Bioaccumulation and translocation of heavy metals in ...

Environmental Nanotechnology, Monitoring & Management 10 (2018) 272–279

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Environmental Nanotechnology, Monitoring & Management journal homepage: www.elsevier.com/locate/enmm

Bioaccumulation and translocation of heavy metals in mangrove rhizosphere sediments to tissues of Avicenia marina – A field study from tropical mangrove forest

T

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Ganeshkumar Arumugam, Rajaram Rajendran , Arun Ganesan, Rameshkumar Sethu Department of Marine Science, Bharathidasan University, Tiruchirappalli, 620 024, Tamil Nadu, India

A R T I C LE I N FO

A B S T R A C T

Keywords: Mangrove ecosystem Rhizosphere Bioaccumulation Translocation

Samples of rhizosphere sediment, plant tissues like branch, bark, root, leaf and stem of Avicenia marina were collected from the Muthupet mangrove forest and analyzed for heavy metal (Cu, Cd, Pb and Zn) accumulation and translocation. The results showed that the samples of A. marina have increased concentration of heavy metals especially, the non essential metals like Cd and Pb. Also, seasonal influence occurred during the accumulation of metals, among them summer and postmonsoon recorded as more contaminated season. The essential metals like Cu and Zn were found higher in rhizosphere sediment of A. marina when compared with non essential metals. Thus the plant was rapidly utilizing Cu and Zn for their active metabolism. The accumulation and translocation of Cu and Zn were lesser than the concentration scaled by WHO. High Bioaccumulation factors (BAFs) and Translocation factor were observed for Cd and Pb. The recorded values of metal in rhizosphere sediment and plant tissue were below the sediment quality guideline and upper critical limit of metals in plant. However, the values of present study several fold higher than the previously reported studies from the study area, which confirmed that extended anthropogenic activity takes place in the study area. These findings provide actual and reliable data on heavy metal accumulations and translocation in rhizosphere sediment to plant tissues of A. marina from Muthupet mangrove ecosystem, further long-term management and conservation policies are needed to protect the ecosystem.

1. Introduction

tidal zone, the intermittent medium-sized Avicenna mangrove shrubs are found. The deposited metallic elements are dissolved in beneath and bind with iron oxides and transferred to the mangrove plant. Despite the mangrove ecosystem are involved to impel of anthropogenic contaminant releases (Agoramoorthy et al., 2008; Ganeshkumar et al., 2018). Since a decade heavy metal pollution has a nuclear concern outright of anthropogenic affects particularly in polluted mangrove wetlands (Tam et al., 1995; Tam and Wong, 2000; Qiu et al., 2011). In terms of ecosystem, metals can be classified either as nutrients (Broadley et al., 2012) or, depending on their density, trace metals (Broadley et al., 2012), or heavy metals (Epstein and Bloom, 2004). While they act as micronutrients, it supplies essential plants metabolites and their lack may casts back on whole enzymatic system (Gupta, 2001). The excess can bealter cell membrane permeability, they inhibit enzyme activity and interfere with photosynthesis (MacFarlane and Burchett, 1999). Therefore, plants usually react differently in terms of use, storage and tolerance of metals in their different parts (MacFarlane

A mangrove forest consists of several mangrove species growing with submerged bases at the area between land and sea interface. They cover more than three quarters of tropical coastlines of almost 200,000km². They act as a buffer zone between the lagoon and the mountain mining areas, rich in metallic elements. The mangrove plays a most significant ecological role in stabilising and maintaining the balance within marine habitats and coastal landforms (Sarika and Chandra mohanakumar, 2008; Chen et al., 2010). Nearly fifty nine mangrove species are widespread in worldwide; Rhizophora sp., Avicennia marina are cosmopolitan species which are extensively present in several coastal habitats viz, India, Indonesia, Sri Lanka, Australia, Brazil and Arab Gulf and Eastern Africa (Shriadah, 1999; Burchett, 2003). The different zones of mangrove ecosystem are dominated by distinct mangrove types, by extended tidal amplitude and duration on the topography. Rhizophora are habituated on seaward sides of the mangrove forest, larger in size with above grounded root systems. In the central

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Corresponding author. E-mail addresses: drrajaram69@rediffmail.com, [email protected] (R. Rajendran).

https://doi.org/10.1016/j.enmm.2018.07.005 Received 23 August 2017; Received in revised form 10 July 2018; Accepted 16 July 2018 2215-1532/ © 2018 Elsevier B.V. All rights reserved.


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activities are occurring in the study area such as agriculture, aquaculture, salt pan, fishing and other recreational boating.

et al., 2003). The analysis of heavy metals concentration in mangrove plants has been proved to be a more accurate instrument than meagre soil analysis. In fact, soils retain heavy metals in different fractions and are submitted to the hydrodynamic variations archetypal of the mangrove ecosystem (Saenger and McConchie, 2004; Cuzzuol and Rocha, 2012). Still no valid reports available on heavy metal accumulation and translocation of mangrove plant from Muthupet mangroves. Hence in the present investigation to fulfil the gap with the following objectives 1) Analysis of both essential (Cu, Zn) and non essential (Pb, Cd) metals in rhizosphere sediment and various tissues of A. marina 2) In order to ensure the accumulation and translocation of metals in rhizosphere sediment to different plant tissues 3) Obtained results were correlated with international regulatory policies in order to identifying environmental quality of Muthupet mangroves.

2.2. Sampling All the samples are collected from the Muthupet mangrove ecosystem, Southeast coast of India between 2015–2016 which including four different seasons viz., Premonsoon, Monsoon, Postmonsoon and Summer. The rhizosphere sediment samples were collected from A. marina dominated area through 1meter acid cleaned PVC pipes at 10–15 cm depth. Plants samples like leaf, branch and root from A. marina were collected by hand picking, where as the stem and bark were collected with the help of acid cleaned stainless steel knife. Collected plant samples were thoroughly washed with Double distilled water and transported to the laboratory for further study.

2. Materials and methods 2.3. Heavy metal extraction and analysis 2.1. Study area The rhizosphere sediment samples were oven dried at 60 °C to remove the moisture content before this the residues of excessive rhizosphere was manually removed. After drying, the samples were subjected to crushing with acid clean dry mortar and pestle in order to get fine particles, and then sieved through a 2-mm sieve. 1 g of sieved sediment samples were weighed, and then digested with 10 ml of acid mixture HNO3, H2SO4 and HCLO4 in the ratio of 5:2:1 at 100 °C until clear solution were obtained to ensure proper digestion. A few drops of

Muthupet mangrove ecosystem (Lat. 10˚25′N: Long. 79˚39′E) is situated at southern most end of the Cauvery delta connected to Palk strait which opens to Bay of Bengal (Fig. 1). It covers around 12,000 ha between Thiruvarur and Thanjavur districts under Nagapattinam Wildlife Sanctuary. The lagoon receives fresh water from various canals viz. Paminiyar, Koraiyar, Kandankurichanar, Kilaithangiyar and Marakkakoraiyar. There are various developmental and socioeconomic

Fig. 1. Showing heavy metal (Cu, Cd, Pb and Zn) concentration in different seasons A. marina and rhizosphere sediment samples from Muthupet mangrove ecosystem. 273


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12.34 ppm. The amount of Cu present in the plant tissues were ranged between 2.43–7.74 ppm, it was lower than the rhizosphere sediment of A. marina (Fig. 2). Total concentration Cu in the Muthupet sediment samples ranged between 2.25 to 18.64 ppm (Fig. 2). Balakrishnan et al. (2015) reported that the mean Cu concentration in Muthupet sediment is 5.41 ppm but in present study shows double the values of previous report (Table 2). Moreover, average concentration of 58 ppm of Cu was recorded in uncontaminated surface sediment of India (Veerasingam et al., 2016). Cu accumulation in plant tissues were varied among the season, predominantly summer and post monsoon seems to be higher accumulation rate rather than the other season. Rajaram et al. (2017) reported that higher concentration of Cu in Muthupet mangroves during the summer and monsoon season. The concentration of Cu in sediment was several folds higher than the plant tissues. Significant differences were found in Cu concentration in plant tissues and the rhizosphere sediment (ANOVA, F = 0.41, P < 0.01). Multivariate Linear model regression results suggested that the concentration of metals in rhizosphere sediment of A. marina shown statistical significant with concentration of metals in bark (p = 0.01; r2 = 0.94) and root (p = 0.01; r2 = 0.94) with strong positive correlation. The leaf (p > 0.05; r2 = 0.74) and stem (p > 0.05; r2 = 0.44) showed nonsignificant variation and the concentration of metal in branch (p > 0.05; r2= - 0.28) was statistically non-significant with negative relationship (Fig. 3). The elevated level of Cd concentration was observed in the bark of A. marina with a value of 0.90 ppm. However, concentration of Cd ranged between 0.13 – 0.90 ppm was observed from the other parts of the same plant. Maximum of 1.83 ppm concentration of Cd was recorded in Muthupet sediment samples (Fig. 2). Plot shows higher Cd concentration of 1.83 ppm than the previous report in Muthupet sediment (Balakrishnan et al., 2015) and the background values of Cd concentration in uncontaminated surface sediment in India (Veerasingam et al., 2016). Cd accumulation in plant tissues were varied as Cu. Cd concentration in sediment was several folds lesser than accumulated cadmium in plant tissue. Non-significant differences were found in Cd concentration in plant tissues and the rhizosphere sediment (ANOVA, F = 0.41, P > 0.05). Multivariate Linear model regression results suggested that the concentration of metals in associated sediment of A. marina shown non-statistical significant with concentration of metals in other parts of plants (Fig. 3). The maximum amount of Pb was recorded from the stem of A. marina with a value of 23.73 ppm is shown in the Fig. 2. Concentration Pb recorded from the other parts of same plant was ranged between 6.43–23.73 ppm. Total concentration of lead is fivefold higher than the previous report in the Muthupet sediment but it is slightly higher than the uncontaminated surface sediment samples in India (Table 2). Pb gathering in plant tissues was varied among the season, chiefly premonsoon and post monsoon seems to higher accumulation rate than the other season. Pb concentration in sediment was much fold higher than accumulated Pb in plant tissue. No Significant differences were found in Pb concentration in plant tissues and the associated sediment (ANOVA, F = 0.15, P > 0.01). Multivariate Linear model regression results (Fig. 3) suggested that the concentration of metals in rhizosphere sediment of A. marina showed no statistical significant with concentration of metals all plant parts (p > 0.05) but the positive relationship found between metal concentration in rhizosphere sediment with stem, bark and root (p > 0.05; r2 = 0.20; 0.09; 0.15 respectively). The higher concentration of Zn was recorded from the rhizosphere sediment of A. marina with a value of 4.15–37.98 ppm with an average of 20.20 ppm (Fig. 2). Values recorded from the plant tissues were ranged between 0.66–30.09 ppm. Total concentration Zn in the Muthupet sediment samples varied ranged between 0.10 to 37.98 ppm (Fig. 2). The mean Zn concentration in Muthupet sediment is 7.28 ppm (Balakrishnan et al., 2015) while the background values in India of Cd in uncontaminated surface sediment is 95 ppm (Veerasingam et al., 2016). Zn accumulation in plant tissues were varied among the season,

Table 1 Quality control and Quality assurance of Instrumental methods. Metal

Cd

Cu

Pb

Zn

True ppm

Concentration detected (ppm)

%R

0.50 1.00 2.00 0.50 1.00 2.00 0.50 1.00 2.00 0.50 1.00 2.00

0.59 1.05 1.95 0.46 1.03 1.99 0.67 0.99 1.82 0.49 1.12 1.95

118 105 97.5 92 103 99.5 134 99 91 98 112 97.5

r

1.00

0.99

0.99

0.99

%R = recovery percentage, r = linear regression.

hydrochloric acid (2 N) were added to allow the complete digestion of sample (Jonathan et al., 2008). Double distilled water was added make up in to 25 ml and then filtered with a Whatman No.1 filter paper. Likely, 0.5 g of each plant sample was digested without addition of 2 N HCL. The solution was kept at room temperature until further analysis. Then concentration of heavy metals (Cu, Cd, Pb and Zn) in the sediment and plant samples was analyzed using Atomic Absorption Spectrophotometer (AAS 7000, Shimadzu). The working wavelength for the heavy metals are 213.85 nm for Zn, 324.75 nm for Cu, 228.80 nm for Cd and 217.00 nm for Pb. Quality assurance and Quality control (Table 1) testing was relied on the control of blanks and yield for chemical procedure. 2.4. Bioaccumulation factor and translocation factors BAF is a ratio of metal concentration in specified tissues (root, shoot, bark, branch and leaf) to the concentration in the surrounding environment (Mackay and Fraser, 2000; Franke et al., 1994; Feijtel et al., 1997). Translocation is an ability of plant to uptake and distribute across the plant body, it was estimated by calculating translocation factor. Both bioaccumulation factors (BAF) and translocation factors (TF) can be used as indicator to estimate phytoremediation potential of plant (Yoon et al., 2006). BAF = Concentration in tissues/concentration in rhizosphere sediment TF = Concentration in tissue (leaf, stem, bark and branch)/concentration in root 2.5. Statistical analysis All the Data were expressed in terms of means with standard deviation (SD). One way ANOVA performed to test the significant different in concentration of metals present in plant tissue and rhizosphere sediment. Multivariate regression model was used to identifying the relationship between metal concentration in rhizosphere sediment and plant tissue like root, leaf, stem, bark and branch. All the statistical procedures were carried out using origin 8.0 (Windows 7), data were processed and maintained using Microsoft excel (Windows 7). 3. Results In the present study, maximum concentration of Zn presents in the premonsoon seasons and copper on summer of A. marina associated sediment shown in the Fig. 2. While non-essential metal Pb & Cd present in plant tissues with highest concentration. Elevated Pb was found in the stem (postmonsoon), root (monsoon & premonsoon) followed by rhizosphere sediment (summer). The concentration of Cu was ranged between 2.43–12.34 ppm from the rhizosphere sediment of A. marina and the average was found to be 274


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Fig. 2. Showing heavy metal (Cu, Cd, Pb and Zn) concentrations in different seasons. A. marina and rhizosphere sediment samples from Muthupet mangrove ecosystem (—————) – Upper earth crust level of metal (Cu – 25; Cd – 0.098; Pb – 17; Zn –71), (____) – Previous report of heavy metals in Muthupet mangrove ecosystem (Cu – 5.41; Cd – 0.18; Pb – 3.45; Zn – 7.28). Table 2 Comparison of heavy metal concentration detected from Muthupet mangroves with the permissible level of international agencies along with background values.

Cu Cd Pb Zn

Permissible value of plant by WHO1

Upper critical level in plant3

Permissible value of CEQG, 20012

Background value of UEC4

Background value of Muthupet mangroves5

Present study Sediment Plant

10 0.02 2 0.06

30 3 NS 200

18.27 0.7 30.2 124

25 0.098 17 71

5.41 0.18 3.45 7.28

12.34 0.31 11.35 20.20

4.29 0.35 13.22 9.80

WHO = World Health Organization (1996); CEQG (1999) = Canadian Environmental Quality Guidelines; UEC = upper continental earth crust (Taylor and McLennan (1985); Muthupet mangroves (Balakrishnan et al. (2015); 5 = Beckett and Davis (1977).

r2 = −0.28) was statistically non-significant with negative correlation.

chiefly summer and post monsoon seems higher accumulation rate than the other seasons. Zn concentration in sediment was much fold higher than accumulated Zn in plant tissue. Significant differences were found in Zn concentration in plant tissues and the rhizosphere sediment (ANOVA, F = 0.41, P < 0.01). Multivariate Linear model regression results suggested (Fig. 3) that the concentration of metals in rhizosphere sediment of A. marina shown statistical significant with concentration of metals in bark (p = 0.01; r2 = 0.94) and root (p = 0.01; r2 = 0.94) with strong positive correlation. The leaf (p > 0.05; r2 = 0.74) and stem (p > 0.05; r2 = 0.44) showed non-significant variation and the concentration of metal in branch (p > 0.05;

3.1. Translocation of metals The calculated translocation factor (TF) of Cu, Cd, Pb, and Zn for A. marina is given in Table 3. In the present study, the translocation factor (TF) varied between the plant parts and among the non essential metals like Cd and Pb has the TF values comparably higher than the TF values of essential metals in A. marina. In A. marina, translocation of metal was high in root-bark for Cd, root-stem for Pb, root-branch for Cu and rootleaf for Zn (Table 4). However, the unique range of metals translocation 275


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Fig. 3. Showing significant relationship between accumulated heavy metal (a = Cd, b = Cu, c = Pb and d = Zn) in different tissues of A. marina with rhizosphere sediment samples of Muthupet mangrove ecosystem. Regression models describing the relationships by adjusted determination coefficient (R2) and significance level (P).

3.2. Bioaccumulation of metals

Table 3 Biological accumulation factor (BAF) and Translocation factor (TF) of heavy metal (Cu, Cd, Pb and Zn) in Avicennia marina collected from Muthupet mangroves ecosystem, Southeast coast of India. Bioaccumulation factor

The investigated species of A. marina were characterized by a bioaccumulation (BAF) for some of heavy metals (Table 3). BAF was generally higher for Pb with the mean value of 1.16 for A. marina, followed by Cd, Zn and Cu. However, A. marina shown that higher degree of bioaccumulation in roots.In A. marina, both the essential metals Cu and Zn shown relatively lesser BAF (BAF < 1) values indicated that the plant has been rapidly utilizing the essential metals for their active metabolism. Thus, both Cu and Zn are essential plant micronutrients whereas the non essential metals like Cd and Pb shown the BAF greater than one. Thus the present study evidenced that A. marina has the tendency to accumulate non essential metals and known to be potent ecological indicator for heavy metal pollution with the correlation of earlier reports.

Translocation factor

Metal

Branch

Leaf

Stem

Bark

Root

Branch

Leaf

Stem

Bark

Cd Pb Cu Zn

0.71 1.09 0.36 0.3

1.1 1.06 0.35 0.68

1.19 1.25 0.3 0.35

1.9 1.19 0.28 0.37

0.77 1.24 0.45 0.73

0.92 0.88 0.8 0.41

1.42 0.86 0.77 0.93

1.54 1.01 0.67 0.48

2.46 0.96 0.62 0.51

The bolder values indicated BAF and CF more than 1.

was observed in all the samples resulted in tissue specific translocation factor. The mobility of non essential elements including Cd and Pb was higher in bark, stem, compared with the essential metals. MacFarlane et al. (2003) reported higher degree of metals accumulation in both root and leaf. Thus the study was evidenced that Lead is non-essential and the translocation also minimal to all other because of the potent exclusion mechanism present in the plant (MacFarlane et al., 2003).

4. Discussion Concentrations of metal in sediment and plants were varied depending upon the plant species (Alloway et al., 1990) and season (Mathivanan and Rajaram, 2014). Also uptake of heavy metals by plants from the surrounding environment was massively influenced by several factors including water flow in to the roots, active transport through plasma membrane of epidermal cells present in the root tissue 276


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Table 4 Comparative account on heavy metal (Cu, Cd, Pb and Zn) concentration Avicennia marina from Muthupet mangroves with available literature. Species

Cu

Cd

Pb

Zn

Reference

Study area

Acanthus ilicifolius Aegicerus corniculatum Kandelia candel Avicennia marina Avicennia marina Rhizophora apiculata A. marina Laguncularia racemosa Avicennia marina Avicennia marina Avicennia marina Avicennia marina Aegiceras cornuculatum Avicennia marina

40.7 32.7 24.3 153 20 10.89 3.2 3.7 4.4 16 nil 5 17 2.25–18.64

0.4 0.3 0.5 1.5 0.06 0.15 nil nil nil nil nil nil nil 0.07–0.83

33.33 30 40 189 5.8 0.51 1.7 6.2 6.9 8 nil 1.8 7.9 0.41–23.73

207.1 82.5 122.9 378 26 14.73 14.3 35.8 11 15 nil 23 17 0.66–37.99

Ong Che (1999) Ong Che (1999) Ong Che (1999) Chaudhuri et al. (2014) Nath et al. (2013) Yu et al. (2007) MacFarlane and Burchett (2002) Defew et al. (2005) Sadiq and Zaidi (1994) Chen (2003) Zahir et al. (2004) Zheng and Lin (1995) Chen (2003) Present study

Mai Po, Hong Kong Mai Po, Hong Kong Mai Po, Hong Kong Sydney estuary (Australia Sydney estuary (Australia) Peninsula, south China Australian mangrove Panama Saudi coast Ting Kok, Hong Kong Karachi, Pakistan Shenzhen, S. China Ting Kok, Hong Kong Muthupet mangroves

uptake and accumulation in plants such as size of the root, concentration of the metals, nature of the sediment, level of salinity, temperature, pH and the presence essential nutrients (Yan et al., 2017). Interestingly, Huang and Cunningham 1996 found, translocation of Pb in monocot plants were several fold increased when treated with 1 mM HEDTA a synthetic chelator, EDTA enhanced plant uptake of Pb and Hg (Hale and Wallace, 1970) also known as chelant induced metal uptake (Nowack et al., 2006). The Muthupet mangrove ecosystem was rich in anthropogenic activities (Balakrishnan et al., 2015; Natesan et al., 2014; Priya et al., 2014; Thilagavathi et al., 2011), primarily the main sources of heavy metals in the lagoon is the agricultural drain, the ecosystem is surrounded by enormous agricultural land which mainly used for paddy cultivation along with it receives various construction based wastages (Priya et al., 2014; Thilagavathi et al., 2011). The present study suggested that the mobility of non essential metal to the A. marina tissue is mainly influenced by natural and chemical chelators present the environment. Nowack and Van Briesen (2005) described various chelators present in the environment as anthropogenic wastages such as EDTA, EDDHA and glyposate as herbicide (in agriculture), phosphonates used as a cement modifier and EDTMP, HEDP, DTPMP and ATMP used in detergent application (Jaworska et al., 2002). Most importantly, the recorded values of Pb in A. marina were somehow higher than the permissible scale detailed by WHO especially in plant and soil (WHO, 1996). The root – shoot, leaf, branch and bark translocation of metal was limited in A. marina. Zinc mobility was relatively higher in A. marina through absorption at the root and transported to leaf tissue (MacFarlane and Burchett, 1999), than other mangrove sp. (Chiù et al., 1995) and different angiosperms (Streit and Stumm, 1993). Immobilization, exclusion, complexation by phytochelatins, compartmentalization and barriers at the root endodermis are certain physiological mechanisms (Hall, 2002; Almeida et al., 2007) which may responsible for restriction/regulation of metal uptake, accumulation and translocation within plants (Baker and Walker, 1990). Brake fern (Pteris vittata) grown at 7500 ppm of arsenic containing soil in which this showing hyper accumulation behaviour of heavy metal like arsenic and translocated from the root to leaf around 150 fold (Ma et al., 2001). Majority of the plants showed a common tendency to accumulate metals either in root /pneumatophores (Chowdhury et al., 2015). In this present study, the prominent level of metal was accumulated primarily in root followed by bark and stem. Thus the phenomenon was correlated with (Chowdhury et al., 2015) and the organs like root and stem are the barriers to protect the sensitive part of the plants (Pahalawattaarachchi et al., 2009). In the present study the recorded concentration of heavy metal in rhizosphere sediment exhibiting reported values of this study area (Balakrishnan et al., 2015), but all the concentration below the permissible level of Canadian Environmental Quality Guidelines (Table 2). Likely, recorded concentration in plant tissues below the upper critical

(Hall, 2002; MacFarlane and Burchett, 2000). The most possible source of elevated heavy metals in Muthupet mangrove forest was attributed by direct influence of household and municipal wastages, mixing of untreated industrial effluents, drain water from agriculture and aquaculture ponds (Rajaram et al., 2017; Ganeshkumar et al., 2018). However, idol immersion activities are the major contributors of heavy metals in the major aquatic bodies of India (Giripunje et al., 2014; Rajaram et al., 2017). Likely, the present investigation was directly correlated with the finding of Bhuyan et al. (2017) water and sediment samples of the Meghna River, Bangladesh (Bhuyan et al., 2017). Cu is an essential metal which has an important physiological role including photosynthesis and respiration, reproduction, disease resistance, water permeability, carbohydrate and nitrate metabolisms (Kabata-Pendias and Pendias, 2001). Notably, Plants utilize Cu for their basic metabolism influenced by several phenomenon including active transportation and compartmentalization (Hall, 2002). Cu concentration in xylem and phloem saps was correlated with the concentration of amino acids in the plants during their development aspect. The inter transport of Cu from the root to other parts is much lower than other metals due to the brawniest capillary action of roots (MacFarlane et al., 2003). Higher degree of metals accumulation in both root and leaf was observed in A. marina and it has a regulator mechanism to control metal uptake via root, primarily endodermis of roots (MacFarlane and Burchett, 2000). The saturation or exclusion mechanism was observed by Baker 1981, resulting even increased concentration of Cu in sediment not being accumulated/transported by A. marina (MacFarlane and Burchett, 2002). Accumulation of Cu in root and bark showed strong linear relationship at different concentration of Cu present in the rhizosphere sediment and this study was correlated with MacFarlane et al. (2003). Cd is non-essential element which is highly toxic to plants, affects growth, metabolism and the water transport of plants (Divan et al., 2009) and causing inhibition of germination, chlorosis of leaves & plant biomass reduction (Wang et al., 2013). They are metabolically active and effectively absorbed by both root and leaf systems (SmeyersVerbeke et al., 1978). In the present study Cd was rapidly translocated to bark followed by stem, leaf and branches of A. marina. Comparably, because of its high mobility within the soil–plant system Cd showed higher translocation factor than other metals (MacFarlane et al., 2003; Nedjimi and Daoud, 2009; Gill et al., 2012) Lead is non-essential element and the translocation also minimal than all other metals, because of the potent exclusion mechanism present in the plant (MacFarlane et al., 2003), reported by many researchers (Qiu et al., 2011; Yu et al., 2007; Zheng and Lin, 1995; MacFarlane and Burchett, 2002) that accumulation and translocation of Pb in plant tissues are generally limited than the other metals like Cu, Zn and Cd. There are several factors contributing the level of heavy metal 277


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References

limit of metals in plant (Beckett and Davis, 1977), whereas the present study demonstrate the metal concentration was several fold higher than the WHO permissible level in plant. Compared to the concentrations of metals in mangrove plants around the world, the metal levels recorded from A. marina from Muthupet mangrove were at higher in most investigated metals except Zn from few studies (Nath et al., 2013; Qiu et al., 2011; Sadiq and Zaidi, 1994; Chen, 2003; Zahir et al., 2004; Zheng and Lin, 1995; Chen et al., 2003). Mean while the recorded concentration was lesser than the following studies reported (Ong Che, 1999; Chaudhuri et al., 2014; MacFarlane and Burchett, 2000). Among the metals recorded, Zn and Pb seems to be several fold higher in Mai Po, Hong Kong and Sydney estuary (Australia) when compared with Muthupet mangrove ecosystem (Ong Che, 1999; Chaudhuri et al., 2014). Yoon et al. (2006) analysed a total of 36 plant species from the different family in order to identifying potent hyperaccumulation among them the plant like Cyperus esculentus L., Plantago major L (Pb), Paspalum notatum, Cyperus esculentus L, Rubus fruticosus, Sesbania herbacea (Cu), Gentiana pennelliana, Bidens alba var, Cyperus esculentus, Rubus fruticosus, Sonchus asper (Zn) accumulating higher metal content in shoot rather than the root collected from northwest Jacksonville, Florida (Table 4). Likely, A. marina from Muthupet mangrove had the higher concentration of non essential metal in different tissues rather than the root tissue. BAF of the present study was higher than the previous studies concluded by Li et al. (2016) (A. marina, A. corniculatum, S. caseolaris, S. apetala) for Cd and Cu; Yoon et al., 2006 Cd, Pb and Cu except fem plant and lesser than Kim et al., 2003 (Polygonum thunbergii) for Cd, Cu, Pb and Zn. The hydroponic experimental study shown the accumulation patterns of metal is Cd < Pb < Zn in whole plants of C. odorata (Tanhan et al., 2007) and Kim et al. (2003) reported a translocation pattern in Polygonum thunbergii with a different accumulation pattern (Cd < Pb < Zn < Cu), Nanda Kumar et al. (1995) reported that the accumulation of metals in Brassica juncea shoots were increased in the order as follows Cu < Cd < Pb < Zn. But the present study shown the accumulation and translocation order as follows Pb (1.16) > Cd (1.13) > Zn (0.48) > Cu (0.38) and Cd (1.5) > Pb (0.92) > Cu (0.7) > Zn (0.58) respectively.

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5. Conclusion The present study has concluded that accumulation of Pb and Cd in all the tissue like branch, leaf, root, stem and bark of Avicennia marina is equal or lesser than rhizosphere sediment concentrations under field conditions. While the translocation and bioaccumulation factor of root and sediment to bark, stem, leaf and branch was greater than one, thus confirmed that the A. marina have the tendency to accumulate and translocate the non essential metals. However, A. marina tissues especially, bark, stem and leaf may be employed as a biological indicator of Muthupet mangrove environmental exposure of non essential metals like Pb and Cd due to increased Bioaccumulation and translocation factor evidenced. According to the BAF and TF values it is evident that a tissue of AM has increased ability to accumulate and translocate both essential and nonessential metals. Hence it could be considered as the potent bioaccumulator species to be effectively used for sustainable management of valuable mangrove environment.

Acknowldgement All the authors are thankful to the authorities of Bharathidasan University for providing the necessary facilities to conduct this study; authors also thankful to Ministry of Earth Science, Government of India (Ref. No.: MoES/36/OOIS/Extra./9/2013) for providing the financial assistance.

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