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International Journal of Phytoremediation
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Accumulation of Trace Metals by Mangrove Plants
in Indian Sundarban Wetland: Prospects for
Phytoremediation
Ranju Chowdhury
a
, Paulo J.C. Favas
bc
, J. Pratas
cd
, M. P. Jonathan
e
, P. Sankar Ganesh
f
&
Santosh Kumar Sarkar
a
a
Department of Marine Science, University of Calcutta, Ballygunge Circular Road, Calcutta,
West Bengal, India
b
Department of Geology, School of Life Sciences and the Environment, University of Trás-os-
Montes e Alto Douro, UTAD, Quinta de Prados Vila Real, Portugal
c
IMAR-CMA Marine and Environmental Research Centre / MARE – Marine and Environmental
Sciences Centre, Faculty of Sciences and Technology, University of Coimbra, Coimbra,
Portugal
d
Department of Earth Sciences, Faculty of Sciences and Technology, University of Coimbra,
Coimbra, Portugal
e
Centro Interdisciplinario de Investigaciones Estudios sobre Medio, Ambiente Desarrollo
(CIIEMAD), Instituto Politécnico Nacional (IPN), Calle de Junio de Barrio la Laguna Ticomán
C.P., Del. Gustavo A. Madero, México, D.F., MEXICO
f
Department of Biological Sciences, Birla Institute of Technology and Science, Pilani,
Hyderabad Campus, Hyderabad, Telengana, India
Accepted author version posted online: 12 Jan 2015.
To cite this article: Ranju Chowdhury, Paulo J.C. Favas, J. Pratas, M. P. Jonathan, P. Sankar Ganesh & Santosh Kumar Sarkar
(2015) Accumulation of Trace Metals by Mangrove Plants in Indian Sundarban Wetland: Prospects for Phytoremediation,
International Journal of Phytoremediation, 17:9, 885-894, DOI: 10.1080/15226514.2014.981244
To link to this article: http://dx.doi.org/10.1080/15226514.2014.981244
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International Journal of Phytoremediation, 17: 885–894, 2015
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ISSN: 1522-6514 print / 1549-7879 online
DOI: 10.1080/15226514.2014.981244
Accumulation of Trace Metals by Mangrove Plants in Indian
Sundarban Wetland: Prospects for Phytoremediation
RANJU CHOWDHURY
1
,PAULOJ.C.FAVAS
2,3
,J.PRATAS
3,4
,M.P.JONATHAN
5
, P. SANKAR GANESH
6
,
and SANTOSH KUMAR SARKAR
1
1
Department of Marine Science, University of Calcutta, Ballygunge Circular Road, Calcutta, West Bengal, India
2
Department of Geology, School of Life Sciences and the Environment, University of Tr
´
as-os-Montes e Alto Douro, UTAD, Quinta
de Prados Vila Real, Portugal
3
IMAR-CMA Marine and Environmental Research Centre / MARE – Marine and Environmental Sciences Centre, Faculty of
Sciences and Technology, University of Coimbra, Coimbra, Portugal
4
Department of Earth Sciences, Faculty of Sciences and Technology, University of Coimbra, Coimbra, Portugal
5
Centro Interdisciplinario de Investigaciones Estudios sobre Medio, Ambiente Desarrollo (CIIEMAD), Instituto Polit
´
ecnico
Nacional (IPN), Calle de Junio de Barrio la Laguna Ticom
´
an C.P., Del. Gustavo A. Madero, M
´
exico, D.F., MEXICO
6
Department of Biological Sciences, Birla Institute of Technology and Science, Pilani, Hyderabad Campus, Hyderabad, Telengana,
India
The work investigates on the potential of ten mangrove species for absorption, accumulation and partitioning of trace metal(loid)s
in individual plant tissues (leaves, bark and root/pneumatophore) at two study sites of Indian Sundarban Wetland. The metal(loid)
concentration in host sediments and their geochemical characteristics were also considered. Mangrove sediments showed unique
potential in many- fold increase for most metal(loid)s than plant tissues due to their inherent physicochemical properties. The
ranges of concentration of trace metal(loid)s for As, Cd, Co, Cr, Cu, Fe, Hg, Mn, Ni, Pb and Zn in plant tissue were 0.006–0.31,
0.02–2.97, 0.10–4.80, 0.13–6.49, 4.46–48.30, 9.2–938.1, 0.02–0.13, 9.8–1726, 11–5.41, 0.04–7.64, 3.81–52.20 µgg
−1
respectively. The
bio- concentration factor (BCF) showed its maximum value (15.5) in Excoecaria agallocha for Cd, suggesting that it can be considered
as a high-efficient plant for heavy metal bioaccumulation. Among all metals, Cd and Zn were highly bioaccumulated in E. agallocha
(2.97 and 52.2 µgg
−1
respectively. Our findings suggest that the species may be classified as efficient metal trap for Cd in aerial parts,
as indicated by higher metal accumulation in the leaves combined with BCF and translocation factor (TF) values.
Keywords geochemical characteristics, Excoecaria agallocha, bioaccumulation
Introduction
Mangroves are facultative halophytes and form a unique
group of intertidal ecosystems. They are increasingly
threatened due to anthropogenic chemicals sourced from
uncontrolled agricultural runoff, urban and industrial efflu-
ents and wastewaters, coupled with urbanization and pop-
ulation growth. Despite being exposed to metal contam-
inated sediments, mangroves seem to be highly tolerant
to heavy metals. This may be due to the ability of man-
groves to exclude or regulate uptake of metals at root
level and limit translocation to the shoot (MacFarlane and
Burchett 2001). Mangrove sediments are anaerobic and re-
duced, as well as rich in sulphide and organic matter. They
Address correspondence to Santosh Kumar Sarkar, Department
of Marine Science, 35 Ballygunge Circular Road, Calcutta, West
Bengal 700019, India.
Color versions of one or more of the figures in the article can
be found online at www.tandfonline.com/bijp.
therefore favor the retention of water-borne trace metals
(Tam and Wong 2000) and the subsequent oxidation of sul-
phides allows metal mobilization and bioavailability (Clark
et al. 1998).
The present study has been undertaken with the following
objectives: (i) to investigate the extent of accumulation and
the distribution of trace metal(loid)s in individual plant tis-
sues (ii) to establish correlation between metal(oids) present
in sediments and plant tissues and (iii) to find out the suitable
candidate for phytoremediation species to be used for con-
servation and sustainable management of Sundarban coastal
regions.
Materials and Methods
Area of Investigation
The Indian Sundarban, formed at the estuarine phase of the
Hugli (Ganges) River Estuary is a tide-dominated mangrove
wetland belonging to the low-lying humid and tropical coastal
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886 R. Chowdhury et al.
zone. This vulnerable environment suffers from environmen-
tal degradation due to rapid human settlement, tourism and
port activities, and operation of excessive number of mech-
anized boats, deforestation and increasing agricultural and
aquaculture practices. A significant ecological change is pro-
nounced in this area due to reclamation of land, deforesta-
tion, huge discharges of untreated or semi-treated domestic
and municipal wastes and effluents from multifarious indus-
tries such as tanneries, chemicals, paper and pulp, phar ma-
ceuticals as well as contaminated mud disposal from harbor
dredging. All these factors impart a variable degree of anthro-
pogenic stresses leading to elevated concentrations of heavy
metals.
Two study sites, Chandanpiri (S
1
) and Jharkhali (S
2
)have
been chosen for the present investigation, covering the eastern
and western flank of Sundarban (Fig. 1). The later (S
2
) is more
diversely populated with mangrove species (n = 7) than the
former (S
1
)(n= 4) and this anomalous distribution patterns
of mangrove species is related to multiple factors, such as in-
fluence of environmental gradients (especially salinity), wave
energy and tidal amplitude controlling sediment dispersal pat-
terns.
Collection and Processing of Sediment Samples
Sediment samples were collected in triplicate from top 0–5 cm
of the surface at each sampling site (Corsolini et al. 2012)
over an area of 1m x 1m using a clean, acid-washed plastic
scoop. Samples were stored in clean plastic zip lock pouches
and transported to the laboratory. Individual sediment sam-
ples were placed in a ventilated oven at low temperature (max.
45
◦
C) (Watts et al. 2013) as high temperature may contribute
to the alteration of volatile and even non- volatile organics of
the sample (Mudroch and Azcue 1995), until they get com-
pletely dried. Samples were pulverized using an agate mortar
and pestle, sieved through 63 µm metallic mesh since this frac-
tion contains more sorbed metal per gram of sediment due to
its larger specific surface area (Chatterjee et al. 2009) and indi-
vidually transferred into pre-cleaned, inert polypropylene bags
and stored at room temperature until subsequent extraction
and chemical analyses. Sediment pH was determined by pH
meter (Water Analyzer 371). Organic carbon (C
org
) content
of the sediments was determined following a rapid titration
method (Walkey and Black, 1934). Mechanical analyses of
substrate sediments were done by sieving in a Ro-Tap shaker
(Krumbein and Pettijohn 1938), and statistical computation
of textural parameters was done by using the formulae of
Folk and Ward (1957) and following standards of Friedman
and Sanders (1978).
Collection and Preservation of Mangrove Samples
During October – November (2012), plant organs of Avicen-
nia officinalis, A. marina, A. alba (Avicenniaceae), Bruguiera
gymnorrhiza, Ceriops tagal, Rhizophora apiculata (Rhi-
zophoraceae), Aericeros corniculatum (Myrsinaceae), Ex-
coecaria agallocha (Euphorbiaceae), Lumitzera racemosa
(Combretaceae), Heritiera fomes (Malvaceae), Sonneratia
caseolaris (Lythraceae) were randomly collected, from dif-
ferent trees belonging to the same species at low tide
conditions for root / pneumatophore collection in tidal
exposure.
For analyses of plant samples, we took leaves of two differ-
ent stages of development: young and mature as well as trunk
bark, pneumatophores/roots in consideration. Sample organs
were collected from trees that were greater than 1m tall with a
girthatbreastheightofgreaterthan2cmandthatwereofsim-
ilar health conditions (as determined by degree of predation
on leaves) and were then sampled with a thin stainless steel
knife. Samples were t horoughly washed by deionised water in
the laboratory to remove dust, sediment particles and algal
trace. These were oven-dried under 50
◦
C until they became
completely dried and then homogenized (methods adapted
by MacFarlane et al. 2003). Samples were preserved in clean
sealed plastic zip pouches for further analyses.
Analytical Protocol
The dried sediment samples were prepared by microwave di-
gestion (Multiwave 3000, Anton Paar) with aqua regia in
closed Teflon vessels (Walsh et al. 1997). The determination of
total metal(loid) contents was performed using current ana-
lytical methods, including: Atomic Absorption Spectrometry
(AAS, SOLAAR M Series equipment from Thermo–Unicam)
for Co, Cr, Cu, Fe, Mn, Ni, Pb and Zn; coupled graphite fur-
nace AAS for As and Cd; and a hydride generation system
(HGS) linked to an atomic absorption for Hg. Most of the
trace metal(loid)s in consideration were very low in concen-
tration in the samples, so precautions were taken and necessary
instruments were used for particular trace metal(loid)s.
The plant samples were also microwave digested with an
HNO
3
–H
2
O
2
mixture in closed Teflon vessels, which was fol-
lowed by analysis with AAS for Cu, Fe, Mn and Zn; coupled
graphite furnace AAS for As, Cd, Co, Cr, Ni and Pb due to the
reduced sample amount and to increase sensitivity; and a hy-
dride generation system (HGS) linked to an atomic absorption
for Hg (Fletcher 1981; Brooks 1983; Van Loon 1985).
The detection limits for metal(loid)s in sediment samples
were 0.004 µgg
−1
for Cd; 0.01 µgg
−1
for As and Hg; 0.4 µg
g
−1
for Zn; 1 µgg
−1
for Co, Cu, Mn and Ni, 1.5 µgg
−1
for Cr
and Pb; 2 µgg
−1
for Fe. The detection limits for metal(loid)s
in plant samples were 0.002 µgg
−1
for Cd; 0.005 µgg
−1
for
As, Hg and Pb; 0.01 µgg
−1
for Cr and Ni; 0.02 µgg
−1
for
Co; 0.5 µgg
−1
for Cu and Mn; 0.8 µgg
−1
for Fe; 0.2 µgg
−1
for Zn.
Quality assurance and quality control
Certified reference material for sediment (2711 SRM reference
material Montana Soil, from LGC Promochem, Barcelona,
Spain), and for plant materials (Virginia Tobacco Leaves
(CTA-VTL-2, Poland), were used to ensure the quality con-
trol and accuracy of the analyses. The agreement between the
certified reference values and the values determined by the
analytical method were in the range of 87.8% to 108.2%.
Downloaded by [Universidade de Tras-os-Montes e Alto Douro] at 04:51 08 July 2015
Accumulation of Trace Metals by Mangrove Plants in Sundarban 887
Fig. 1. Map showing location of two study sites Chandanpiri (S
1
) and Jharkhali (S
2
) in Indian Sundarban wetland.
Concentration and Translocation Factors
In order to compare the degree of storage of the metal(loid)s,
bio- concentration factors (BCF) were calculated as con-
centration of metal(loid) in tissue over the concentration of
metal(loid) in sediment. Translocation factor (TF) was de-
scribed as ratio of trace metal(loid)s in plant shoot to that in
plant root (Usman and Mohamed 2009; Usman et al. 2012).
It is important to note that TF>1 indicates that the plant
translocates metals effectively from root to the shoot (Baker
and Brooks 1989).
Statistical Analyses
Partitioning of individual metal(loid)s in plant tissues and sed-
iments were pooled over site and sampling time and analyzed
using one-way ANOVA in the ANOVA module of STATIS-
TICA Statsoft Inc. 1995. Statistica for windows release 5.0.
Tulsa. Oklahoma. USA. It was assessed by using MINITAB
13. Weightage of independent variables was assessed by stan-
dardized beta coefficients (Statsoft Inc. 1995. Statistica for
windows release 5.0. Tulsa. Oklahoma. USA). Independent
variables examined with exponential accumulation relation-
ships were log transformed ln (x + 1), prior to all calculation
(Zar 1966).
Results and Discussion
Sediment Geochemistry
Sediment showed differences in their physicochemical proper-
ties pertaining to pH, C
org
and textural properties. Values of
pH are characterized by mild alkaline in nature (7.76–8.01)
and were similar between plants within the same location
(p > 0.05). According to Middleburg et al. (1996) mangrove
sediments have basic pH values due to the limited buffer ca-
pacity of these sediments. The C
org
values showed very low
concentrations (0.60–0.66%), which might be the result of
marine sedimentation and mixing processes at the sediment-
water interface where the rate of delivery as well as the rates
of degradation by microbial-mediated processes can be high
(Canuel and Martens 1993). Regarding texture, sediment sam-
ples exhibit a variable admixture of sand (1.80–15.45%), silt
(32.58–38.93%) and clay (51.98–59.28%). A variable amount
of erosion and depositions in study sites can explain the ob-
served heterogeneity in textural contents.
Possible sediment enrichment of metal(loid)s was evaluated
in terms of the geoaccumulation Index (I
geo
)ofM
¨
uller (1979).
It consists of seven classes. Class 0 (practically unpolluted): I
geo
≤ 0; Class 1 (unpolluted to moderately polluted): 0 < I
geo
< 1;
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