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Assessment of Bioaccumulation of Heavy Metal by Pteris Vittata L. Growing in the Vicinity of Fly Ash a

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Alka Kumari , Brij Lal , Yogesh B. Pakade & Piar Chand

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Biodiversity Division, Institute of Himalayan Bioresource Technology, Council of Scientific and Industrial Research, Palampur, Himachal Pradesh, India b

Hill Area Tea Science Division, Institute of Himalayan Bioresource Technology, Council of Scientific and Industrial Research, Palampur, Himachal Pradesh, India Available online: 01 Jun 2011

To cite this article: Alka Kumari, Brij Lal, Yogesh B. Pakade & Piar Chand (2011): Assessment of Bioaccumulation of Heavy Metal by Pteris Vittata L. Growing in the Vicinity of Fly Ash, International Journal of Phytoremediation, 13:8, 779-787 To link to this article: http://dx.doi.org/10.1080/15226514.2010.525561

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International Journal of Phytoremediation, 13:779–787, 2011 C Taylor & Francis Group, LLC Copyright  ISSN: 1522-6514 print / 1549-7879 online DOI: 10.1080/15226514.2010.525561

ASSESSMENT OF BIOACCUMULATION OF HEAVY METAL BY PTERIS VITTATA L. GROWING IN THE VICINITY OF FLY ASH Alka Kumari,1 Brij Lal,1 Yogesh B. Pakade,2 and Piar Chand2 1

Biodiversity Division, Institute of Himalayan Bioresource Technology, Council of Scientific and Industrial Research, Palampur, Himachal Pradesh, India 2 Hill Area Tea Science Division, Institute of Himalayan Bioresource Technology, Council of Scientific and Industrial Research, Palampur, Himachal Pradesh, India Pteris vittata L. subsp. vittata, a potential arsenic hyperaccumulator fern, growing naturally in the vicinity of fly ash was analyzed for the concentration of nine heavy metals (Fe, Cu, Zn Ni, Al, Cr, Pb, Si, and As) from five different sites around of Kanti Thermal Power Station at Muzaffarpur in Bihar State, India. Metal accumulation in P. vittata was correlated with the level of pollution at five selected sampling sites. The results revealed significantly more accumulation of these metals in the above ground parts of the plant than the parts below ground. Statistical parameters such as the coefficient of variation (CV%) showed a higher for As, Cu, Cr, and a lower one for Fe, Ni, Al. There was high spatial variability in the total metal concentration at different sites. The present study confirmed that P. vittata is a heavy metals accumulator and that it is a highly suitable candidate for phytoremediation of metal contaminated wastelands. KEY WORDS: bioaccumulation, fern, fly ash, heavy metal, pollution, P. vittata L. subsp. vittata

INTRODUCTION The majority of power generating stations in India are coal based (Khan and Khan 1996) which produces around 90 million tons of fly ash per annum during 1995 and it is likely to exceed 140 million tons per annum by 2020 (Kalra et al. 1998). Its disposal is therefore a major challenge. Deposits of dumped fly ash may cover large area of fertile land and the residue contaminates the water (surface and ground), soil, and vegetation. Although fly ash is being used in India in various construction activities including land filling, manufacturing of cement, and quarry restoration, a large portion of the ash remains left over and must be utilized in an environmentally friendly way. The only cost-effective and eco-friendly solution suggested so far for managements of fly ash is revegetation of landfill areas by fly ash tolerant plants, which serves the purposes of both stabilization and

Address correspondence to Alka Kumari, Biodiversity Division, Institute of Himalayan Bioresource Technology, Council of Scientific and Industrial Research, Palampur 176061, Himachal Pradesh, India. E-mail: [email protected] 779

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providing a pleasant landscape (Adriano et al. 1980; Wong and Wong 1990; Vajpayee et al. 2000; Rai et al. 2004). In addition, a small amount of fly ash is used for neutralization of acidic soil for growing agricultural crops, depending on the initial pH of the soil (Moliner and Street 1982). It also increases the availability of other essential elements such as sodium, potassium, calcium, magnesium, boron, and sulphates but not nitrogen (Elseewi et al. 1980; Wong and Wong 1990). Utilization of fly ash to improve agriculture productivity would not only be a solution to the problem but might also decrease the use of inorganic non-nitrogenous fertilizers. Unfortunately, in addition to essential elements, fly ash contains several noxious metals and metalloids such as, Hg, Al, Cd, Pb, Cr, and As (Mehra et al. 1998). These toxic heavy metals are a serious health hazard and are known to cause renal failure, major symptoms of chronic toxicity, and liver damage (Andrew et al. 2003; Shaw et al. 1997). The dust of fly ash also possesses a similar health hazard and has a potential impact on the visibility in nearby sites, as well as contributing to the deterioration of surface and ground water quality (Wu 1996). Thus an immediate and technologically affordable solution is required for disposal of fly ash generated from thermal power plants. Phytoremediation is one of the cost-effective technologies that utilizes plants to remove, transform, or stabilize contaminants, including organic pollutants and toxic metals in water, sediments, or soil (Cherian and Oliveira 2005). Over 400 plant species have been identified as natural metal hyperaccumulators (Brooks 1998; Reeves and Baker 2000). For example, Alyssum murale, Thlaspi rotundifolium, Pteris vittata, and Sesbania drummondii are known for their ability to hyperaccumulate Ni, Zn, As, and Pb, respectively (Ma et al. 2001a, b; Rasico 1977; Sahi et al. 2002; Severne and Brooks 1972). Plant species belonging to the family Leguminoceae has been found successful in revegetate fly ash landfills (Gupta et al. 2007; Rai et al. 2004). Various inorganic and organic blending of fly ash and inoculation of N2 –fixing microbes (Blue Green Algae) have been found useful in enhancing growth of the plants. Most of the literature concerning metallophytes is related to angiosperms but some reports on ferns are also available. Ferns are ancient non-flowering vascular plants, which appeared in the fossil record around 400 million years ago (Kendrick and Crane 1997). Ferns represent the highest evolutionary stage of vascular plants and occupy a middle branch of vascular plants evolutionary tree. Despite, over million years of evolution they still maintain an independent haploid gametophytic generation evolved by their distinct ancestors and hence they are evolutionarily quite distinct (Raven et al. 1992). Some ferns are used as metallophytes. For instance, Asplenium adulterium is an indicator of nickel (Vogt 1942), while Pellaea calomelanus and Chelianthes hirta were found on copper and occasionally nickel soils (Wild 1968). The fern Asplenium septentrionale (L.) Hoffm. deserves metallophytes status as it was found in old lead and copper mines in north and central Wales (Page 1988). Ferns are also recorded on serpentine soils high in nickel and chromium (Kruckerberg 1964). For instance, some ferns are apparently true endemics at the species level; others are morphological and ecological variants of species possessing broader tolerance (Kruckeberg 1964). Apart from terrestrial ferns, some aquatic ferns (such as Azolla filiculoides) also accumulate large concentrations of heavy metals in its shoots (Sela et al. 1989). Other ferns with metal accumulating capabilities include Salvinia natans for copper (Sen and Mondal 1990), S. molesta, Azolla pinnata, and Marsilea minuta for cadmium (Gupta and Devi 1995), and S. minima for chromium (Nichols et al. 2000). Other than heavy metals, ferns have also been known to accumulate large quantities of trace elements in their tissues (Ozaki et al. 2000). Besides, arsenic hyperaccumulation has been

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reported in Brake fern Pteris vittata (Ma et al. 2001a, 2001b; Mehrag 2002). P. vittata are mainly distributed in tropical and semi-tropical regions (Chen et al. 2005). During survey of fern and fern allies of Indo-Nepal border it has been observed that fly ash deposition from the thermal power stations over time has reduced the soil fertility of adjoining area and consequently local farmers were facing the problem of diminishing crop returns. Interestingly, Pteris vittata L. a common fern species was growing abundantly in the vicinity of fly ash without showing any visual toxicity symptoms. Hence, it was worthwhile to screen Pteris vittata L. growing in the area for metallophytes and their phytoremediation potential. The present study was undertaken with an objective to determine the degree of heavy metal accumulation in Pteris vittata L., which has already been reported as potential hyperaccumulator for arsenic.

MATERIALS AND METHODS Reagents All the metal standard solutions were purchased from Merck (Germany). The water (18M cm) was obtained from Millipore (Direct Q3 ) system. The chemical used for digestion and analysis such as nitric acid (HNO3 ), perchloric acid (HClO4 ) were from Merck, Mumbai, (India) and HCl was from Ranbaxy, India. The standard solutions of individual metal were prepared by appropriate dilution of stock solution (1000 mgL−1). Filter papers were obtained from Qualigens (0.45µm), 615A, Germany.

Study Area The study area is located in the district of Muzaffarpur, Bihar, India which is situated in northern part of Indian sub continent. The city stands between 25◦ 27 –26◦ 13 N latitude and 85◦ 27’–86◦ 10’ E longitude having Gangetic plain topography with fertile arable soil. However, contamination of fly ash retards the fertility of soil and crop production in the area. Sampling sites were selected on the basis of the level of fly ash deposition (Table 1). The schematic diagram of sampling site is shown in Figure 1.

Table 1 Distribution of P. vittata L. in fly ash polluted sampling sites S. No. 1.

2. 3. 4. 5.

Site description Back side of campus (Site 1)

Pollution level a/c to fly ash depth

Fly ash deposited during processing, between campus and railway line Depth of fly ash—3.5 feet Middle of campus (Site 2) (Moderately polluted) Depth of fly ash—3-4 feet Fly ash Dumping (Site 3) (Highly polluted) Depth of fly ash—More than 5 feet Kusi village (Site 4) (Low pollution) Depth of fly ash— 2 feet Nearby residential campus (Very low pollution) Depth of fly (Site 5) ash—1 feet

Fern ditribution Average vegetation of Pteris vittata L. Average rich vegetation of Pteris vittata L. Rich vegetation of Pteris vittata L. Poor vegetation of Pteris vittata L. Very poor vegetation of Pteris vittata L.

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Figure 1 Schematic diagram of selected sampling site.

Plant Culture The fern species P. vittata was collected from five different sites of Kanti Thermal Power Station (KTPS) and its diversity was observed according to pollution levels at the five sites (Table 1). Collected plants were washed thoroughly with deionised water until complete removal of fly ash particles. The ferns were separated into two portions, i.e., above ground (fronds) and below ground (roots including rhizomes) and oven dried at 80◦ C for 24 h. Dried fern samples were grounded and stored at room temperature for further digestion. The digestion was carried out with 0.1 g of sample in glass digestion tube of 250 mL along with mixture of concentrated nitric acid (HNO3 ) and perchloric acid (HClO4 ) (V/V 3:1). The solution was evaporated to dryness. After digestion the solution was cooled, filtered and made up to 50 mL with distilled water for heavy metal analysis. The heavy metals measurement in foliar and root samples was performed with Flame Atomic Absorption Spectrophotometer (Perkin Elmer, Model A Analyst 300 and Shimadzu AA6300 with HVG).

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Table 2 Heavy metal accumulation in above ground parts by Pteris vittata L. at different sites

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Sites Site 3 Site 2 Site 1 Site 4 Site 5 CD 5% CD 1% f probab. f values CV%

Iron 917 ± 39.9 887 ± 41.6 781 ± 50.8 657 ± 61.5 348 ± 29.7 38.75 56.32 0.000 382.96∗ 2.95

∗ Significantly different

Copper

Zinc

Nickel

Aluminium Chromium

49 ± 2.6 145 ± 5.8 141 ± 6.5 149 ± 7.7 47 ± 29.5 47 ± 29.5 87 ± 4.1 147 ± 8.5 47 ± 17.7 102 ± 3.5 69 ± 2.1 85 ± 2.3 38 ± 13.3 97 ± 9.8 49 ± 5.5 61 ± 1.35 34 ± 11.7 49 ± 7.9 45 ± 9.9 49 ± 4.4 NS 11.94 5.0346 14.32 NS 17.39 7.35 20.85 0.000 0.000 0.000 0.000 3.35 119.54∗ 624.25∗ 74.08∗ 12.66 6. 82 3.65 6.85

Lead

Silicon

Arsenic

117 ± 9.7 133 ± 4.6 138 ± 11.3 264 ± 18 95 ± 2.9 93 ± 3.2 127 ± 9.2 211 ± 6.5 79 ± 1.5 109 ± 11.5 102 ± 13.6 174 ± 7.0 65 ± 5.4 97 ± 26.6 89 ± 23.5 163 ± 12.2 43 ± 4.5 58 ± 2.4 65 ± 3.9 107 ± 5.5 17.98 9.18 20.65 7.7 26.16 13.36 30.07 11.30 0.000 0.000 0.000 0.000 26.85∗ 152.25∗ 24.75∗ 71.67 12.38 5. 81 10.35 29.73

at 1% level.

NS = Not Significant.

RESULTS AND DISCUSSION Fly ash is an only industrial pollution source in Kanti block of Muzaffarpur city. The fly ash generated from thermal power plant is dispersed from dumping site to nearby area through wind. Due to fly ash deposition the soil fertility of adjoining area has decreased and consequently retards the crop yield. Correlated with earlier studies on physico-chemical properties of fly ash (Kumari 2007), fly ash used in the experiment was alkaline in nature (pH 9.6) and had low total nitrogen and phosphorus content. The electrical conductivity of the fly ash was very high (8.0 mhos cm−1) indicating high ionic concentration. Organic carbon (1.13%), total nitrogen (0.02%), and phosphorus (0.14%) contents were very low in fly ash. The total moisture (water holding capacity) and humidity was 48.38% and 60–80%, respectively, which is an ideal condition for growth of fern species. Though levels of all the metals were very high: Al, Si, Fe, and Ni need special attention. Beside this, fly ash also contained micronutrients. Although fly ash contained several noxious metals and metalloids, ferns growing on fly ash showed no visual phytotoxic symptoms. Growth of fern plant and metal uptake by it, thus was influenced by soil physico-chemical properties (Singh et al. 2006; Xu et al. 2010). The recent study on the influence of pH and Ca concentration on germination of P. vittata revealed that higher pH and calcium concentration accelerated and increased the germination of P. vittata (Wan et al. 2010). Present study showed significant metal uptake at alkaline pH. (Tables 2 and 3). Table 3 Heavy metal accumulation in below ground part by P. vittata at different sites Sites

Iron

Copper

Zinc

Nickel

Aluminium Chromium

Lead

Silicon

Arsenic

Site 3 981 ± 24 35.7 ± 10 101 ± 21.5 123 ± 21 124 ± 20 93 ± 13.3 137 ± 13 126.6 ± 17 173 ± 4.7 Site 2 895 ± 17.5 33 ± 11.5 91 ± 19.5 108 ± 9.6 125 ± 13.5 89 ± 7.9 131 ± 7.8 103 ± 11.5 163 ± 6.0 Site 1 797.7 ± 13 31.5 ± 3.5 77.7 ± 16.9 88 ± 8 116.6 ± 23 81.7 ± 9.3 130 ± 18.5 85 ± 8.3 151 ± 11 Site 4 676 ± 15.5 27.7 ± 7.5 77 ± 17.7 86 ± 8.5 104 ± 11.3 78 ± 9.7 108 ± 13.4 77 ± 7.9 125 ± 8.9 Site 5 413 ± 13.5 28 ± 3.6 66 ± 15.66 72 ± 6.9 106 ± 9.8 66 ± 11.3 92 ± 8.7 74 ± 6.9 105 ± 12.5 CD 5% 21.39 NS 9.78 10.54 11.08 9.19 NS 12.54 5.11 CD 1% 31.13 NS 14.19 15.33 16.11 13.38 NS 18.24 7.43 f probab 0.000 0.000 0.000 0.000 0.000 0.0000 0.000 0.000 0.000 f values 411.89∗ 2.58 20.53∗ 37.62∗ 32.93∗ 12.07∗ 2.61 32.41∗ 38.44 CV% 5.644 11.243 6.262 5.847 4.922 5.963 9.152 7.14 18.89 ∗ Significantly different

NS = Not Significant.

at 1% level.

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The diversity of P. vittata growing in fly ash polluted sampling site for metals evaluation are depicted in Table 1. Pteris vittata has rich vegetation in fly ash dumping site (site 3) and campus of power plant (site 2). Poor vegetation of P. vittata was found in Kusi village (site 4) followed by residential site (site 5). The middle site of campus (site 1) showed moderate vegetation of target species (Figure 1).

Metal Concentration in Above Ground Part of Pteris vittata at Different Sites The comparative metal accumulations in above ground part of P. vittata at different sites are depicted in Table 2. The accumulation of most of the metals by P. vittata was higher at site 3 and site 2 followed by site 4 and site 5. The metal content in above ground part of P. vittata at different sites was significantly higher than residential site (site 5) which was treated as control site. The high metal content in most polluted sites, i.e., site 3 and 2 is due to high deposition of fly ash and rich bioavailability of metals. Among the metals analyzed, high level of iron was found in plants at all study sites, indicating that fly ash of Kanti Thermal Power Station has high value of iron. Copper and nickel concentration showed least variations among different sites, while other metals exhibited distinct variation. The toxic elements like chromium, arsenic, lead, copper, zinc, and aluminum showed high content in above ground part. It indicates that the accumulated metal content was translocated and deposited in the above ground part, mostly in leaf frond.

Metal Concentration in Below Ground Part of Pteris vittata at Different Sites Metal concentrations in below ground part of P. vittata at different sites are summarized in Table 3. The result reveals that accumulation of all metals was maximum in plants at sites 3 and 2 followed by sites 1, 4, and 5. It indicates that below ground parts of P. vittata had more iron content in comparison to above ground part. However, other elements like copper, zinc, nickel, and aluminium show lower accumulation in below ground part in comparison to above ground part. Toxic metals like chromium, lead and silicon exhibited similar accumulation pattern. Probably, it was due to translocation of metal contents from lower part to upper leaf parts. Earlier studies on phytoremediation through some ferns also indicated similar pattern of metal accumulation (Kumari 2007). In both conditions P. vittata accumulated higher concentration of metals in fronds (above ground part) as well as in roots (below ground part). The present study reveals that P. vittata accumulates Zn in both fronds and roots significantly. An et al. (2006) have also reported that P. vittata had a very high tolerance and grew at sites with high Zn concentrations and could effectively take up Zn into its fronds under field conditions. Several studies reported the suitability of this fern for phytoremediation of arsenic contaminated lands (Fayiga et al. 2004; Singh and Ma 2006; Singh et al. 2006). Suitability of a plant for phytoremediation can be determined by its ability to produce a high above ground biomass, high bioconcentration, and transfer factors (Fayiga et al. 2004). Pteris vittata fulfills all these characteristics and above data shows that it is not only hyperaccumulator of arsenic but also of mixed multi-metals. Therefore, it can survive even in vicinity of fly ash having high concentration of multi-metals. According to literature, the total arsenic concentrations, bioaccumulation and translocation factors in fronds showed that arsenic accumulation by

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P. vittata was different from site to site possibly due to the difference in soil properties at each site (Wei and Tong 2006; Singh et al. 2006; Natrajan et al. 2010). The calculation of the coefficient of variation (CV%) for element concentration in above ground part of P. vittata was higher for As, Cu, Cr, and Si, and lower for Fe, Ni, and Pb. Similarly, CV% for element concentration in below ground part of P. vittata (Table 3) was higher for As, Cu, Pb, and Si, and lower for Al, Ni, and Fe. It indicates the pattern of metal accumulation in above and below ground parts of P. vittata. It also indicates similar trend in element accumulation in both parts of P. vittata like higher for As, Cu, and Si and lower for Fe and Ni. Furthermore, the f values for different elements in above ground part was found higher for Ni, Fe, Pb followed by Zn, Al, As, Cr, Si, and Cu, but in below ground part (Table 3) it was maximum for Fe, followed by As, Ni, Al, Si, Cr, and Cu. Statistical analysis of data also highlights that all analyzed metals was significantly different at 1% (CD%) among different pollution level of selected sampling sites. Pteris vittata plays noteworthy role in reducing the toxicity of fly ash by accumulating mixed metals in its tissues with consequent detoxification responses without showing any toxicity symptoms. CONCLUSION The results of this study indicate that the application of single fern species can play an important role in amelioration of fly ash by significant decrease in metal content. The ameliorated fly ash can be amended in bare lands to revegetate it. Current findings present useful baseline data to search new hyperaccumulator ferns in the area, which can be used for fly ash management and rehabilitation of metal contaminated wastelands. Thus, a major problem of fly ash disposal can be addressed through phytoremediation by rapidly-growing fern could be the one way of removal of heavy metals in excess. It also provides the option to use this species in surface stabilization program, which reduce the potential of wind blown fallout already stated to be an issue locally. The present study suggested that P. vittata species is highly tolerant to mixed metals like Fe, Cu, Cr, Pb, Zn, Ni, Al, and Si and affirms that it is an efficient candidate for phytoremediation of multi metal contaminated wastelands. ACKNOWLEDGEMENTS The authors are thankful to the Directors, Institute of Himalayan Bioresource Technology, Palampur and National Botanical Research Institute (CSIR), Lucknow for providing laboratory facilities and encouragement. Thanks to Department of Science and Technology (DST), New Delhi for financial support under Fast Track scheme and Women Scientist scheme (SR/WOS-A/LS-117/2008). We are also thankful to Dr. R. D. Singh, IHBT for his help in statistical analysis. REFERENCES Adriano DC, Page AL, Elseewia A, Chang AC, Satrughes I. 1980. Utilization and disposal of fly ash and other coal residues in terrestrial. Ecosystems: A review. J Environs Qual. 9: 333–344. An ZZ, Huang ZC, Lei M, Liao XY, Zheng YM, Chen TB. 2006. Zn tolerance and accumulation in Pteris vittata L. and its potential to phytoremediation of Zn and As- contaminated soil. Chemosphere. 62: 796–802.

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