 4000 3000 2000 1000

2000

1500

1000

500

0 0 50 100 150 200

c
250

d
0 0 100 200 300 400 500 600 700 800

Cd in plant (mg/kg)
120 180 160 100

Cd in plant (mg/kg)

Ni total content in soil (mg/kg)

Ni total content in soil (mg/kg)

140 120 100 80 60 40 20 0

80

60

40

20

0 0 5 10 15 20 25 30 35

e
40

f
0 5 10 15 20 25 30 35

Ni in tillering (mg/kg)
120

Ni in shooting (mg/kg)

Ni total content in soil (mg/kg)

100

80

60

40

20

g
0 0 5 10 15 20 25 30

Ni in earing (mg/kg)
Fig. 1. Curves tted according to Equation (5) (equivalently Equation (6)) for experimental results. a), b), c) and d) by Moreno et al. (2006). e), f) and g) by Poulik (1997).

S.D. Guala et al. / Environmental Pollution 158 (2010) 2659e2663

2663

shooting and earing of living oats (Avena sativa L.) are 35.73, 31.47, 28.81 respectively, corresponding to a dose of 84 mg kg1 of Ni in soil. In this case, in Table 3 the model predicts plant death before 66.31, 37.52, and 32.82 respectively. Table 2 shows the Cd thresholds in ryegrass (Lolium perenne, L.) (Moreno et al., 2006) both for the total and available Cd content in soil. In the case of uncultivated soil, the last value for Cd concentration in a living plant is 228 mg kg1 corresponding to a total Cd content of 2000 mg kg1 and available Cd of 778 mg kg1. In the case of cultivated soil, the last value for a living plant is 721 mg kg1 corresponding to a total Cd content of 5000 mg kg1 and available Cd in soil of 1030 mg kg1, which is the highest concentration recorded. A test for the accuracy of the different approaches of the model could be computed by the relative difference between C3 tted from Equation (5) and from Equation (6). According to Table 4, the model predicts plant death in uncultivated soil before reaching a Cd concentration in the living plant of 425.1 mg kg1 and 529.7 mg kg1 for Cd dose and Cd in soil, respectively, with an accuracy of more than 80%. Similarly, the model predicts plant death in cultivated soil before reaching a Cd concentration in the living plant of 2169 mg kg1 and 1629 mg kg1 for Cd dose and Cd in soil, respectively, with an accuracy of more than 75%. 4. Discussion The concentration of metals in plants, and in parts of plants, can be predicted by a simple kinetic model based on the concentration of metals in the soil. This fact can be linked to physiological absorption mechanisms in plants. Hamon et al. (1999) found out a plateau in the accumulation of metals by plants attributed to physiological reasons. The pattern of accumulation by plants is quite similar to saturable uptake of metals described for root membrane transporters of Cd, Zn or Hg (Lombi et al., 2009; Esteban et al., 2008). The model proposed in this study makes possible to characterize the nonlinear behavior of the soileplant interaction with metal pollution, in order to contribute towards establishing threshold values for the toxic effects of metals on plants and eventual plant mortality. The model can be applied to different plants or crops in order to understand how the different concentrations of metals that can be found in the soil can inuence their growth. Also knowing the threshold values for toxic effects on plants and knowing the concentrations of metals that are in the soil will help to choose the most suitable crop for each eld in order to remediate the soil contamination by means of biouptake. The effects of metals on plant development vary according to the different soil characteristics, the type of plant and the type of metal. As a result, the model makes it possible to directly compare the relative fragility of different environments to the same pollutant. Finally, the effects of metals on both plants and crops must be taken into account in order to establish the risk of these contaminants being transferred to the food chain. Acknowledgements This study was supported by the Xunta de Galicia in partnership with the University of Vigo through ngeles Alvario and Parga Pondal research contracts awarded to F.A. Vega and E.F. Covelo, respectively. References
Adriano, D.C., 1986. Trace Elements in the Terrestrial Environment. Springer-Verlag, New York.

Alloway, B.J., 1995. Heavy Metals in Soils. Blackie Academic and Professional, Glasgow, UK. Athar, R., Ahmad, M., 2002. Heavy metal toxicity: effect on plant growth and metal uptake by wheat, and on free living Azotobacter. Water Air and Soil Pollution 138 (1e4), 165e180. Brun, L.A., Maillet, J., Hinsinger, P., Pepin, M., 2001. Evaluation of copper availability to plants in copper-contaminated vineyard soils. Environmental Pollution 111, 293e302. Chehregani, A., Malayeri, B., Golmohammadi, R., 2005. Effect of heavy metals on the developmental stages of ovules and embryonic sac in Euphorbia cheirandenia. Pakistan Journal of Biological Science 8, 622e625. Dan, T., Hale, B., Johnson, D., Conard, B., Stiebel, B., Veska, E., 2008. Toxicity thresholds for oat (Avena sativa L.) grown in Ni-impacted agricultural soils near Port Colborne, Ontario, Canada. Canadian Journal of Soil Science 88, 389e398. De Leo, G., Del Furia, L., Gatto, M., 1993. The interaction between soil acidity and forest dynamics: a simple model exhibiting catastroc behavior. Theoretical Population Biology 43 (11), 31e51. Doelman, P., Haanstra, L., 1984. Short-term and longterm effects of cadmium, chromium, copper, nickel, lead and zinc on soil microbial respiration in relation to abiotic soil factors. Plant and Soil 79 (33), 317e327. Esteban, E., Moreno, E., Pealosa, J., Cabrero, J.I., Milln, R., Zornoza, P., 2008. Short and long-term uptake of Hg in white lupin plants: kinetics and stress indicators. Environmental and Experimental Botany 62 (3), 316e322. Friesl, W., Friedl, J., Platzer, K., Horak, O., Gerzabek, M.H., 2006. Remediation of contaminated agricultural soils near a former Pb/Zn smelter in Austria: batch, pot and eld experiments. Environmental Pollution 144, 40e50. Giller, K.E., Witter, E., McGrath, S.P., 1998. Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biology and Biochemistry 30 (10e11), 1389e1414. Gincchio, R., Rodriguez, P.H., Badilla-Ohlbaum, R., Allen, H.E., Lagos, G.E., 2002. Effect of soil copper content and pH on copper uptake of selected vegetables grown under controlled conditions. Environmental Toxicology and Chemistry 21, 1736e1744. Guala, S.D., Vega, F.A., Covelo, E.F., 2009. Modication of a soil-vegetation nonlinear interaction model with acid deposition for simplied experimental applicability. Ecological Modelling 220 (18), 2137e2141. Hamon, R.E., Holm, P.E., Lorenz, S.E., McGrath, S.P., Christensen, T.H., 1999. Metal uptake by plants from sludge-amended soils: caution is required in the plateau interpretation. Plant and Soil 216 (1e2), 53e64. Kabata-Pendias, A., 2001. Trace Elements in Soils and Plants. CRC Press, Boca Raton, Florida. USA. Lindsay, W., 1979. Chemical Equilibria in Soils. Wiley, New York. Lombi, E., Scheckel, K.G., Pallon, J., Carey, A.M., Zhu, Y.G., Meharg, A.A., 2009. Speciation and distribution of arsenic and localization of nutrients in rice grains. New Phytologist 184 (1), 193e201. MacFarlane, G.R., Burchett, M.D., 2002. Toxicity, growth and accumulation relationships of copper, lead and zinc in the grey mangrove Avicennia marina (Forsk.) Vierh. Marine Environmental Research 54, 65e84. Moreno, J.L., Sanchez-Marn, A., Hernndez, T., Garca, C., 2006. Effect of cadmium on microbial activity and a ryegrass crop in two semiarid soils. Environmental Management 37 (5), 626e633. Nannipieri, P., Badalucco, L., Landi, L., Pietramellara, G., 1997. Measurement in assessing the risk of chemicals to the soil ecosystem. In: Zelikoff, J.T. (Ed.), Ecotoxicology: Responses and Risk Assessment, an OECD Workshop. SOS Publications, Fair Haven, NJ, pp. 507e534. Nedelkoska, T.V., Doran, P.M., 2000. Characteristics of heavy metal uptake by plant species with potential for phytoremediation and phytomining. Minerals Engineering 13, 549e561. Oliver, M.A., 1997. Soil and human health: a review. European Journal of Soil Science 48 (4), 573e592. Poulik, Z., 1997. The danger of cumulation of nickel in cereals on contaminated soil. Agriculture Ecosystems & Environment 63 (1), 25e29. Ryser, P., Sauder, W.R., 2006. Effects of heavy-metal-contaminated soil on growth, phenology and biomass turnover of Hieracium piloselloides. Environmental Pollution 140 (1), 52e61. Speir, T.W., Kettles, H.A., Parshotam, A., Searle, P.L., Vlaar, L.N.C., 1995. A simple kinetic approach to derive the ecological dose value, ED50, for the assessment of Cr(VI) toxicity to soil biological properties. Soil Biology and Biochemistry 27, 801e810. Ulrich, B., Pankrath, J., 1983. Effects of Accumulation of Air Pollutants in Forest Ecosystems. D. Reidel, Dordrecht, Holanda. Ulrich, B., Mayer, R., Khanna, P.K., 1980. Chemical changes due to acid precipitation in a loess derived soil in Central Europe. Soil Science 130 (4), 193e199. Van Assche, F., Clijsters, H., 1990. Effects of metals on enzyme activity in plants. Plant Cell and Environment 13, 195e206. Walker, D.J., Clemente, R., Roig, A., Bernal, M.P., 2003. The effects of soil amendments on heavy metal bioavailability in two contaminated Mediterranean soils. Environmental Pollution 122, 303e312. Wani, P.A., Khan, M.S., Zaidi, A., 2007. Chromium reduction, plant growthpromoting potentials and metal solubilization by Bacillus sp. isolated from alluvial soil. Current Microbiology 54, 237e243. Wilke, B.M., 1991. Effects of single and successive additions of cadmium, nickel and zinc on carbon dioxide evolution and dehydrogenase activity in a sandy luvisol. Biology and Fertility of Soils 11, 34e37.

You might also like