Factors influencing arsenic accumulation by Pteris vittata: A comparative field study at two sites

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1 Environmentl Pollution 141 (2006) 488e493 Fctors influencing rsenic ccumultion by Pteris vittt: A comprtive field study t two sites C.Y. Wei*, X. Sun, C. Wng, W.Y. Wng Institute of Geogrphicl Sciences nd Nturl Resources Reserch, Chinese Acdemy of Sciences, Beijing , Chin Received 8 April 2005; ccepted 19 August 2005 Nutrient elements influenced the rsenic-ccumultion cpcity of Pteris vittt in the field. Abstrct This study compred the fctors influencing rsenic (As) ccumultion by Pteris vittt t two sites, one contining As long with Au minerliztion nd the other contining Hg/Tl minerliztion. The soils bove these two sites contined high As concentrtions (26.8e 2955 mg kg ÿ1 ). Although the As concentrtion, ph, soil ction exchnge cpcity nd plnt biomss differed significntly between the two sites, no differences were observed in the As concentrtions in the fronds nd roots, or the trnsloction fctors, of P. vittt, suggesting tht this species hs consistent As hyperccumultion properties in the field. The As concentrtion in the fronds ws positively relted to phosphorus (P) nd potssium (K), but negtively relted to clcium (C), t one site. This suggested tht P, K nd C influenced As ccumultion by P. vittt in the field. Ó 2005 Elsevier Ltd. All rights reserved. Keywords: Arsenic hyperccumultion; Nutrient elements; Phytoremedition; Soil property 1. Introduction Since the discovery of the first known rsenic (As) hyperccumultor, Pteris vittt, in Chin nd the USA, growing interest hs been focused on the mechnism of As uptke nd ccumultion by this fern. P. vittt hs high As tolernce nd good As-ccumulting bilities, nd ws shown to grow helthily both in tilings contining mg kg ÿ1 As on mining site nd in soils contining 1500 mg kg ÿ1 spiked As under greenhouse conditions (M et l., 2001; Chen et l., 2002). Another fern, Pityrogrmm clomelnos, ws lso reported to be n As-hyperccumultor nd showed gret potentil in the phytoremedition of As-contminted soils in Thilnd (Frncesconi et l., 2002; Visoottiviseth et l., 2002). Additionl screening for As hyperccumultors mong fern * Corresponding uthor. Tel.: C ; fx: C E-mil ddress: weicy@igsnrr.c.cn (C.Y. Wei). species, especilly within the genus Pteris, hs been crried out using field surveys nd/or greenhouse experiments. Pteris cretic hs been reported s nother As-hyperccumultor (Mehrg, 2002; Wei et l., 2002; Zho et l., 2002). P. vittt from Florid in the USA (M et l., 2001), Hunn in Chin (Chen et l., 2002) nd Thilnd (Visoottiviseth et l., 2002) ll show high As concentrtions in the fronds. Pteris longifoli, which is the most closely relted fern species to P. vittt, is widely distributed throughout northern USA nd Europe, nd hs been proven to be n As-hyperccumultor (Mehrg, 2002). Although field surveys nd pot/hydroponic experiments hve confirmed the As-hyperccumultion properties of P. vittt (Chen et l., 2002,b; Tu et l., 2002; Tu nd M, 2002; Zho et l., 2002), no previous studies hve compred As ccumultion by P. vittt from different loclities in the field. Arsenic is usully present in ores of gold (Au), copper (Cu), led (Pb), tin (Sn) nd zinc (Zn) (O Neill, 1995). Previous surveys showed tht soils in some minerlized sites in southern /$ - see front mtter Ó 2005 Elsevier Ltd. All rights reserved. doi: /j.envpol

2 C.Y. Wei et l. / Environmentl Pollution 141 (2006) 488e Chin hd elevted As levels from geogenic sources. P. vittt growing on different minerlized sites might provide vluble informtion on As ccumultion nd its reltionship with nutrient elements. The purposes of the present study were s follows: first, to determine the differences in As-ccumultion ptterns of P. vittt from two sites with high As levels from different geogenic sources; nd second, to investigte the possible reltionship between the ccumultion of As nd mjor nutrient elements in P. vittt. 2. Mterils nd methods 2.1. Sites nd smpling Two sites, Zimudng (ZMD) nd Lnmuhng (LMC), with high geogenic As levels were chosen for this study. Both sites were locted ner Huilong town, Xinren City, in the southwest Guizhou province of Chin, with north ltitude of 25 34#22$ nd n est longitude of #58$ for ZMD, nd north ltitude of 25 31#40$ nd n est longitude of #32$ for LMC. The distnce between the two sites ws 12 km. However, the geology differed mrkedly between the two sites: ZMD ws n Au-minerlized site, while LMC ws n unexploited mercury/thllium (Hg/Tl) e minerlized site. As ws present t both sites, nd neither site hd been contminted by nthropogenic sources of mining or smelting ctivities. Smples of P. vittt nd soil from round the roots were collected t both sites. A distnce of more thn 20 m ws kept between the smples to ensure tht they were independent nd representtive Determintion of rsenic nd soil physiclechemicl properties In the lbortory, the fern smples were seprted into fronds (bove ground) nd roots (below ground), wshed thoroughly under tp wter, rinsed in deionized wter three times nd then dried in n oven t 70 C for 5 h. Plnt smples were powdered using n electric miller nd mixed thoroughly to ensure tht they were homogenized. Soil smples were ir dried, seprted from stone nd plnt debris, nd pssed through 20 mesh (0.84 mm) before the soil ph, grin size (soil texture) nd ction-exchnge cpcity (CEC) nlyses. Sub-smples (w15 g) were ground with qurtz mortr nd pestle nd pssed through 100 mesh (150 mm) for chemicl nlysis. The ph ws mesured using 1:2.5 rtio of soil to deionized wter, the CEC ws determined by the neutrl mmonium cette method (Rhodes, 1982) nd the totl orgnic mtter (TOM) ws clculted using the WlkleyeBlck method (Nelson nd Sommers, 1982). The grin size of the soil ws determined by lser-diffrction nlysis (Mstersizer 2000, Mlvern, UK). The soil nd plnt powders were digested by mixture of HNO 3 nd HClO 4 on n electric hot plte t 120 C. Thioure nd scorbic cid were dded s reducing regents, nd the finl solution for the determintion of totl As contined 5% HCl. The As concentrtion ws determined using hydride-genertion tomic-fluorescence spectrometer (AFS830, Beijing Jitin Xiotine Compny, Chin). The concentrtions of clcium (C), Cu, iron (Fe), potssium (K), mgnesium (Mg), mngnese (Mn), sodium (N), phosphorous (P), sulphur (S) nd Zn were determined by inductively coupled plsm tomic-emission spectroscopy (ICP-AES). Stndrd soil nd plnt references (Centre for Stndrd Reference of Chin) were used to check the ccurcy of the chemicl nlysis. Milli Q wter (18 U) ws used to dilute the digested residues. All regents were of nlyticl grde or better Sttisticl nlysis Sttisticl nlysis ws crried out using SPSS softwre. Student t-tests were used to compre the following dt from the two sites: grin size, CEC, As nd nutrient concentrtions in the fronds nd roots of P. vittt, nd As nd nutrient concentrtions in the soil round the roots. Correltions were evluted using the bi-vrition method, with two-tiled significnce nd Person correltion coefficients. Principle components nlysis (PCA) ws used to test the inter-reltionships mong the different elements in P. vittt t ech site. 3. Results nd discussion 3.1. Ecology of P. vittt t the two sites Although the soils t both sites contined high levels (26.8e2955 mg kg ÿ1 ) of As from geogenic sources, P. vittt grew well, which indicted high As tolernce. The nlyticl results showed only minor chnges in ph, CEC, TOM nd soil texture for both sites, suggesting tht the soil properties t ech were reltively uniform. However, the As concentrtions vried gretly nd showed mrked heterogeneity in the field. The soils t the two sites differed significntly in ph: the men vlue ws 7.1 (6.5e8.0) t ZMD compred with 5.9 (5.0e6.7) t LMC. The snd nd silt contents s well s the CEC t the two sites were lso significntly different. The As nd P concentrtions in the soils of the two sites were significntly different, with higher As nd lower P t ZMD compred with those t LMC (Tble 1). Thus, the soil properties between the two sites t which P. vittt grew were evidently different Hyperccumultion of rsenic by P. vittt All of the plnt smples contined high As concentrtions, with verge vlues of 1104 nd 810 mg kg ÿ1 in the fronds t ZMD nd LMC, respectively. The As concentrtions in the roots were lower thn those in the fronds, with verge vlues of 690 nd 536 mg kg ÿ1 t ZMD nd LMC, respectively. These results were consistent with previous reports on P. vittt grown under controlled pot/hydroponic conditions (Chen et l., 2002b; Zho et l., 2002; Co, et l., 2003; Tu nd M, 2003, 2005). More thn one-hlf of the smples of P. vittt hd greter As concentrtions in the fronds thn those detected in the soils (dt not shown). The verge trnsloction fctors (the rtio of the As concentrtion in the fronds Tble 1 Arsenic concentrtion nd bsic property of soils t the two sites Sites ph CEC (mmol 100 g ÿ1 ) TOM (g kg ÿ1 ) Texture (%) As (mg kg ÿ1 ) P (mg kg ÿ1 ) Fe (mg kg ÿ1 ) Snd Silt cly ZMD 7.1 G 0.4** 28.3 G 3.8** 6.2 G G G 2.2* 42.7 G G 653** 973 G G 7337 LMC 5.9 G G G G 5.1* 22.9 G G G G 365** G * ZMD: Zimudng (n Z 14), LMC: Lnmuchng (n Z 13). Sttisticl difference of the dt between the two sites t the level of *P! 5, **P! 1. Dt re presented s mens G SD.

3 490 C.Y. Wei et l. / Environmentl Pollution 141 (2006) 488e ZMD LMC b mg kg ZMD LMC b b b 0 TF BF 1 As C Cu Fe K Mg Mn N P S Zn Fig. 1. Comprison of the vlues of rsenic trnsloction nd bioccumultion fctor in Pteris vittt t the two sites. Brs with the sme letter re not significntly different (P! 5). ZMD: Zimudng (n Z 14); LMC: Lnmuchng (n Z 13); TF: trnsloction fctor (rtio of rsenic in fronds to tht in roots); BF: bioccumultion fctor (rtio of rsenic in fronds to tht in soils). to the As concentrtion in the roots) were 2.2 t ZMD nd 1.8 t LMC. The verge bioccumultion fctors (the rtio of the As concentrtion in the fronds to the As concentrtion in the soils) were 0.9 t ZMD nd 2.5 t LMC (Fig. 1). Although the As concentrtions, ph vlues nd CEC of the soils nd plnt biomsses (we found the verge height of P. vittt to be 90 cm t ZMD versus only 30 cm t LMC) were significntly different between the two sites, no differences were observed in the As concentrtions in the fronds nd roots or the trnsloction fctors (Fig. 1). This suggests tht P. vittt hs fixed As-ccumultion pttern nd tht the trnsloction fctors re physiologiclly controlled; thus, the As concentrtions nd properties of the soils hve little effect on As ccumultion. This is consistent with the results of Cille et l. (2004), who reported similr As-ccumultion ptterns in P. vittt bsed on pot experiments with five different As-contminted soils. However, the current study reveled significnt sttisticl differences in bioccumultion fctors between the two sites (Fig. 1), suggesting tht the As-ccumultion cpcity cn be influenced by soil properties. Previous pot experiments hve often reported bioccumultion fctors greter thn 10 for P. vittt. However, under field conditions, the ging of As is expected to mke it more stble nd less-esily tken up by plnts, leding to much lower bioccumultion fctors. Despite the fct tht the As concentrtions t the two sites were high, we found reltively low biovilble As concentrtions ( M N 2 HCO 3 extrction), with verge vlues of 10.4 nd 15.0 mg kg ÿ1 t ZMD nd LMC, respectively (dt not shown). Only the biovilble As in the soil cn be tken up by plnts; therefore, we reclculted the verge bioccumultion fctors, bsed on the biovilble As vlues, s 103 nd 141 t ZMD nd LMC, respectively (dt not shown). These higher vlues were consistent with the results of previous pot experiments Accumultion of other elements by P. vittt Our dt did not show the hyperccumultion of other elements by P. vittt, indicting tht the plnts selectively tke Fig. 2. The concentrtion of multi-elements in the fronds of Pteris vittt t the two sites. Brs with the sme letter re not significntly different (P! 5). ZMD: Zimudng (n Z 14); LMC: Lnmuchng (n Z 13). up certin elements. These results confirmed those of previous pot experimentl studies employing both metl slt tretments nd nturl multiple hevy metl-contminted soils (Cille et l., 2004; Fyig et l., 2004; Tu nd M, 2005). No differences were observed in the concentrtions of C, Cu, K, Mg, Mn, S nd Zn in the fronds nd roots of P. vittt between the two sites. However, the concentrtions of Fe, N nd P in the fronds of P. vittt were significntly different between the two sites (Fig. 2). P. vittt showed lower P nd higher Fe concentrtions in the fronds t ZMD compred to those t LMC (Fig. 2), lthough this did not explin the overll lrger biomss of P. vittt t the former site. The lower biomss t LMC might hve been cused by the low soil ph, s P. vittt usully prefers lkline conditions. We lso found tht the As hyperccumultors P. vittt nd P. cretic hd fr greter Fe concentrtions thn other plnts (unpublished dt). Fitz et l. (2003) discovered significntly higher level of Fe in soil solutions round the roots of P. vittt in rhizosphere experimentl study using rhizobox, which suggested tht the roots of this fern were ble to dissolve soil grins/minerls. However, no correltion ws found between the Fe nd As concentrtions in P. vittt in this study, contrry to previous findings in other As-tolernt plnts (Poter nd Peterson, 1975). At LMC, higher levels of P in the soil corresponded to incresed concentrtions of P in the fronds, while higher Fe levels in the soil were ssocited with lower Fe concentrtions in the fronds (Tble 1, Fig. 2). This reflected the different influences of soil properties on the uptke of these two elements Correltion between rsenic nd mjor nutrient elements The correltion nlysis found significnt positive reltionship between As nd K, N nd P, but negtive reltionship between As nd C, in the fronds of P. vittt t ZMD. No significnt reltionship ws found between As nd the other elements tested t this site (Tble 2). The results from ZMD lso suggested tht P, K nd N might enhnce positive correltion, wheres C ppered to inhibit negtive correltion, As ccumultion. These findings were in greement with previous pot experimentl results (Co et l., 2004;

4 C.Y. Wei et l. / Environmentl Pollution 141 (2006) 488e Tble 2 Elementl correltion mtrix for () ZMD nd (b) LMC As C Cu Fe K Mg Mn N P S Zn () ZMD As 00 C ÿ0.601* 00 Cu ÿ Fe ÿ K 0.660** ÿ0.111 ÿ Mg 36 74* ÿ0.262 ÿ Mn ÿ ÿ ** ÿ0.191 ÿ N 50* ÿ ÿ ÿ P 0.790** ÿ0.298 ÿ ** ÿ S ÿ * Zn ÿ ** ÿ0.100 ÿ ** ÿ (b) LMC As 00 C Cu 56 ÿ Fe ÿ ÿ0.707** 00 K ÿ Mg ÿ ÿ ÿ Mn ÿ ÿ ÿ ** 00 N ÿ0.272 ÿ ** P ÿ ÿ0.618** ÿ0.618** ÿ94 00 S 18 ÿ26 39 ÿ * ÿ0.617* 00 Zn ÿ ÿ0.117 ÿ ÿ ZMD: Zimudng (n Z 14), LMC: Lnmuchng (n Z 13). Correltion is significnt t the *P! 5 level, **P! 1 level. Correltion ws mde bsed on every nlytic result of smples. Lio et l., 2003), prticulrly the recent dt reported by Tu nd M (2005). In ddition, our results confirmed the results described in Section 3.3 (bove), in which only the Fe, N nd P concentrtions showed differences in P. vittt. Both sets of results suggest tht As-ccumultion by P. vittt is closely ssocited with these three elements; K nd N probbly ct s counterblncing ions, while phosphte is chemicl nlogue of rsente. However, no such reltionship Tble 3 Principl component nlysis for () ZMD nd (b) LMC Component Initil eigenvlues Extrction sums of squred loding Rottion sums of squred lodings Totl % of Vrince Cumultive % Totl % of Vrince Cumultive % Totl % of Vrince Cumultive % () ZMD (b) LMC ZMD: Zimudng (n Z 14), LMC: Lnmuchng (n Z 13).

5 492 C.Y. Wei et l. / Environmentl Pollution 141 (2006) 488e493 Tble 4 Rotted component mtrices for () ZMD nd (b) LMC () ZMD Element Component As ÿ0.104 ÿ0.153 C ÿ0.346 ÿ Cu ÿ82 95 Fe ÿ K ÿ79 Mg ÿ Mn ÿ N ÿ P ÿ0.349 Zn ÿ (b) LMC Elements Component As 07 ÿ06 ÿ ÿ0.154 C ÿ ÿ Cu ÿ0.122 ÿ ÿ87 Fe ÿ0.101 ÿ80 ÿ89 ÿ0.179 ÿ81 K ÿ Mg ÿ0.229 ÿ Mn ÿ38 ÿ N ÿ0.183 P ÿ ÿ0.291 S Zn ZMD: Zimudng (n Z 14), LMC: Lnmuchng (n Z 13). ws observed in the fronds t LMC (Tble 2b). In ddition, no significnt correltion between As nd nutrient elements ws found in the roots of P. vittt t both sites (dt not shown). This implies tht the fronds nd roots show differences in As nd nutrient ccumultion. Phosphte cts s n ntgonist to rsente nd consequently suppresses As uptke in some Astolernt plnts (Mehrg et l., 1994). However, pot experiments hve shown tht phosphte cn enhnce both the plnt biomss nd the As concentrtion in the fronds of P. vittt (Chen et l., 2002b). The results of our field study showed tht P. vittt did not decrese the P uptke when it ccumulted certin degree of As from the soil, indicting tht P fertilizer could hve beneficil effects on the As-phytoremedition efficiency in the field. The lck of correltion between As nd nutrient elements t LMC, s seen t ZMD, might be due to the greter P concentrtion in the soils, s P co-precipitted with severl elements in the rhizosphere, which could hve disturbed the norml blnce of elementl uptke. Principle component nlysis ws crried out in order to investigte the possible reltionship between As nd vrious elements during its uptke nd ccumultion by P. vittt. Different results were obtined for the two sites: 91% of the vrince could be explined t ZMD when O1 eigenvlues were considered (Tble 3), while 86% of the vrince could be explined t LMC when O0.8 eigenvlues were considered (Tble 3b). Component 2 Component 2 ZMD LMC The rotted component mtrix indicted tht the first fctor, including As, K, N nd P, explined 29% of the totl vrince t ZMD, which highlights the importnce of these elements (Tbles 3, 4). By contrst, t LMC, S ppered in the first fctor with high loding of nd explined 20% of the vrince, wheres As nd K only ppered in the fourth fctor nd explined just w16% of the vrince (Tbles 3b, 4b). The reson for S plying the most importnt role t LMC, while K nd P were less relevnt, is not cler from the present study. However, when PCA component plots were produced using the dt from the two sites, the results were similr, with As, P nd K forming one group of fctor lodings (Fig. 3). This further confirmed the importnce of P nd K for the uptke nd ccumultion of As by P. vittt. These findings suggest tht P, K nd C might ll influence the uptke nd ccumultion of As by this fern. 4. Conclusion As P Component1 Component1 Zn K Mg Mn Zn S Cu Fe N Fe Mn In summry, our field study showed tht P. vittt hd consistent As-hyperccumultion properties. Vrition in the soil properties hd little influence on the As-trnsloction fctors in P. vittt. The ph, CEC, nd P, K nd Fe levels in the soil were ll importnt fctors in determining the As-phytoremedition efficiency in the field. N Cu C Mg C Component 3 K As P Component 3 Fig. 3. Component plot lodings for rsenic nd nutrient elements in the fronds of Pteris vittt. ZMD: Zimudng (n Z 14); LMC: Lnmuchng (n Z 13).

6 C.Y. Wei et l. / Environmentl Pollution 141 (2006) 488e Acknowledgments This study ws finncilly supported by the Ntionl Science Foundtion of Chin (Grnt No , ), nd the Renovtion Project of the Institute of Geogrphicl Sciences nd Nturl Resources Reserch, Chinese Acdemy of Sciences (Grnt No. CXIOG-C04-02). The uthors express thnks to Mr. C. D. Sun for his kind help with the field smpling. We lso thnk the two nonymous reviewers for their insightful comments on this pper. References Co, X.D., M, L.Q., Shirlipour, A., Effects of compost nd phosphte mendments on rsenic mobility in soils nd rsenic uptke by the hyperccumultor, Pteris vittt L. Environmentl Pollution 126, 157e167. Co, X.D., M, L.Q., Tu, C., Antioxidtive responses to rsenic in the rsenic-hyperccumultor Chinese brke fern (Pteris vittt L.). Environmentl Pollution 128, 317e325. Chen, T.B., Wei, C.Y., Hung, Z.C., Hung, Q.F., Lu, Q.G., Arsenic hyperccumultor Pteris vittt L. nd its rsenic ccumultion. Chinese Science Bulletin 47, 902e905. Chen, T.B., Fn, Z.L., Lei, M., Hung, Z.C., Wei, C.Y., 2002b. Effect of phosphorus on rsenic ccumultion in As-hyperccumultor Pteris vittt L. nd its impliction. Chinese Science Bulletin 47, 1876e1878. Cille, N., Swnwick, S., Zho, F.J., McGrth, S.P., Arsenic hyperccumultion by Pteris vittt from rsenic contminted soils nd the effect of liming nd phosphte fertilistion. Environmentl Pollution 132, 113e120. Fitz, W.J., Wenzel, W.W., Zhng, H., Nurmi, J., Stipek, K., Fischerov, Z., Schweiger, P., Kollensperger, G., M, L.Q., Stingeder, G., Rhizosphere chrcteristics of the rsenic hyperccumultor Pteris vittt L. nd monitoring of phytoremovl efficiency. Environmentl Science nd Technology 37, 5008e5014. Fyig, A.O., M, L.Q., Co, X.D., Rthinsbpthi, B., Effects of hevy metls on growth nd rsenic ccumultion in the rsenic hyperccumultor Pteris vittt L. Environmentl Pollution 132, 289e296. Frncesconi, K., Visoottiviseth, P., Sridokchn, W., Goessler, W., Arsenic species in n rsenic hyperccumulting fern, Pityrogrmm clomelnos: potentil phytoremeditor of rsenic-contminted soils. The Science of Totl Environment 284, 27e35. Lio, X.Y., Xio, X.Y., Chen, T.B., Effects of C nd As ddition on As, P nd C uptke by hyperccumultor Pteris vittt L. under snd culture. Act Ecologic Sinic 23, 2057e2065 (in Chinese with English bstrct). M, L.Q., Kenneth, M.K., Tu, C., Zhng, W.H., Ci, Y., Kennelley, E.D., A fern tht hyperccumulting rsenic. Nture 409, 579. Mehrg, A.A., Nylor, J., Mcnir, M.R., Phosphorus nutrition of rsente-tolernt nd non-tolernt phenotypes of velvet grss. Journl of Environmentl Qulity 23, 234e238. Mehrg, A.A., Vrition in rsenic ccumultionehyperccumultion in ferns nd their llies. New Phytologist 157, 25e31. Nelson, D.W., Sommers, L.E., Totl crbon, orgnic crbon, nd orgnic mtter. In: Pge, A.L., Miller, R.H., Keeney, D.R. (Eds.), Methods of Soil Anlysis, Prt 2. Americn Society of Agronomy, Mdison, Wisconsin, pp. 539e579. O Neill, P., Arsenic. In: Allowy, B.J. (Ed.), Hevy Metls in Soils. Blckie Acdemic nd Professionl, pp. 105e121. Poter, P.K., Peterson, P.J., As ccumultion by plnts on mine wstes (United Kingdom). The Science of Totl Environment 4, 365e371. Rhodes, J.D., Ction exchnge cpcity. In: Pge, A.L., Miller, R.H., Keeney, D.R. (Eds.), Methods of Soil Anlysis, Prt 2. Americn Society of Agronomy, Mdison, Wisconsin, pp. 149e158. Tu, C., M, L.Q., Bondd, B., Arsenic ccumultion in the hyperccumultor Chinese brke nd its utiliztion potentil for phytoremedition. Journl of Environmentl Qulity 31, 1671e1675. Tu, C., M, L.Q., Effects of rsenic concentrtions nd forms on rsenic uptke by the hyperccumultor ldder brke. Journl of Environmentl Qulity 31, 641e647. Tu, C., M, L.Q., Effects of rsente nd phosphte on their ccumultion by n rsenic-hyperccumultor Pteris vittt L. Plnt nd Soil 249, 373e382. Tu, C., M, L.Q., Effects of rsenic on concentrtion nd distribution of nutrients in the fronds of the rsenic hyperccumultor Pteris vittt L. Environmentl Pollution 135, 333e340. Visoottiviseth, P., Frncesconi, K., Sridokchn, W., The potentil of Thi indigenous plnt species for the phytoremedition of rsenic contminted lnd. Environmentl Pollution 118, 453e461. Wei, C.Y., Chen, T.B., Hung, Z.C., Zhng, X.Q., Cretn brke e n rsenic-ccumulting plnt. Act Ecologic Sinic 22, 776e778 (in Chinese with English bstrct). Zho, F.J., Duhm, S.J., McGrth, S.P., Arsenic hyperccumultion by different fern species. New Phytologist 156, 27e31.