Zinc tolerance and accumulation in Pteris vittata L. and its potential for phytoremediation of Zn- and As-contaminated soil

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1 Chemosphere 62 (26) Zinc tolerance and accumulation in Pteris vittata L. and its potential for phytoremediation of Zn- and As-contaminated soil Zi-Zhuang An, Ze-Chun Huang, Mei Lei, Xiao-Yong Liao, Yuan-Ming Zheng, Tong-Bin Chen * Center for Environmental Remediation, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, 11A Datun Road, Beijing 111, PR China Received 26 January 25; received in revised form 6 April 25; accepted 15 April 25 Available online 28 June 25 Abstract A field investigation and pot experiments were conducted to determine the potential of arsenic (As) hyperaccumulator, Pteris vittata L., to remediate sites co-contaminated with zinc (Zn) and As. We found that P. vittata L. had a very high tolerance to Zn and grew normally at sites with high Zn concentrations. In addition, P. vittata L. could effectively take up Zn into its fronds, with a maximum of 737 mg kg 1 under field conditions. In pot experiments, the accumulated Zn concentration increased significantly as the Zn treatment was raised from to 2 mg kg 1, with a maximum Zn accumulation of.22 mg pot 1. Although the concentration of As in P. vittata L. was reduced by the addition of Zn, total frond accumulation of As was elevated when the Zn treatment was increased from to 1 mg kg 1, with a maximum As accumulation of 8.3 mg pot 1 in the presence of 1 mg kg 1 Zn. The high Zn tolerance, relatively high ability to accumulate Zn, and great capacity to accumulate As under conditions of suppression by high Zn suggest that P. vittata L. could be useful for the remediation of sites co-contaminated with Zn and As. Ó 25 Elsevier Ltd. All rights reserved. Keywords: Accumulation; Arsenic; Hyperaccumulator; Pteris vittata L.; Tolerance; Zinc 1. Introduction Phytoremediation, the use of green plants to remove pollutants from soils, has been considered as a promising technique for the remediation of contaminated soils (Salt et al., 1995). Pteris vittata L., an arsenic (As) * Corresponding author. Tel.: ; fax: address: chentb@igsnrr.ac.cn (T.-B. Chen). hyperaccumulator discovered independently by ChenÕs and MaÕs groups, has a great capacity to phytoextract As from soils (Ma et al., 21; Chen et al., 22; Tu et al., 22). The excellent potential of this plant to remediate As-contaminated soils was verified in the first field demonstration of As phytoremediation in Chenzhou City, Hunan Province of Southern China in 2. For example, it was shown that, within 7 months, P. vittata L. could clean up to 7.8% of the As from soil where the As concentration was 64 mg kg 1 (Liao et al., 24) /$ - see front matter Ó 25 Elsevier Ltd. All rights reserved. doi:1.116/j.chemosphere

2 Z.-Z. An et al. / Chemosphere 62 (26) Zinc (Zn) is an essential element for normal growth and development of plants. This metal plays an important role in several metabolic processes in plants. Zn deficiency is one of the most widespread micronutrient deficiencies in many regions of the world (Cakmak, 2; Fageria et al., 22). On the other hand, excess Zn in soils caused by anthropogenic activities, such as mining, metal refining (Fialkowski et al., 23), compost application (Ramos and López-Acevedo, 24), and wastewater irrigating (Yediler et al., 1994), may retard the growth and development of plants (Alia et al., 1995; Kamal et al., 24), and induce damage to the ecosystem (Nahmani and Lavelle, 22; Lock et al., 23). Because As usually occurs together with Zn in minerals, As contamination caused by mining and refining is often accompanied by Zn contamination (Black and Craw, 21; Kim et al., 23). Moreover, the use of chromated-copper arsenate with Zn sulfate as a wood preservative (Hingston et al., 21; Bhattacharya et al., 22) may also cause co-contamination of soils with Zn and As. Therefore, whether P. vittata L. can be used to clean up As from soils co-contaminated with Zn is an important issue. Fayiga et al. (24) carried out pot experiments to study the effect of heavy metals on As concentration by P. vittata L., but the Zn concentration,.8 mg kg 1, in the soil used in their studies was much lower than in normal soil. In fact, we found in the present study that Zn contamination in soil, especially in mining and refining areas, was high (up to thousands of mg kg 1 ). Furthermore, whether P. vittata L. could be used in the phytoremediation of soil heavily contaminated with Zn has not been verified. Therefore, we conducted both a field investigation and pot experiments to understand the ability of P. vittata L. to endure Zn toxicity and to examine the impact of Zn on As accumulation. These studies should provide useful information for the application of P. vittata L. to remediate soils co-contaminated with As and Zn. 2. Materials and methods 2.1. Field sites A field investigation was carried out in Guangxi and Hunan Provinces of Southern China. Fronds and roots of well grown P. vittata L. and rhizosphere soils were sampled from 22 sites where P. vittata L. were found. Sites 1 7 were located in Guangxi Province with a tropical plateau monsoon-type climate, and the other 15 sites were located in Hunan Province with a subtropical monsoon-type climate. Except for the sites 1 5 and 7, the other sites were all located near metal mines or refineries. Of these, site 6 was located in a manganese mining area, 8 1 were located near a vanadium mine, near a nonferrous refinery, and near two lead (Pb) Zn and copper (Cu) mining areas, and near a tin (Sn) refinery Pot experiment The soil used for cultivation was a loam cinnamon soil (Typical Agric-Udic-Luvisols) collected from the top layer ( 2 cm) of farmland in Beijing, China. The soil ph (soil:water = 1:1) was 7.9. The soil contained 14.4 g kg 1 of organic matter, 1.1 g kg 1 of total N, 19. mg kg 1 of Olsen-P, 85.2 mg kg 1 of NH 4 OAcextractable K, 5.5 mg kg 1 of total As, 75.8 mg kg 1 of total Zn and 3.9 mg kg 1 of DTPA-extractable Zn. A rate of 4 mg kg 1 As, applied as Na 2 HAsO 4 Æ7H 2 O, was added to each pot contained 5 g of soil, and then amended with KH 2 PO 4 (.4 g pot 1 ) and (NH 4 ) 2 - SO 4 (.9 g pot 1 ) as basal fertilizers. The soils were treated four times with, 5, 1, 2 and 3 mg kg 1 Zn, applied as ZnSO 4 Æ7H 2 O, and then incubated for 1 month. Full-grown sporelings of P. vittata L. with three or four true leaves, which had been propagated from spores collected from lead Zn mine areas in Hunan Province, China, were transplanted into the pots. The plants were allowed to grow in greenhouse for 15 weeks with light phase of 12 h per day and at a temperature of 3/ 22 C (day/night) Sampling and analysis Field and greenhouse plant samples were washed with tap water followed by three rinses with deionized water and then separated into roots and fronds with stainless steel scissors. The biomass of each pot was measured after oven drying at 6 C to a constant weight. Soil and plant samples were ground to fine powder using an agate mortar, weighed, and digested with a 4:1 (v/v) mixture of nitric/perchloric acid according to the method described by USEPA (35B). Diethyltriaminepenta acetic acid (DTPA)-extractable Zn was obtained by using a mixture of.5 M DTPA,.1 M CaCl 2, and.1 M triethylamine (ph 7.3) (Lindsay and Norvell, 1978). Water-soluble As was extracted using a 1:1 soil/water ratio. The concentrations of Zn and As were determined using a flame atomic absorption spectrophotometer (Vario 6, Analytik Jena, Germany) and an atomic fluorescence spectrophotometer (AFS-222, Beijing Haiguang Co., China), respectively. 3. Results 3.1. Properties of soils and Zn concentrations in P. vittata L. at field sites Soil ph varied greatly, from 4.6 at site at site 19, among sites where P. vittata L. grew (Table 1). It

3 798 Z.-Z. An et al. / Chemosphere 62 (26) Table 1 Important properties of soils and Zn concentrations of P. vittata L. at field sites investigated Site Soil ph Soil As (mg kg 1 ) Soil Zn (mg kg 1 ) Plant Zn (mg kg 1 ) Total DTPA-extractable Root Frond ND ND ND ND ND: not detected; BF (bioaccumulation factor) means the ratio of Zn concentration in frond of P. vittata L. to that in soil; TF (translocation factor) means the ratio of Zn concentration in frond to that in root of P. vittata L. BF TF indicated that P. vittata L. could survive at a wide range of soil ph in field naturally, and soil ph might not be a limiting factor for P. vittata L. to be used in field phytoremediation. Concentrations Zn and As in the soils also varied over a wide range in soils investigated (Table 1). They were relatively low at sites 1 1 located in Guangxi Province, but high up to hundreds and thousands mg kg 1 at sites near Pb, Zn, Cu, Sn and nonferrous mining or refining areas (sites 11 22). Furthermore, among most of the sites 11 22, high As concentration usually occur together with high Zn concentration in soil at the same site. It indicated that those sites might seriously co-contaminated with As and Zn. P. vittata L. could well grow in those sites might show it capability to be used to phytoremediate or revegetate sites co-contaminated with As and Zn. DTPA-extractable Zn was measured to estimate the bioavailable Zn in field site. It was relatively low at sites 1 1, but relatively high at sites where total Zn in soils was also higher (Table 1). Bioavailability of soil Zn (the ratio of DTPA-extractable Zn to total Zn at same site) varied site to site, for example, DTPA-extractable Zn only accounted for.6% of the total Zn in soil at site 12, but it accounted for 2.2% at site Zn accumulation and translocation in P. vittata L. in the field Except for sites 1 1, where Zn concentrations especially bioavailable Zn concentrations were relatively low, Zn concentrations in P. vittata L. in other sites were relatively high. They reached up to 816, 727, and 674 mg kg 1 in the roots at sites 12, 15, and 22 and up to 737, 474, and 563 mg kg 1 in the fronds at sites 17, 19, and 22, respectively (Table 1), suggesting that P. vittata L. has a great capacity to accumulate Zn. The Zn concentration in the roots and the fronds positively correlated with total Zn in the soil, and the correlations were significant with P =.1 (r =.73, n = 19) and.5 (r =.48,n = 22) for the roots and the fronds, respectively. Thus, Zn accumulation in P. vittata L. was greatly affected by the soil Zn concentration. Although P. vittata L. has a relatively high capacity to accumulate Zn, Zn accumulation was lower than the limit of Zn hyperaccumulation (Yang et al., 22). Regardless of whether the sites had high or low soil Zn concentrations, the bioaccumulation factor (BF) for Zn in P. vittata L., defined as the ratio of Zn concentration in frond to that in soil, was always less than 1.

4 Z.-Z. An et al. / Chemosphere 62 (26) (the maximum was.76 at site 4). In contrast, the translocation factor (TF) for Zn in P. vittata L., defined as the ratio of Zn concentration in frond to that in root, at most of the sites investigated was more than 1. (the maximum was 3.25 at site 4) (Table 1). High TFs for Zn in P. vittata L. indicated that it has relatively high ability to transport Zn to aboveground tissues Zn tolerance of P. vittata L. grown in a greenhouse Total and frond dry biomass increased significantly when the Zn application increased from to 1 mg kg 1. In addition, the biomass at 1 mg kg 1 Zn treatment was nearly two-fold higher than it was in the absence of added Zn (Fig. 1). This suggested that the growth of P. vittata L. benefits from a moderate concentration of Zn (61 mg kg 1 ) in the soil. However, both total and frond biomass were significantly reduced as more than 1 mg kg 1 Zn were applied, which indicates that excessive level of Zn also suppresses the growth of P. vittata L. Although the biomass decreased when more than 1 mg kg 1 was applied, the biomass Biomass of P. vittata L. (g pot -1 DW) Frond Total Zn addition to soil (mg kg -1 ) Fig. 1. Biomass of P. vittata L. after growing for 15 weeks in soils amended with 4 mg As kg 1 and various concentration of Zn. Vertical bar for each point represents the standard deviation for 4 replicates. when 2 mg kg 1 Zn was added to the soil (24.7 mg kg 1 of bioavailable Zn (Table 2)) was still greater than without added Zn (Fig. 1), which suggests that P. vittata L. has a relatively high tolerance to Zn Zn accumulation in P. vittata L. grown in a greenhouse The Zn concentration in P. vittata L. increased significantly as Zn addition increased from to 2 mg kg 1 (Fig. 2a). It was consistent with that Zn concentrations in P. vittata L. positively correlate with total Zn in the soil in field investigation. The maximum Zn accumulation in frond (mg pot -1 ) Zn concentration in frond (mg kg -1 ) Frond Root Zn addition to soil (mg kg -1 ) a b Zn concentration in root (mg kg -1 ) Fig. 2. Zinc concentration (a) in frond (j), root () of P. vittata L and Zn accumulation (b) in frond of P. vittata L. with various concentration of Zn addition. Vertical bar for each point represents the standard deviation for 4 replicates. Table 2 DTPA-extractable Zn and water-soluble As in soil in pot experiments Zinc addition (mg kg 1 ) DTPA-extractable Zn (mg kg 1 ) Water-soluble As (mg kg 1 ) 3.3 ±.8 a a 41.5 ± 2.2 a ± 3.5 b 38.2 ± 1.6 b ± 6.3 c 37.6 ± 1.8 b ± 6.1 d 36.9 ± 1.9 b ± 5.8 e 35.7 ± 1.7 b a Values are means ±SD (n = 4). Values followed by different letters in same column are significantly different at P <.5 according to S N K t-test using SPSS statistical software (SPSS Inc.).

5 8 Z.-Z. An et al. / Chemosphere 62 (26) Zn concentrations in the root and frond (3434 and 271 mg kg 1, respectively) were found in the 2 mg kg 1 Zn treatment. As the concentration of supplied Zn increased from 2 to 3 mg kg 1, the Zn concentrations in root and frond of P. vittata L. decreased slightly to 3152 and 23 mg kg 1, respectively, but they were still greater than those in the 5 mg kg 1 Zn treatment (Fig. 2a). The Zn concentrations in fronds were lower than that in roots in all treatments, which is to say that TFs of Zn in P. vittata L. were less than 1. in the greenhouse. The TFs in the greenhouse were lower than that in the field might be due to that P. vittata L. was grown in the greenhouse for only 15 weeks, a much shorter time than the years of growth period in the field. The total Zinc accumulation in frond biomass was used to determine the efficiency of P. vittata L. to remove Zn from soil. The total Zn accumulation in fronds of P. vittata L. increased linearly with Zn addition increased from to 1 mg kg 1. As the Zn addition increased from 1 to 2 mg kg 1, Zn accumulation in the fronds increased slightly, and it decrease significantly as Zn addition increased to 3 mg kg 1 (Fig. 2b). The maximum Zn accumulation in fronds was.22 mg pot 1 at 2 mg kg 1 Zn treatment. Therefore, the results indicate that, although P. vittata L. has a high tolerance to Zn, excessive Zn in the soil might not only inhibit the growth P. vittata L. (Fig. 1) but also reduce its ability to accumulate Zn Effects of Zn on As accumulation in P. vittata L. in a greenhouse The As concentration in fronds and roots of P. vittata L. decreased significantly as Zn application increased from to 3 mg kg 1 (Fig. 3a). The As concentration in fronds without Zn addition was as high as 8719 mg kg 1, but it decreased significantly when the Zn application was increased to 5 mg kg 1. The As concentration was 318 mg kg 1 at 3 mg kg 1 Zn treatment, which was only 37% of that without Zn application. Although the As concentration in roots also decreased as the concentration of applied Zn increased, in contrast to As concentration in fronds, As concentration in roots did not begin to decrease until 5 mg kg 1 Zn was added (Fig. 3a). Because arsenate might precipitate Zn in solution (Robins and Glastras, 1987), we also examined the effect of Zn addition on water soluble As. We found that, although water-soluble As tended to decrease as the Zn addition increased, it was not significantly different among the different levels of added Zn (Table 2). Compared to the effect of Zn on As concentration in P. vittata L., there was less effect of Zn on water soluble As. Thus, precipitation of arsenate by Zn might not appear to play a large role in the inhibition of As uptake by P. vittata L. As accumulation in frond (mg pot -1 ) As concentration in frond (mg kg -1 ) Although the As concentration in P. vittata L. decreased as the Zn addition increased (Fig. 3a), total As accumulated in P. vittata L. did not decrease in parallel. In fact, As accumulation was enhanced at lower levels of applied Zn (61 mg kg 1 ), and the maximum As accumulation in P. vittata L. of 8.3 mg pot 1 was attained at 1 mg kg 1 Zn treatment, which is 177% of that without Zn addition (Fig. 3b). The enhancement of As accumulation in P. vittata L. might be due to the increase in biomass at lower levels of applied Zn (Fig. 1). Although the accumulation of As in P. vittata L. was significantly reduced (by 77%) when Zn addition increased from 1 to 2 mg kg 1 (Fig. 3b), it was still similar to that of control. Therefore, As accumulation P. vittata L. does not appear to be suppressed much by Zn toxicity, even in soil with Zn concentration higher than 2 mg kg 1. Therefore, an appropriate level of Zn in soil (<1 mg kg 1 ) might promote the phytoextraction of As by P. vittata L. 4. Discussion Frond Root Zn addition to soil (mg kg -1 ) As concentration in root (mg kg -1 ) Fig. 3. Effect of Zn addition on As concentration (a) in frond (j), root () ofp. vittata L. and As accumulation (b) in frond of P. vittata L. Vertical bar for each point represents the standard deviation for 4 replicates. This study showed that P. vittata L. grew well at many field sites where the total Zn concentration in soil was greatly higher than 4 mg kg 1 and the biomass of a b

6 Z.-Z. An et al. / Chemosphere 62 (26) greenhouse-cultivated P. vittata L. was not reduced by 2 mg kg 1 Zn treatment. Whereas, it is generally considered that a total Zn concentration in soil between 7 and 4 mg kg 1 is toxic to plants (Kabata-Pendias and Pendias, 1984). So it could be suggested that, except for high As tolerance which has been shown by Ma et al. (21) and Chen et al. (22), Zn tolerance of P. vittata L. was also relatively high than normal plants. It has been considered that a Zn concentration up to 23 mg kg 1 in aboveground tissues might be toxic to normal plants (Borkert et al., 1998; Long et al., 23). However, we found that Zn concentrations could be high up to 737 and 271 mg kg 1 in fronds of P. vittata L. at some field sites and in greenhouse, respectively. These levels are much greater than those in normal plants (Outridge and Noller, 1991). The relatively high Zn concentration in P. vittata L. not only demonstrated its Zn tolerance, but also indicated its ability to remove Zn from contaminated soils. Furthermore, this study showed that the As concentration in P. vittata L. was reduced by Zn addition, which agrees with the results of Caille et al. (24) and Fayiga et al. (24). Because the efficiency of As phytoremediation is determined by the total As accumulation in its harvestable biomass and because some of the Zn treatments caused an increase in frond biomass, the maximum total As accumulation in fronds (two-fold as that without Zn addition) was found in plants treated with 1 mg kg 1 Zn. Also, As accumulation from soil treated with 2 mg kg 1 Zn was approximately the same as without Zn addition. These results suggest that P. vittata L. remains effective in As phytoremediation even in presence of high Zn co-contamination and that an appropriate level of Zn may actually promote As removal from the soil. 5. Conclusion The greenhouse experiments and field investigation in this study showed that P. vittata L. can tolerate high levels of Zn in the soil. Although excessive Zn in soil could reduce the accumulation of As by P. vittata L., As phytoremediation was effective even in soil with as much as 2 mg kg 1 of Zn. In fact, the highest efficiency of As phytoextraction was 8.3 mg pot 1 at 1 mg kg 1 of added Zn. In general, a relatively high capacity of P. vittata L. to accumulate Zn from soil was found in this study. Therefore, P. vittata L. might be useful for the remediation of soil co-contaminated with Zn and As. Acknowledgements This research was supported by the National Foundation for Distinguished Youth of China (No ), the National Natural Science Foundation of China (No ), and the National Basic Science Research Program (No. 22CCA38). References Alia, K.V., Prasad, S.K., Pardha, S.P., Effect of zinc on free radical and proline in Brassica juncea and Cajanus cajan. 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