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TECHNICAL REPORTS

Heavy Metals in the Environment

Zinc Accumulation in Plant Species Indigenous to a Portuguese Polluted Site

Relation with Soil Contamination

Escola Superior de Biotecnologia, Universidada Católica Portuguesa, Rua Dr. António Bernardino de Almeida, 4200-072 Porto, Portugal

^* Corresponding author (plcastro{at}esb.ucp.pt)

Received for publication July 18, 2006.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
The levels of zinc accumulated by roots, stems, and leaves of two plant species, Rubus ulmifolius and Phragmites australis, indigenous to the banks of a stream in a Portuguese contaminated site were investigated in field conditions. R. ulmifolius, a plant for which studies on phytoremediation potential are scarce, dominated on the right side of the stream, while P. australis proliferated on the other bank. Heterogeneous Zn concentrations were found along the banks of the stream. Zn accumulation in both species occurred mainly in the roots, with poor translocation to the aboveground sections. R. ulmifolius presented Zn levels in the roots ranging from 142 to 563 mg kg^–1, in the stems from 35 to 110 mg kg^–1, and in the leaves from 45 to 91 mg kg^–1, vs. average soil total Zn concentrations varying from 526 to 957 mg kg^–1. P. australis showed Zn concentrations in the roots from 39 to 130 mg kg^–1, in the stems from 31 to 63 mg kg^–1, and in the leaves from 37 to 83 mg kg^–1, for the lower average soil total Zn levels of 138 to 452 mg kg^–1 found on the banks where they proliferated. Positive correlations were found between the soil total, available and extractable Zn fractions, and metal accumulation in the roots and leaves of R. ulmifolius and in the roots and stems of P. australis. The use of R. ulmifolius and P. australis for phytoextraction purposes does not appear as an effective method of metal removing, but these native metal tolerant plant species may be used to reduce the effects of soil contamination, avoiding further Zn transfer to other environmental compartments.

Abbreviations: BCR, Community Bureau of Reference • EDTA, ethilenediaminetetraacetic acid • FA-AAS, flame atomic absorption spectroscopy • HCl, hydrochloric acid • NH₄–Ac, ammonium acetate

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
HEAVY metal contamination in ecosystems poses major environmental problems worldwide with substantial economic consequences. Phytoremediation—the use of plants to remove (phytoextraction) or immobilize (phytostabilization) contaminants (Salt et al., 1998)—may offer a safe and low cost method for the remediation of metal-contaminated soil. The relatively low potential cost of phytoremediation allows the treatment of sites that cannot be addressed with currently available engineering methods, while preserving the topsoil. Plants can be grown and harvested economically, leaving only residual levels of pollutants (Ensley, 2000).

Heavy metals play an important role in plant metabolic functions and some, such as zinc, are essential for plant growth and are involved in numerous physiological processes (Rengel, 1999). However, at high concentrations they are strongly toxic and may impair the growth of some plant species. The metal phytoavailability—fraction of the total contaminant mass in soil actually available for the receptor plant (National Research Council, 2003)—has emerged as an important paradigm, replacing the old belief that biological response by receptor organisms could be predicted by the total concentration in the soil (Adriano et al., 2004). During the investigation of metal bioavailability different soil extraction techniques should be used (Lasat, 2002). In general, aqueous extraction seems to provide an estimate of the amount of bioavailable metal in the soil solution. Estimates of the total bioavailable metal, which includes not only the metal available in soil solution but also the metal ions bound to soil exchange sites, are obtained by extracting the soil with organic compounds.

Many studies have been conducted to identify plant species capable of accumulating Zn. Thlaspi caerulescens is probably the best known Zn hyperaccumulator species (Whiting et al., 2001). Schwartz et al. (2001) showed evidence that the plants Armeria maritima and Arabidopsis halleri are Zn and Pb hyperaccumulators. Peralta-Videa et al. (2004) presented Medicago sativa plants as an option for cleaning up soils through Zn tissue accumulation. Brassica juncea (Ebbs and Kochian, 1998) and several willow species (Vandecasteele et al., 2004) have also been reported amongst the plants with potential for the phytoremediation of Zn.

It is often difficult to predict the behavior and fate of a metal on a contaminated matrix only through an extrapolation of results obtained from laboratory ecotoxicity experiments (Straalen and Denneman, 1989). In the field, differences in the metal availability for plant uptake, operation of ecological compensation mechanisms, exposure to metal mixtures, and adaptation to metal stress may occur (Lock et al., 2003). Field studies are necessary to obtain information on how indigenous plants behave under the conditions installed. The use of fast-growing pioneer species capable of colonizing poor, contaminated soils is potentially very useful for phytoremediation strategies (Alvarez et al., 2003). Studies identifying species with potential capacity for heavy metal accumulation are necessary and valuable when selecting the most appropriate plants for phytoremediation strategies. In addition, it is important to study the accumulation of the contaminant in the different plant sections (root and shoot). A plant which accumulates higher levels of the contaminant in its harvestable sections (usually stems and leaves) is considered a good candidate for phytoextraction (Blaylock and Huang, 2000), while a species which restricts the accumulation to its roots will be useful for the stabilization of the contaminated soil, reducing the human health and environmental hazards by a different but yet equally protective strategy–phytostabilization (Berti and Cunningham, 2000).

A large industrial complex, composed essentially by chemical facilities, surrounds the area considered in the present study. For many years, several of these industries have discharged their solid residues in an improvised sediment basin in the surrounding area, and released its wastewaters into a nearby stream—"Esteiro de Estarreja"—which is a small and almost stagnated watercourse (Oliveira et al., 2001). Profiting from the high permeability of the site, the percolates proceeding from this improvised sediment basin infiltrated in the soil of the area. Therefore, the levels of heavy metals in the sediments of this stream are above the limits established by EC Directive 86/278/EC (Atkins, 1999). Among the metals present at higher levels in those sediments—average levels of 835 mg Pb kg^–1, 66 mg Hg kg^–1, 26 mg Cr kg^–1, 37 mg Ni kg^–1, 16 800 mg Fe kg^–1 were measured for the site (Oliveira et al., 2001)—Zn appears as one of the main contaminants, with the soils presenting levels of up to 3620 mg Zn kg^–1 (total Zn) (Oliveira et al., 2001). The area near the former exit of contaminated wastewaters is the most polluted one (to a distance of ca 50 m further from the exit), although the contamination along the banks and between banks is very heterogeneous, and is mainly occurring in the top 20 cm layer of the soil (Atkins, 1999; Oliveira et al., 2001). The banks of the stream (with a slope of approximately 45°), with approximately 2-m width, are periodically flooded with rainwater, from late October to late February, and the ditch of the stream (with approximately 1.5-m depth) remains almost dry during the remaining months. Despite the high levels of metals in the sediments, the vegetation in the banks of the stream remains prolific, yet heterogeneously distributed. Two plants appeared as the main colonizers: Rubus ulmifolius Schott dominating the side where the wastewaters were discharged and Phragmites australis (Cav.) Trin. ex Steudel being the main colonizer on the opposite side. Both R. ulmifolius and P. australis are plant species widely distributed throughout this region of Portugal. Remediation studies using P. australis, namely for Cd (Ali et al., 2004) and also for Pb- and Zn-contaminated mine tailings (Ye et al., 1997) have shown that the plant is able to accumulate these metals. R. ulmifolius was mentioned as a vascular plant growing on mine refuse (Freitas and Prasad, 2003), but studies evaluating metal accumulation are not common.

The aim of this study was to determine the accumulation of Zn in different sections—roots, stems, and leaves—of plants colonizing a contaminated site (P. australis and R. ulmifolius), and relate that feature to the Zn content of the soil. Accordingly to the accumulation patterns and abilities of R. ulmifolius and P. australis, the analysis of their possible application in soil phytoremediation was evaluated.

	MATERIALS AND METHODS

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Research Site and Sampling Techniques
Plant and soil sampling was made at seven different spots in each bank, starting near the conduct exit and following the stream course, with each of the species being collected from the bank in which they were predominant. The seven collection spots in each bank were separated by 10 m from each other, as performed by Atkins (1999), to cover a high range of soil metal concentrations potentially toxic to plants, profiting from the heterogeneity of the site contamination. At each sampling location, 0.5 m sided squares delimited the location from which plant samples were collected. In each square three plants were collected randomly—selected plants were approximately 1.5 and 1 m in height, for P. australis and R. ulmifolius, respectively. A soil sample from each plant rooting zone (0- to 20-cm depth) was also collected. Sampling was made in the dry season, particularly in the flowering season for each one of the plant species in the site—April for R. ulmifolius and August for P. australis. In addition, soil and R. ulmifolius and P. australis plant samples, in a similar development stage, from uncontaminated areas were collected, using the same procedure.

Soil Analysis
Soil samples were oven-dried at 40°C for 48 h and passed through a 2-mm sieve. The soil pH was measured using a 1:2.5 soil/water ratio. Water content was determined by drying pre-oven-dried (40°C) soil at 105°C until constant mass was achieved. Organic matter content was determined by loss on ignition. Samples for total phosphorous and nitrogen were digested at high temperatures (up to 330°C) with a Se and salicylic and sulfuric acids mixture. For total N colorimetric determination, two reagents were added to the digests: reagent 1, consisting of a mixture of a 5 x 10^–2 M dissodium hydrogen phosphate buffer (pH = 12.3) and a 4% bleach solution, and reagent 2 consisting of a mixture of a 1 M salicylate solution, a 1 x 10^–3 M sodium nitroprusside solution and a 3 x 10^–3 M EDTA solution. For total phosphorous colorimetric determination, two different reagents were added to the digests: reagent 1, consisting of a 3 x 10^–2 M ascorbic acid solution and reagent 2 consisting of a mixture of a 6 x 10^–3 M antimonyl tartarate solution, a 5 x 10^–3 M ammonium molybdate solution, 0.7 M sulfuric acid, and an anticoagulation agent (Wetting aerosol 22, Cytek, New Jersey, USA). The elements concentration on the resulting preparations was determined on an UNICAM HELIOS spectrophotometer (Waltham, USA), at 660 nm for nitrogen and 880 nm for phosphorous. For total soil Zn determination, soil samples were digested at high temperatures (up to 140°C) with concentrated nitric and hydrochloric acids (1:1). All previous methods were based on Houba et al. (1995). The water (De Koe, 1994), exchangeable (Thomas, 1982)—ethilenediaminetetraacetic acid (EDTA)-extractable—, and available (Thomas, 1982)—ammonium acetate (NH₄–Ac)-extractable—Zn fractions were determined using, respectively, 1:5 soil/water (De Koe, 1994), 1:5 soil/1M NH₄–Ac (De Koe, 1994), and 1:10 soil/0.05 M EDTA (Houba et al., 1995) ratios. The resulting solutions were incubated for 2 h at 20°C, after which they were filtrated through a 0.45-µm cellulose acetate filter. The Zn content of the resulting digests and extracts were determined using flame atomic absorption spectroscopy (FA-AAS) in an UNICAM 960 spectrophotometer (Waltham, USA) (Houba et al., 1995). BCR (Community Bureau of Reference) reference sample CRM 141 R (calcareous loam soil) was analyzed through the referred total Zn determination analytical method. The value obtained by FA-AAS (281 ± 1 mg Zn kg^–1 sample) confirmed the accuracy and precision of the method by comparison with the certified value (283 ± 5 mg Zn kg^–1 sample).

Plant Analysis
Entire plants were washed with tap water, followed by washing with HCl 0.1 M, and with demineralized water, after which they were separated in roots, stems, and leaves, oven-dried at 70°C for 48 h, grinded, and sieved to <1 mm. The resulting samples were digested at high temperature (up to 205°C) with a mixture of concentrated nitric, perchloric, and sulfuric acids (40:4:1). Zinc content was determined using FA-AAS of the digests (Wallinga et al., 1989). BCR (Community Bureau of Reference) reference sample CRM 279 (sea lettuce) was analyzed using the above-described total Zn determination analytical method. The value obtained by FA-AAS (52.3 ± 1.5 Zn kg^–1 sample) confirmed the accuracy and precision of the method by comparison with the certified value (51.3 ± 0.2 mg Zn kg^–1 sample).

Statistical Analysis
Statistical analysis was performed using the SPSS program (SPSS Inc., 2003). The data were analyzed through analysis of variance (ANOVA). To detect the statistical significance of differences (P < 0.05) between means, the Tukey test was performed. Regression analyses were performed with different variables and Spearman's correlation coefficients were determined.

Chemicals
The chemicals used were analytical grade and were obtained from Pronalab (liquid reagents), and Merck (solid reagents).

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Soils
The soil collected from the banks of the stream presented a range of pH from 5.3 to 7.5, a water content ranging from of 1.1 to 2%, and organic matter contents ranging from 7.5 to 12% (Table 1). The nutrient content of the soils was variable. The levels of nitrogen in the contaminated soils were higher than the levels found in the control sites (Table 1).

View this table: [in this window] [in a new window]   Table 1. Soil properties of the study sites.

View this table: [in this window] [in a new window]   Table 2. Total and extractable Zn concentrations in soils from different sampling locations of P. australis.

View this table: [in this window] [in a new window]   Table 3. Total and extractable Zn concentrations in soils from different sampling locations of R. ulmifolius.

Plants
The Zn content in the sections of plants collected in the banks of the stream varied among sites of collection, for both species (Fig. 1). In R. ulmifolius, Zn concentrations (mg kg^–1) ranged from 142 to 563 in the roots, 35.5 to 110 in the stems, and 45.1 to 90.8 in the leaves. In P. australis Zn concentrations (mg kg^–1) ranged from 39.4 to 130 in the roots, 31.2 to 63.3 in the stems, and 37.3 to 82.6 in the leaves. P. australis presented accumulation levels similar to those registered by Aksoy et al. (2005) for P. australis growing in a polluted wetland in Turkey—average Zn accumulation of approximately 70, 41, and 22 mg kg^–1dry wt., for respectively roots, stems, and leaves were reported.

View larger version (40K): [in this window] [in a new window]   Fig. 1. Zinc levels in (a) P. australis and (b) R. ulmifolius sections.

View this table: [in this window] [in a new window]   Table 5. Zinc concentration in the different plant parts for P. australis.

View this table: [in this window] [in a new window]   Table 6. Zinc concentration in the different plant parts for R. ulmifolius.

In this study, despite the clear influence of the soil contamination in the accumulation of Zn by P. australis and R. ulmifolius, the amounts were almost always below the Zn phytotoxic levels reported for plants—500 to 1500 mg kg^–1, according to Chaney (1989). Exceptions were registered in some cases for R. ulmifolius roots (according to the range presented in Table 6). The roots of both plant species, especially of R. ulmifolius, presented Zn levels generally above the considered normal levels of Zn in plant tissues—10 to 100 mg kg^–1, according to Frisberg et al. (1986), which may indicate that these plant species growing on the contaminated site were tolerant to Zn. Significant (P < 0.05) differences between the Zn levels in the roots and the aboveground sections (stems and leaves) were observed for both plant species (Tables 5 and 6). Zinc was mainly accumulated in the roots of both plant species, indicating poor metal translocation into stems and leaves. Similar differences between root and aboveground concentrations of Zn have been observed for other plant species (Armeria maritima ssp. halleri and Agrostis tenuis) (Dahmani-Muller et al., 2000), and Osmorhiza longistylis (Mbila and Thompson, 2004) and may suggest a Zn exclusion strategy from stems and reproductive tissue by retaining the metal in the roots (Baker, 1981). The mechanism behind the successful growth of these species in the site may also be a reason to disregard the use of these plants in a phytoextraction strategy. The harvest of the aboveground sections will not be an effective source of metal removal from a contaminated soil matrix, as the plant is excluding the metal from these sections, and concentrating it at the root zone. Tolerant plants tend to restrict soil-root and root-shoot transfers, having much less accumulation in their biomass (Yoon et al., 2006). However, from a toxicological point of view, this may be a desirable property, as Zn would not pass into the food chain via herbivores thus avoiding further environmental risks (Deng et al., 2004).

Soil–Plant Relations
The metal uptake by plants is largely influenced by the bioavailability of the metal in the soil. In previous studies it has been shown that the accumulation of metals, both by roots and aboveground tissues, was not linear in correlation to the soil metal concentration increase (Keller et al., 1998; Greger, 1999). Nevertheless, Cardwell et al. (2002) have reported that aquatic macrophytes exhibited an increasing Zn accumulation with an increasing sediment metal concentration.

Regression analyses were performed with the levels of Zn in plants roots, stems, and leaves vs. the total, water-extractable, available (EDTA-extractable), and exchangeable (NH₄–Ac-extractable) Zn concentrations in the soil (Table 7). For P. australis, positive correlations were found between Zn concentrations in the soil with all the different extractants and the Zn levels in the roots and stems sections. As to the levels of Zn in the leaves, no correlation was seen with the soil concentration (Table 7). An increase in Zn soil concentration (total and EDTA, H₂O, and ammonium acetate-extractable fractions) resulted in an increasing accumulation in the stems and especially in the roots. For R. ulmifolius, positive correlations were found between Zn concentrations in the soil with different extractants (with the exception of water-extractable Zn) and the Zn levels in the roots and leaves, with stronger correlations being found for the roots. Regarding the levels of Zn in the stems, no correlation with the soil concentrations was found (Table 7). This indicates that an increasing Zn soil concentration (total and EDTA and ammonium acetate-extractable fractions) results in an increasing accumulation in the stem and especially in the root.

Regression analyses were performed only between metal concentrations in plant root, stem, and leaves, and in the soil (with different extractants). The lack of correlation obtained in some cases may imply that in isolation these factors are not dominant in determining metal accumulation by that plant part. It is possible that variation and interaction of these factors with parameters such as organic content (Wright and Otte, 1999), pH (van der Merwe et al., 1990), soil nutrient status (Deng et al., 2004), and salinity (Fitzgerald et al., 2003) obscures any possible relationship between Zn in the soil and in the plant.

Bioconcentration factors (BCF values) based on dry weight have been determined for the different plant sections (root, stems, and leaves), expressed as the ratio between the metal concentration in the plant section and in soil (Fig. 2). The BCF has been used to evaluate plant availability of heavy metals in contaminated soils (Li et al., 2006; Yoon et al., 2006). In this study, the highest BCF value registered was 0.54, obtained for R. ulmifolius growing on collection site 2. Plants exhibiting BCF values less than one are referred to be unsuitable for phytoextraction (Fitz and Wenzel, 2002). Nevertheless, these species established successfully on the Zn-polluted soil, whether or not metal was taken up into their aboveground tissues, and their application may be interesting in the rehabilitation of Zn-contaminated soils via phytostabilization. Metals accumulated in the roots are considered relatively stable concerning their release to other environmental compartments, such as water and biota (Yoon et al., 2006).

View larger version (44K): [in this window] [in a new window]   Fig. 2. Bioconcentration factors (BCF) for (a) P. australis and (b) R. ulmifolius sections.

	CONCLUSIONS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

	ACKNOWLEDGMENTS

 
The authors wish to thank Câmara Municipal de Estarreja for the provision of access to the site. Ana Marques had the support of a Fundação para a Ciência e a Tecnologia grant SFRH/BD/7030/2001. The work was funded by Project MICOMETA- POCI/AMB/60131/2004 (Fundação para a Ciência e Tecnologia).

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TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 

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