Arsenic accumulation in native plants of West Bengal, India: prospects for phytoremediation but...

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Environ Monit Assess (2012) 184:2617–2631 DOI 10.1007/s10661-011-2139-y Arsenic accumulation in native plants of West Bengal, India: prospects for phytoremediation but concerns with the use of medicinal plants Preeti Tripathi · Sanjay Dwivedi · Aradhana Mishra · Amit Kumar · Richa Dave · Sudhakar Srivastava · Mridul Kumar Shukla · Pankaj Kumar Srivastava · Debasis Chakrabarty · Prabodh Kumar Trivedi · Rudra Deo Tripathi Received: 8 September 2010 / Accepted: 25 May 2011 / Published online: 29 June 2011 © Springer Science+Business Media B.V. 2011 Abstract Arsenic (As) is a widespread environ- mental and food chain contaminant and class I, non-threshold carcinogen. Plants accumulate As due to ionic mimicry that is of importance as a measure of phytoremediation but of concern due to the use of plants in alternative medicine. The present study investigated As accumulation in native plants including some medicinal plants, from three districts [Chinsurah (Hoogly), Por- bosthali (Bardhman), and Birnagar (Nadia)] of Preeti Tripathi and Sanjay Dwivedi contributed equally to the results of this study. P. Tripathi · S. Dwivedi · A. Mishra · A. Kumar · R. Dave · M. K. Shukla · P. K. Srivastava · D. Chakrabarty · P. K. Trivedi · R. D. Tripathi National Botanical Research Institute, Council of Scientific and Industrial Research, Lucknow, 226 001, UP India S. Srivastava Nuclear Agriculture & Biotechnology Division, Bhabha Atomic Research Centre, Mumbai, 400085, Maharashtra India R. D. Tripathi (B ) Ecotoxicology & Bioremediation Group, National Botanical Research Institute (C.S.I.R.), Rana Pratap Marg, Lucknow, 226 001, India e-mail: [email protected] West Bengal, India, having a history of As pol- lution. A site-specific response was observed for Specific Arsenic Uptake (SAU; mg kg 1 dw) in total number of 13 (8 aquatic and 5 terrestrial) collected plants. SAU was higher in aquatic plants (5–60 mg kg 1 dw) than in terrestrial species (4–19 mg kg 1 dw). The level of As was lower in medicinal plants (MPs) than in non-medicinal plants, however it was still beyond the WHO per- missible limit (1 mg kg 1 dw). The concentration of other elements (Cu, Zn, Se, and Pb) was found to be within prescribed limits in medicinal plants (MP). Among the aquatic plants, Marsilea showed the highest SAU (avg. 45 mg kg 1 dw), however, transfer factor (TF) of As was the maximum in Centella asiatica (MP, avg. 1). Among the ter- restrial plants, the maximum SAU and TF were demonstrated by Alternanthera f icoidea (avg. 15) and Phyllanthus amarus (MP, avg. 1.27), respec- tively. In conclusion, the direct use of MP or their by products for humans should not be practiced without proper regulation. In other way, one fern species (Marsilea) and some aquatic plants (Eich- hornia crassipes and Cyperus dif formis) might be suitable candidates for As phytoremediation of paddy fields. Keywords Arsenic · Medicinal plants · Selenium · Specific Arsenic Uptake

Transcript of Arsenic accumulation in native plants of West Bengal, India: prospects for phytoremediation but...

Environ Monit Assess (2012) 184:2617–2631DOI 10.1007/s10661-011-2139-y

Arsenic accumulation in native plants of West Bengal,India: prospects for phytoremediation but concernswith the use of medicinal plants

Preeti Tripathi · Sanjay Dwivedi · Aradhana Mishra · Amit Kumar ·Richa Dave · Sudhakar Srivastava · Mridul Kumar Shukla ·Pankaj Kumar Srivastava · Debasis Chakrabarty · Prabodh Kumar Trivedi ·Rudra Deo Tripathi

Received: 8 September 2010 / Accepted: 25 May 2011 / Published online: 29 June 2011© Springer Science+Business Media B.V. 2011

Abstract Arsenic (As) is a widespread environ-mental and food chain contaminant and class I,non-threshold carcinogen. Plants accumulate Asdue to ionic mimicry that is of importance asa measure of phytoremediation but of concerndue to the use of plants in alternative medicine.The present study investigated As accumulationin native plants including some medicinal plants,from three districts [Chinsurah (Hoogly), Por-bosthali (Bardhman), and Birnagar (Nadia)] of

Preeti Tripathi and Sanjay Dwivedi contributedequally to the results of this study.

P. Tripathi · S. Dwivedi · A. Mishra · A. Kumar ·R. Dave · M. K. Shukla · P. K. Srivastava ·D. Chakrabarty · P. K. Trivedi · R. D. TripathiNational Botanical Research Institute,Council of Scientific and Industrial Research,Lucknow, 226 001, UP India

S. SrivastavaNuclear Agriculture & Biotechnology Division,Bhabha Atomic Research Centre, Mumbai, 400085,Maharashtra India

R. D. Tripathi (B)Ecotoxicology & Bioremediation Group,National Botanical Research Institute (C.S.I.R.),Rana Pratap Marg, Lucknow, 226 001, Indiae-mail: [email protected]

West Bengal, India, having a history of As pol-lution. A site-specific response was observed forSpecific Arsenic Uptake (SAU; mg kg−1 dw) intotal number of 13 (8 aquatic and 5 terrestrial)collected plants. SAU was higher in aquatic plants(5–60 mg kg−1 dw) than in terrestrial species(4–19 mg kg−1 dw). The level of As was lowerin medicinal plants (MPs) than in non-medicinalplants, however it was still beyond the WHO per-missible limit (1 mg kg−1 dw). The concentrationof other elements (Cu, Zn, Se, and Pb) was foundto be within prescribed limits in medicinal plants(MP). Among the aquatic plants, Marsilea showedthe highest SAU (avg. 45 mg kg−1 dw), however,transfer factor (TF) of As was the maximum inCentella asiatica (MP, avg. 1). Among the ter-restrial plants, the maximum SAU and TF weredemonstrated by Alternanthera f icoidea (avg. 15)and Phyllanthus amarus (MP, avg. 1.27), respec-tively. In conclusion, the direct use of MP or theirby products for humans should not be practicedwithout proper regulation. In other way, one fernspecies (Marsilea) and some aquatic plants (Eich-hornia crassipes and Cyperus dif formis) might besuitable candidates for As phytoremediation ofpaddy fields.

Keywords Arsenic · Medicinal plants ·Selenium · Specific Arsenic Uptake

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Introduction

Arsenic (As) is a metalloid present ubiquitouslyin trace amounts with a global average concen-tration of about 5 mg kg−1 dw in soils; how-ever, its contamination has emerged in past fewdecades due to enhanced entry into the environ-ment through natural and anthropogenic sources(Fitz and Wenzel 2002; Tripathi et al. 2007; Zhaoet al. 2010). Irrigation of agricultural soils with As-contaminated groundwater in Bangladesh, India,China, and other countries in South-East Asiahas caused the accumulation of As in both soilsand plants and elevated the transfer of As inthe food chain, which poses long term risks tohuman health (Williams et al. 2005; Tuli et al.2010). Therefore, the environmental fate and tox-icity of As to organisms has attracted increasingattention in recent years and a solution either inthe form of remediation or in a way of prevent-ing As entry into food/medicinal plants is beingsought for.

Technologies available for the remediation ofmetal/metalloid contaminated soils are soil exca-vation, electrokinetics, solidification, vitrification,chemical oxidation, soil flushing, bioremediation,phytoremediation, natural attenuation, and sur-factant foam technology (Wang and Mulligan2006; Dwivedi et al. 2008). Phytoremediation is asolar driven technology with low cost and hencemight be suitable for the cleaning up of the wide-spread As contamination of paddy fields (Hanet al. 2007). In this direction, discovery of variousAs hyperaccumulator ferns like Pteris vittata andPityrogramma calomelanos has been a major step(Ma et al. 2001; Francesconi et al. 2002; Srivastavaet al. 2005; Xie et al. 2009; Singh et al. 2010),however, ferns suffer from habitat restriction andthus cannot find wide-scale application (Tripathiet al. 2007). Hence, there is a need to screenmore plants to find the best suited option for aparticular area/for global use. These efforts haveled to the identification of a number of otherpotential As accumulator aquatic and terrestrialplants, such as Mimosa pudica, Melastoma mal-abrathricum, Portulaca tuberosa, P. oleracea, Hy-drilla verticillata, Eclipta alba and Limnanthes spp.(Visoottiviseth et al. 2002; Srivastava et al. 2007;

Tiwari et al. 2008; Dwivedi et al. 2008, 2010a).With this focus, the present study emphasizedon identifying native weed-like/non-commercialplants for the area of West Bengal, India, whichcan find some field application.

The ability of plants to accumulate both essen-tial and non-essential metals due to ionic mimicryand present day widespread As contaminationalso means that As accumulation may occur totoxic levels in economically important plants; tocite the worst case of its kind is the As accumu-lation in rice grains (Williams et al. 2005; Dwivediet al. 2010b). However, no study, to the best of ourknowledge, has concentrated on determining Asaccumulation in medicinally important and tradi-tionally used plants growing in the contaminatedarea. Medicinal plants (MPs) are considered to bean important source of natural products and tradi-tionally occupy an important position in the socio-cultural, spiritual and health arena of rural andtribal lives of India (Pala et al. 2010). In West Ben-gal, several MPs have been found to grow, such asCentella asiatica, Phyllanthus amarus, Polygonumspp., Vernonia cinerea, and Euphorbia hirta. In theIndian system of Ayurvedic medicine, C. asiaticahas been used for the cure of headache, bodyache, insanity, asthma, leprosy, ulcers, eczemas,and wound healing (Suguna et al. 1996; Shuklaet al. 1999). P. amarus is also one of the importantmedicinal plants, and has been reported to haveantibacterial (Macrae et al. 1988), antihepatotoxic(Thabrew and Hughes 1996), and antihepatitis Bvirus (Lee et al. 1996) effects. Some other plantslike Polygonum spp., V. cinerea, and E. hirtahave antibacterial and anti-inflammatory proper-ties (Vijaya et al. 1995; Iwalewa et al. 2003; Panet al. 2007). One of the major quality problemencountered with the direct usage of MPs is thepresence of high content of heavy metals (Gasseret al. 2009; Baye and Hymete 2010). Profilingof heavy metal accumulation in MPs in Nigeria,Pakistan, and Ghana has been documented(Obiajunwa et al. 2002; Khan et al. 2008; Annanet al. 2010) but there is no report on Asaccumulation in MPs growing naturally onAs-contaminated areas. Considering above back-ground information, an analysis of As accumula-tion in different parts of MPs seems worthwhile.

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Therefore, a field survey was conducted in Asaffected paddy fields during boro season, 2009 toassess As accumulation in native macrophytes fortheir prospective use as phytoremediators as wellas in MPs for determining the risk factor associ-ated with their consumption. The concentrationof other elements (Cu, Se, Zn, and Pb) were alsoanalyzed and being discussed in this paper.

Material and methods

Site survey and samples collection

A field survey was conducted in the As-contaminated paddy fields of West Bengalreceiving continuous loading of As throughgroundwater irrigation. Three sites were selectedfor the collection of samples and survey. Chin-surah, Hoogly (latitude 22◦53′ N, longitude 88◦24′E) was selected as site A. District Bardhaman(latitude 23◦15′0 N, longitude 87◦45′0 E) is situ-ated in the Gangetic alluvial zone and is known asthe “rice bowl of West Bengal”. It has 32 blocks,out of which only two blocks (Purbasthali-Iand Purbasthali-II) are As affected. The surveyedblock Purbasthali-I is severely As affected (siteB), where As level in groundwater ranges from0.5–135.9 μg l−1 (Nag et al. 1996), while Birnagarof district Nadia (latitude 22◦53′–24◦12′ N, longi-tude 88◦01′–88◦48′ E) was selected as site C. Thelevel of As in groundwater of site B and C wasaround >27 and > 52 μg l−1, respectively. Thesamples of plants and soils were collected frompaddy fields of the three selected sites and werebrought to the laboratory for identification andanalysis.

Plant collection and Identification

A total number of 13 plants belonging to differentfamilies were collected and kept in plastic bags.One set of healthy plants were kept in plantpress using standard herbarium method. Afterbringing to laboratory, plant species were iden-tified using the taxonomic keys given by Duthie(1960). Following aquatic plants: C. asiatica(MP, Mackinlayaceae), Polygonum spp. (MP,

Polygonaceae), Eichhornia crassipes (Pontederi-aceae), Colocasia formasa (Colocasceae), Cyperusdif formis (Cyperaceae), Limnophila sessilif lora(Plantginaceae), Typha latifolia (Typhaceae),Marsilea quadrifolia (Marsileaceae), and terres-trial plants: V. cinerea (MP, Asteraceae), E. hirta(MP, Euphorbiaceae), P. amarus (MP, Phyllan-thaceae), Jussiaea repens (Onagraceae), Alternan-thera f icoidea (Amaranthaceae) were identified.

Digestion and quantification of metals in plantsparts

In laboratory, plant samples were divided intoroots, shoots and leaves, washed thoroughly withdouble distilled water for removing the adheringsoil particles, blotted and oven dried at 80◦C for72 h. For analysis of metals (Cu, Zn, and Pb) andmetalloids (As and Se), 0.5 g oven dried tissue wastaken and digested in 3 ml of HNO3 as detailedpreviously (Dwivedi et al. 2010b). The metals andmetalloids (Cu, Zn, Pb, Se, and As) were quan-tified with the help of inductively coupled plasmamass spectrometer (ICP-MS, Agilent 7500 cx).

Soil analysis

Soil pH was analyzed by Orion ion meter (USA).Available nitrogen (%) and available phosphorus(%) were estimated by following the protocolgiven by Carter and Gregorich (2007), while to-tal organic carbon was analyzed by following themethod of Walkley and Black (1949). Water hold-ing capacity was measured hydrometrically. Forthe estimation of various metals/metalloids viz.Cu, Zn, Pb, Se, and As in soil, soils was ground tofine powder after drying at 80◦C and then passedthrough a sieve (<2 mm). Soil (0.2 g) was digestedin HNO3: HF (1:1) at 120◦C for 2 h and 140◦C for4 h (Lu et al. 2010), then filtered in 10 ml of MilliQ water and stored at 4◦C until estimation.

Specific metal uptake and transfer factor

Specific metal uptake indicates the ability of totalmetal accumulation in different plant parts of col-lected species and it was calculated according toZhang and Duan (2008) with slight modification

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as reported in Dwivedi et al. (2010b). Transfer fac-tor (TF) for As was calculated as per the followingformula: TF = shoot As concentration / root Asconcentration.

Quality control and quality assurance

The standard reference materials of metals(E-Merck, Germany) were used for the calibra-tion and quality assurance for each analyticalbatch. Analytical data quality of metals was en-sured with repeated analysis of quality controlsamples (n = 3) and the results were found within(±2.82) the certified values. Recovery of Cu, Zn,Se, and Pb from the plant tissue was found tobe more than 96.5% as determined by spikingsamples with a known amount of each metal. ForAs, rice flour NIST 1568a was used as a referencematerial with known spiked samples and recoveryof total As were 85.3% (±2.8; n = 5) and 89.5%(±3.1; n = 5) respectively. The detection limits forCu, Zn and Pb were 0.001, 0.005 and 0.06 mg l−1

respectively, while, for As and Se, were 1 μg l−1.

Statistical analysis

One-way analysis of variance (ANOVA) was per-formed with all data and Duncan’s multiple rangetest (DMRT) was done to evaluate significant

differences between As accumulation at three se-lected sites (Gomez and Gomez 1984).

Results and discussion

Physico-chemical properties of soil

The physico-chemical analysis of soils collectedfrom As affected paddy fields of West Bengal ispresented in Table 1. The pH of all three sites wasin the alkaline range with site B having the mostalkaline soil (pH 8.0). The level of available nitro-gen (0.38%) and water holding capacity (WHC)(81%) were lower at site B as compared to othertwo sites; however porosity (81.00) and total or-ganic carbon (1.67) were higher. Total As concen-tration varied significantly and was found to be themaximum at site C (15.54 mg kg−1 dw), however,other metals viz., Fe (48326 mg kg−1 dw), Zn(93.52 mg kg−1 dw), and Cu (44 mg kg−1 dw) werehigher at site A than the other sites. The variationin the soil As level may be due to differencesin the baseline soil As, the level of As in thegroundwater and the amount of irrigation in thearea (Lu et al. 2009). The mean As concentrationfrom agricultural lands in a previous study wasfound to be 6.21 mg kg−1 with a range of 3.34–11.3 mg kg−1, whereas a few soils had As in the

Table 1 Physico-chemical properties ofarsenic contaminatedsoils from three fieldlocations

All the values are meanof triplicates ±S.D.ANOVA significant atp ≤ 0.01. Different lettersindicate significantlydifferent values at aparticular treatment(DMRT, p ≤ 0.05)Site A Chinsurah; Site BPurbosthali; Site CBirnagar

Parameters Site A Site B Site C

pH 7.6a ± 1.08 8.00a ± 0.17 7.2a ± 0.26EC μs/cm 74.16b ± 6.98 116.56ab ± 28.02 137.73a ± 27.20Porosity (%) 77.69a ± 3.99 80.96a ± 6.69 76.02a ± 1.85TOC (%) 0.69c ± 0.01 1.67a ± 0.10 1.22b ± 0.13Available-Nitrogen (%) 0.54b ± 0.05 0.38c ± 0.02 0.67a ± 0.01WHC (%) 87.77a ± 1.89 80.63b ± 1.75 86.13a ± 2.36Metals (mg kg−1 dw)

Total As 10.43ab ± 1.53 12.59b ± 1.82 15.54a ± 1.32Fe 48326a ± 4899 17565b ± 5809 24436b ± 6930Zn 93.52a ± 16.49 61.88a ± 11.59 61.8a ± 22.66Mn 295.24a ± 38.89 357.32a ± 27.30 209.04b ± 40.13Cu 44.08a ± 3.99 14.4b ± 1.98 13.96b ± 2.19Available P (%) 848.58a ± 33.4 760.25a ± 86.7 581.22b ± 10.6Se 3.01b ± 0.101 2.33c ± 0.33 3.93a ± 0.393Mo 8.22a ± 0.24 6.18b ± 0.18 7.74a ± 0.54

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higher range of >11.5 mg kg−1 (Roychowdhuryet al. 2002). Comparing the previous studies, thelevel of As at site B and C was on the higherside.

Specific arsenic and lead uptake in medicinalplants

The accumulation of essential, non-essential met-als and metalloids in medicinal plants (used asherbal medicine) beyond the permissible limitis a matter of concern to public safety all overthe world (Annan et al. 2010). The problem be-comes rather more serious when plants growingon contaminated sites are used as raw materialswithout any consideration of presence of suchtoxic chemicals/metals and when there are no reg-ulatory guidelines to assure quality parameters.During the present study, a total number of 13naturally growing plants were collected from As-contaminated paddy fields. Out of these, 5 plantsare commonly used as MPs by local people forthe cure of various diseases. The names of theseMPs, their family and medicinal properties are

presented in Table 2. The range of As accumula-tion varied significantly in these MPs from site tosite with the maximum being in roots followed byshoots and leaves (Fig. 1). Arsenic accumulationin all five MP species was relatively higher at siteC than either at site B or site A; thus the level ofAs accumulation was significantly correlated withthe concentration of As in soil (Fig. 1). SpecificArsenic Uptake (SAU) for MPs like Polygonum,V. cinerea, E. hirta, P. amarus and C. asiatica was20, 18, 17, 17 and 12 mg kg−1 dw, respectively atsite C, whereas these values were 10, 8, 5, 10 and5, respectively at site B (Table 3). The maximumpermissible level of As for food/edible tissues is1 mg kg−1 dw (WHO 1989). In this study, how-ever, majority of the examined MPs had As con-tent higher than the maximum permissible limit.Thus, the accumulation of As in various parts ofmedicinal plants is of particular concern as As isa non-threshold, class 1 human carcinogen (Zhaoet al. 2010) and intake of such high level of Asthrough MPs could potentially lead to As toxicity.The concentration of Pb in the plant samples ispresented in Fig. 2. Though, all five MPs con-

Table 2 As accumulation in different parts of medicinal plants and their medicinal properties

Plants species Family Medicinal uses Parts used Range of As accumulation in plantsparts, at selected sites (mg kg−1 dw)

Root Shoot Leaves

Centella asiatica Mackinlayaceae Headache, body ache, Leaves 2.21–6.34 1.97–3.37 0.91–2.17insanity asthma, leprosy,ulcer, eczemas, woundhealing antitumor

Polygonum spp. Polygonaceae Atherosclerosis, scalds Leaves 5.22–9.72 2.98–6.66 1.31–4.08burns, laxation, adiuretic, skin diseases

Vernonia cinerea Asteraceae Malaria fever, worms, pain Leaf, seeds 4.33–9.27 2.00–4.89 1.34–3.96inflammation, infectionsdieresis cancer, abortionand gastro-intestinaldisorder, antimicrobial

Euphorbia hirta Euphorbiaceae Dysentery, antibacterial Root, Shoot, 2.00–8.62 2.00–4.99 0.99–3.64leaves

Phyllanthus amarus Phyllanthaceae Jaundice, antibacterial, Root, Shoot, 4.23–7.54 3.69–6.00 1.94–3.01Antihyperglycomic, leavesantihepatotoxic,antihepatitis B

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Fig. 1 Arsenic accumulation in different parts of aquaticand terrestrial plants collected from arsenic affected paddyfields; Chinsurah (a); Purbosthali (b); Birnagar (c). All

values are mean of triplicates ±S.D. ANOVA significantat p ≤ 0.01. Dif ferent letters indicate significantly differentvalues among the plant species (DMRT, p ≤ 0.05)

tained detectable levels of Pb, the concentrationdid not exceed the limit of 10 mg kg−1 dw specifiedby WHO (2005) except P. amarus at site B, where

it had SLU of 12 mg kg−1. In a previous studyby Caldas and Machado (2004) in Brazil, variousmedicinal plants analyzed, in general, had lower

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Table 3 Specific Arsenic Uptake (SAU) and specific leaduptake (SLU) in terrestrial and aquatic plants collectedfrom selected paddy fields of As affected areas

Plants species Site A Site B Site C

SAU SLU SAU SLU SAU SLU

Aquatic plantsC. asiaticaa 8.7 3.53 5.09 6.81 11.88 3.28Polygonum sp.a 13.68 5.2 9.51 7.46 20.46 5.91E. crassipes 40.84 1.34 6.39 3.79 50.25 1.46C. formossa 19.12 10.85 9.76 9.7 25.8 5.05C. dif formis 32.3 2.9 15.85 15.33 43.22 1.93L. sessilif lora 13.64 7.46 15.94 10 22.17 6.57T. latifolia 5.16 2.28 23.75 4.42 9.26 2.64Marsilea sp. 44.85 5.72 30.51 2.46 60.45 10.8

Terrestrial plantsV. cinereaa 11.5 4.97 7.67 3.9 18.12 3.9E. hirtaa 4.54 8.14 4.99 4.95 17.25 5.6P. amarusa 7.59 2.57 9.86 11.88 16.55 4.88J. repens 11.02 2.88 10.04 10.98 16.76 2.58A. f icoidea 14.92 2.71 10.4 3.83 18.84 2.84

aMedicinal Plants

Pb concentrations (<2 mg kg−1) except Aesculushippocastanum (having up to 1480 mg kg−1 Pb).Baye and Hymete (2010) also reported the highaccumulation of Pb in Allium sativam, Thymusserrulatus and Haggnia abyssinica plants collectedfrom four different industrial areas of Ethiopia.Although we analyzed four MPs with low Pb lev-els, presence of high Pb level in MP is also ofconcern as there might be other MPs present withhigh Pb levels at various other sites. Hence, MPsshould be properly tested for metal load beforeprocessing them for further use.

Arsenic remediation efficiency of native plants

Environmental cleanup of polluted land is anincreasingly important issue that we need toface. Compelling evidences have demonstratedthat phytoremediation is a promising technol-ogy for the cleanup of toxic metals such as Asin the environment (Xie et al. 2009). Out of13 plants species collected in the present study,8 species belonged to aquatic while 5 to ter-restrial plants. The Table 3 shows the SpecificArsenic Uptake (SAU) of aquatic and terrestrialplants. A site-specific response with great vari-ability among the aquatic and terrestrial plants

was observed for As accumulation. In general, theaccumulation of As was more in aquatic plantsthan in terrestrial species and the concentrationof As in all species showed the accumulationorder roots>shoot>leaves. The maximum SAUwas shown by Marsilea (31–60 mg kg−1 dw),followed by E. crassipes (6–50 mg kg−1 dw)and C. dif formis (16–43 mg kg−1 dw). Amongthe terrestrial plants, A. f icoidea showed maxi-mum SAU (10–19 mg kg−1 dw) at three selectedsites followed by J. repens (10–17 mg kg−1 dw).Similarly, Robinson et al. (2006) sampled 28species of aquatic macrophytes and 11 terres-trial species from Taupo Volcanic Zone, NewZealand and found clear demarcation betweenterrestrial plants, which accumulated negligibleconcentration of As, and aquatic species thathad As concentration many fold higher than theambient waters. It appears that accumulation ofAs from whole plant surface in contact of wa-ter leads to a higher SAU in aquatic plants ascompared to that of terrestrial plants, which ac-cumulate through roots only (Mishra et al. 2008).Site-specific response was also observed in bioac-cumulation coefficient (BC) and transfer factor(Table 4). In terms of BC as well, response ofaquatic plants like Marsilea (2.88–3.88), E. cras-sipes (0.60–3.28), C. dif formis (1.49–2.78) and L.sessilif lora (1.09–1.50) was comparatively betterthan that of terrestrial plants like A. f icoidea(0.98–1.21). For considering a plant suitable forphytoremediation, however, an important crite-rion is considered to be the TF, which shouldbe more than 1. Nevertheless, for aquatic plants,which normally easily float on water surface or areloosely bound to soil and thus can be uprooted/removed easily, the criterion of TF can be omitted.Furthermore many submersed and floating typesrepresent foliar uptake. In this sense, aquaticplants having good BC might appear suitable can-didates for the purpose of phytoremediation. Incase of terrestrial plants, which are firmly rooted,the important criterion becomes how much metalis transferred to shoots i.e. TF of >1 is a must.Considering this and that there were only twonon-medicinal terrestrial plants (J. repens and A.f icoidea), both of which have an average of TFof <1 and hence, cannot be considered suitablecandidates for phytoremediation efforts. In fact,

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ef

c

a

cd

ef

cde

cde

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ab

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ede

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cdcd

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dede

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cde

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bde a a

ef

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C. asia

tica*

Polygonum

sp. *

E. cra

ssip

es

C. form

ossa

C. diff

ormis

L. ses

silifl

ora

T. latif

olia

Marsil

ea

V. cin

erea

*

E. hirt

a*

P. am

arus*

J. re

pens

A. fico

idea

Plant Name

A

B

C

Fig. 2 Lead accumulation in different parts of aquaticand terrestrial plants collected from arsenic affected paddyfields; Chinsurah (a); Purbosthali (b); Birnagar (c). All

values are mean of triplicates ±S.D. ANOVA significantat p ≤ 0.01. Dif ferent letters indicate significantly differentvalues among the plant species (DMRT, p ≤ 0.05)

among terrestrial plants, P. amarus, a medicinalplant, had >1 TF and this fact becomes of moreconcern. There are various factors known to affect

As uptake in plant including As speciation, soilredox status, water and fertilizer management(Abedin et al. 2002; Williams et al. 2005), pres-

Environ Monit Assess (2012) 184:2617–2631 2625

Table 4 Bioaccumulation coefficient (B.C.) of arsenic andTransfer factor (T.F.) in aquatic and terrestrial plant col-lected from the arsenic affected paddy fields

Genus/species Site A Site B Site C

B.C. T.F. B.C. T.F. B.C. T.F.

Aquatic plantsC. asiaticaa 0.69 0.82 0.48 1.30 0.76 0.87Polygonum sp.a 1.10 0.81 0.89 0.82 1.31 1.10E. crassipes 3.28 0.75 0.60 0.29 3.23 0.52C. formossa 1.53 1.03 0.92 0.46 1.66 1.06C. dif formis 2.59 0.40 1.49 0.98 2.78 0.61L. Sessilif lora 1.09 0.55 1.50 0.85 1.42 0.70T. latifolia 0.41 1.08 2.24 0.40 0.59 0.63Marsilea 3.60 0.52 2.88 0.55 3.88 0.92

Terrestrial plantsV. cinereaa 0.92 0.69 0.72 0.77 1.16 0.95E. hirtaa 0.36 0.89 0.47 1.49 1.11 1.00P. amarusa 0.61 1.29 0.93 1.33 1.06 1.19J. repens 0.88 1.07 0.94 0.44 1.07 0.94A. f icoidea 1.20 0.94 0.98 0.69 1.21 0.83

aMedicinal plants

ence of iron, phosphate and silicon (Zhao et al.2010). These findings are agreement with Nortonet al. (2009) who concluded that environmentalfactors affect As accumulation in rice and site-specific response was observed in Bangladesh ricegenotypes. Nevertheless, Lu et al. (2009) con-cluded that baseline soil variation is a major factorin As accumulation. Once inside the plants, Astranslocation to the aboveground parts is furtherinfluenced by plants’ varying capacity to toler-ate metal infiltration due to differential poten-tial to synthesize As chelating peptides and tochelate/sequester As complexes/ions (Srivastavaand D’ Souza 2009; Indriolo et al. 2010). Dueto these various reasons, variations in plants’As accumulation are bound to occur and hencearises the need to screen native plants to suitfor different areas. This present study could notfind any suitable terrestrial plant but recommendssome aquatic plants that may find some applica-tion in As removal from paddy fields.

Accumulation of Cu, Zn, Se and Pb in plants

Aquatic and terrestrial plants were also processedand analyzed for the determination of Pb (Fig. 2)and other elements (Cu, Zn and Se, Figs. 3, 4, 5).

A site-specific response was also observed in up-take and translocation of these elements as well.Further, the accumulation of elements was sig-nificantly different among various plants (DMRT,p ≤ 0.05). In case of Cu content, trends fortotal accumulation, BC and TF were similarto that of As. Aquatic plants had higher totalCu accumulation (12–96 mg kg−1 dw) and BC(1.15–9.07) as compared to that of terrestrialplants (17–52 mg kg−1 dw total Cu accumulation;1.63–4.96 BC). Similarly, TFs were mostly <1in aquatic plants, while >1 in terrestrial plants.Considering total accumulation and BC, Marsilea(39–96 mg kg−1 dw total accumulation; 3.15–9.07BC) and Eichhornia (49–86 mg kg−1 dw totalaccumulation; 4.65–6.90 BC) performed better atall three sites among aquatic plants while takingTF as an important criterion, E. hirta (1.00–1.44)showed a better response among terrestrial plants(Fig. 3). Among MPs, C. asiatica (32–49 mg kg−1)

had higher total Cu accumulation between aquaticMPs, while V. cinerea (24–41 mg kg−1) amongterrestrial MPs. The range of Cu concentration inprevious report was found to be in the range of17.6–57.3 mg kg−1 in leaves (Reddy and Reddy1997). The accumulation of Zn was found to begenerally lower at site C in various plants thanthat at site A and B (Fig. 4). The average TFfor Zn was generally <1 except C. asiatica (1.15)and E. crassipes (1.03). Similarly, the average BCfor Zn also varied 4.7–7.5 for various plants. Theestimated safe and daily intake of Zn is between10 and 20 mg day−1 (NRC 1980). Among MPs,Polygonum (71–85 mg kg−1) and E. hirta (81–100)had a higher range of total Zn accumulation. Thetotal Zn accumulation (root, shoot and leaf) of119 mg kg−1 dw in L. sessilif lora was observed atsite B; still the Zn level per 10 g of plant specieswere not more than 1.12 mg kg−1 and hence werelower than the maximum permissible level. To-tal selenium content (Fig. 5) ranged from 0.532to 10 mg kg−1 dw with C. dif formis recordingthe highest amount at site B (10 mg kg−1). Theaverage TFs and BCs were <1 for all aquaticplants, however in case of terrestrial plants, TFwas >1 for V. cinerea, E. hirta, and J. repens. Themaximum permissible level of Se is 700 μg day−1

(Rayman 2000). The total Se content of MPsranged from 1.18 to 5.41 mg kg−1. Therefore,

2626 Environ Monit Assess (2012) 184:2617–2631

c

bc b

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Cu

(mg

kg-1

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)C

u (m

g kg

-1 d

w)

Cu

(mg

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dw

)Root Shoot Leaf

c

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tica

Polygonum sp

.

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ea

V. cin

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arus

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idea

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A

C

B

Fig. 3 Copper accumulation in different parts of aquaticand terrestrial plants collected from arsenic affected paddyfields; Chinsurah (a); Purbosthali (b); Birnagar (c). All

values are mean of triplicates ±S.D. ANOVA significantat p ≤ 0.01. Dif ferent letters indicate significantly differentvalues among the plant species (DMRT, p ≤ 0.05)

the average intake of about 10 g of plant ma-terial would give a maximum of around 55 μgSe. This implies that all five MPs contained very

low amount of Se. Kirk (2004) reported that un-der reduced conditions, Se is in soluble form be-cause of the thermodynamic stability of selenite

Environ Monit Assess (2012) 184:2617–2631 2627

a

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Fig. 4 Zinc accumulation in different parts of aquatic andterrestrial plants collected from arsenic affected paddyfields; Chinsurah (a); Purbosthali (b); Birnagar (c). All

values are mean of triplicates ±S.D. ANOVA significantat p ≤ 0.01. Dif ferent letters indicate significantly differentvalues among the plant species (DMRT, p ≤ 0.05)

(SeO2−3 ) and selenide (Se2−). Thus, flooded con-

dition (paddy habitat) appears to be an importantfactor for decreasing soil Se availability, which is

the source to for the medicinal plants (Dwivediet al. 2010b). Total Pb accumulation and TFsfor non-medicinal plants were in the lower range

2628 Environ Monit Assess (2012) 184:2617–2631

e

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Fig. 5 Selenium accumulation in different parts of aquaticand terrestrial plants collected from arsenic affected paddyfields; Chinsurah (a); Purbosthali (b); Birnagar (c). All

values are mean of triplicates ±S.D. ANOVA significantat p ≤ 0.01. Dif ferent letters indicate significantly differentvalues among the plant species (DMRT, p ≤ 0.05)

except for J. repens at site B, where it had total Pbaccumulation of 11 mg kg−1 with a TF of 1.35 andL. sessilif lora having more than 5 mg kg−1 total Pb

accumulation at all three sites. Recently, Baye andHymete (2010) reported Pb and Cd accumulationin plants grown in different parts of Ethiopia.

Environ Monit Assess (2012) 184:2617–2631 2629

Conclusion

In conclusion, the overall results indicated thatsignificant As accumulation was present in allplants including the MPs, which showed As levelbeyond the WHO permissible limit. However,other nutrients elements (Cu, Zn, and Se) and Pbwere found to be within the acceptable and safelimits in MPs. Thus, chronic intakes of As in MPsmay impart damaging effect on human beings andother animals, on the other hand As accumulationby aquatic macrophytes may make valuable toolsfor phytoremediation of As from paddy soil.

Acknowledgements This work was supported by Net-work Project (NWP-17) of Council of Scientific and In-dustrial Research, Govt. of India. SD is grateful to SERCDivision, Department of Science and Technology, NewDelhi, India for the award of Young Scientist.

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