Makara Journal of Science 17/1 (2013) 23-28

23
23
Bioconcentration Factor of Copper (Cu), Lead (Pb), and Zinc (Zn) in Anadara
indica Related to the Water Quality in Coastal Areas

Noverita Dian Takarina
1*
, Dietriech Geoffrey Bengen
2
, Harpasis Slamet Sanusi
2
,
and Etty Riani
2


1. Program of Marine Sciences, Post Graduate School, Institut Pertanian Bogor, Bogor 16680, Indonesia
2. Faculty of Fisheries and Marine Science, Institut Pertanian Bogor, Bogor 16680, Indonesia

*
E-mail: takarinanoverita@hotmail.com


Abstract

The Garapan river mouth forms part of the Tanjung Pasir coastal area. This region receives materials not only from
coastal waters but also from domestic sewage and industrial wastewater that contains heavy metals such as Cu, Pb, and
Zn. On the contrary, the Cibungur river mouth in the different coastal area, receives relatively lower amounts of
domestic sewage and industrial wastewater. The objective of this study was to determine the Cu, Pb, and Zn content in
the coastal sediment as well as the levels of A.indica and their relationship with water quality parameters. Samples were
collected from four stations located in the Garapan and Cibungur river mouths and were analyzed for metal content
using atomic absorption spectrometry Shimadzu 6300. Samples of A. indica found in the field are categorized into three
diferent size classes. It is because size related to heavy metal accumulation. Results showed that bioconcentration factor
(BCF) values were Zn>Cu>Pb in both locations. Small size A. indica tends to have higher values of BCF for Cu and Zn
compared to medium and larger sized samples. Furthermore, the BCF values of Cu, Pb, and Zn in A. indica were higher
when the sediment had a lower concentration of organic matter.


Abstrak

Faktor Biokonsentrasi Tembaga (Cu), Timbal (Pb), dan Seng (Zn) pada Anadara indica yang Dihubungkan
dengan Kualitas Air di Daerah Pesisir. Muara sungai Garapan merupakan bagian dari kawasan pesisir Tanjung Pasir.
Daerah ini menerima buangan tidak hanya dari kawasan pesisir tetapi juga dari perumahan dan industri disekitarnya
yang mengandung logam berat seperti Cu, Pb, dan Zn. Sebaliknya, muara sungai Cibungur relatif menerima buangan
perumahan dan industri yang lebih sedikit. Penelitian ini bertujuan untuk menentukan kandungan Cu, Pb, dan Zn pada
sedimen dan Anadara indica, dan hubungannya dengan parameter kualitas air. Sampel diambil dari empat stasiun di
daerah perairan muara sungai Garapan dan Cibungur selanjutnya dianalisis kandungan logam beratnya menggunakan
atomic absorption spectrometry Shimadzu 6300. Sampel A. indica yang ditemukan di lapangan dikelompokkan dalam
tiga kelas ukuran. Hal itu karena ukuran berhubungan dengan akumulasi logam berat. Hasil penelitian menunjukkan
bahwa nilai faktor biokensentrasi (BCF) di kedua muara sungai adalah Zn>Cu>Pb. Sampel A. indica berukuran kecil
cenderung memiliki nilai BCF Cu dan Zn lebih tinggi dibandingkan sampel berukuran sedang dan besar. Selanjutnya,
BCF dari Cu, Pb, dan Zn pada A. indica lebih tinggi ketika sedimen memiliki kandungan organik yang lebih rendah.

Keywords: Anadara indica, bioconcentration factor (BCF), heavy metals, sediments, water quality



1. Introduction

Heavy metals are commonly found in natural waters and
some are essential to living organisms, yet they may
become highly toxic when present in high
concentrations [1]. These metals also gain access into
the ecosystem through anthropogenic sources and are
distributed in the water body and in suspended solids
and sediments during the course of their mobility [2].
Once adsorbed, heavy metals are then absorbed into and
across the biological surface and distributed throughout
the organism.

Aquatic organisms (including mollusks), bioaccumulate
trace metals in considerable amounts and remain in the
environment for long periods. As a consequence,
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accumulation of pollutants, mainly heavy metals, in
mollusks have been reported [3-7]. Therefore, regular
monitoring to trace elements/heavy metals, in particular
Hg, Cd, Ni, Cu, Pb, and Zn, is thoroughly important.
Anadara indica is a well-known commercial species
used for protein source for local people. In Indonesia,
this species can be harvested from the natural habitat. In
this study, two locations were chosen namely Garapan
rivermouth, Tanjung Pasir, Tangerang and Cibungur
rivermouth, Panimbang. Both are located at Banten
Province. Center for Statistical Biereau in 2012 reported
that land use in those area are as follows: agricultural
activities, settlements, and industries. Pandeglang
compared to Tangerang are agriculture: 138484 ha :
1371 ha; settlements: 90.38% : 53.6%, the amount of
industries: 13 : 503. A survey on both locations showed
that A. indica is sold and consumed by local people; it is
locally called kerang mencos.

In monitoring programme, size of individual of species
is important since from the studies before, it showed
that heavy metals content in most of mollusks was
related somehow to their size [8-9]. The
bioconcentration factor (BCF) is the ratio of metal
concentration in an organism to metal concentration in
water/sediment.

In this study, the BCF was measured using the formula
(1) [10]:
Concentration of metals in organism
BCF = ---------------------------------------------- (1)
Concentration of metals in sediments

Besides heavy metals, surface water quality assessment
is commonly considered for an assessment of pollution
in aquatic environment settings. Water quality
parameters, such as dissolved oxygen, temperature, pH,
and salinity, provide an indication of the health quality
of the associated water and organisms in the coastal
environment [11]. Water temperature is a very
important factor for aquatic life, controlling the rate of
metabolic and reproductive activities, and determining
the survival of species. Temperature also affects the
concentration of dissolved oxygen and can influence the
activity of bacteria and toxic chemicals, such as heavy
metals, in water [12].

pH represents the effective concentration (activity) of
hydrogen ions (H
+
) in water and can have a direct or
indirect effect on invertebrate life; decreasing pH can
increase the solubility of metals in water [13].

Salinity in an estuary usually ranges from 535%. It can
influence the heavy metals in the environment by
forming stable chloro-complexes in the presence of
seawater. Higher salinity will increase the sorption of
metals on particulates in seawater. Waters with high
amounts of salt, such as the ocean (which contains about
35 g of salt per 1,000 g of water), have a low dissolved
oxygen concentration. As the amount of salt in any body
of water increases, the amount of dissolved oxygen
decreases. An increase in salt concentration due to
evaporation of water from an ecosystem tends to reduce
the dissolved oxygen available to the ecosystems
inhabitants. It is important to know the organic carbon
(C) content because butrient enrichment in estuarine
water can thus be predicted. Total nitrogen (N) values
are also important for benthic organisms. Sulfur (S)
usually exist in small amounts in seawater. The purpose
of this study is to determine the content of Cu, Pb, and
Zn in both sediment and A. indica through BCF and its
relationship with water and sediment quality parameters.

2. Methods

Study Site. The first study site is the coastal area of
Tanjung Pasir village, in the Tangerang District, Banten
Province with a population of 8,053 inhabitants. The
topography is coastal plain and abrasion occurs due to
mangrove cutting for aquaculture ponds as large as 4.25
hectares. In 1998, the Tangerang sub-district had 254.98
hectares of mangrove; the mangrove forests have, to
date, been depleted. The Garapan river mouth in
Tanjung Pasir is used for boat docking, and is now
home to many industries such as textiles, metal
foundries, and speedboat manufacture as well as
housing, that potentially pollute the environment.

The second study site is the coastal area of Panimbang,
Pandeglang, administratively bordered by Serang
District in the North, the Indian Ocean in the South, and
the Sunda Strait in the West. There are five rivers in this
sub-district, the Cibungur river being the second biggest
river. Here, activity is mostly based on agriculture,
husbandry, and fisheries.Both location are showed at
Figure 1.

Field Sampling. Sampling was performed in July,
September, and October 2012. Sediment samples were
collected using a 3.5 l Ekman grab sampler. The top 23
cm of the sediment layer was collected using a plastic
spatula, and subsequently placed in the acid-washed
plastic bags and stored at 4 C during transportation to
the laboratory.

Collected samples of A. indica were rinsed with
seawater and kept in plastic bags for at least 12 h for
defecation. Sediment and A. indica samples were then
kept in a cooler box, transported to the laboratory, and
stored at 10 C until further analysis.

Analysis of heavy metals in sediments. Sequential
extraction procedures are available for characterizing
sediments [14], but it is well established that such
approaches do not remove metals selectively from
specific components of the sediments [15-20].
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Figure 1. Maps of Sampling Locations at Garapan (Above-Right) and Cibungur (Below-Right) River Mouths, Banten
Province, Indonesia (Banten Province Map from Agency for Geospatial Information, 2000)


Geochemical fractions of Cd, Cu, Pb, and Zn in
sediments were obtained by using the modified sequential
Extraction Technique [14]. The four fractions
considered, the extraction solutions, and the conditions
employed in this study were: 1) Easily, freely, leachable
or exchangeable (EFLE) (Fraction 1): About 10 g of
sample was continuously shaken for 3 h with 50 ml 1.0
M ammonium acetate, pH 7 at room temperature; 2)
Acid-reducible (Fraction 2): The residue from (1) was
continuously shaken for 3 h with 50 ml 0.25 M
hydroxyl-ammonium chloride acidified to pH 2 with
HCl, at room temperature; 3) Oxidizable-organic
(Fraction 3): The residue from (2) was first oxidized
with 15 ml hydrogen peroxide (30%) in a water bath at
80C. After cooling, the metal released from the organic
complexes was continuously shaken for 3 h with 50 ml
of 1.0 M ammonium acetate acidified to pH 2 with HCl,
at room temperature; 4) Resistant (Fraction 4): The
residue from (3) was digested in a 10 ml combination
(ratio of 3:1 of concentrated nitric acid and perchloric
acid). However, the EFLE fraction was used for
measurement of BCF since it is a better measure of
bioavailable metal forms and is considered to have the
most immediate effect on benthic organisms dwelling
on this sediment [21].

Analysis of heavy metals in A. indica. About 1 g of the
soft tissue of A. indica were thoroughly washed with
Milli-Q water and extracted for further processing. The
soft tissue was macerated into 12 cm clumps, dried at
7080 C, grinded, and stored until chemical analysis.
Cu, Pb, and Zn content was analyzed by digesting the
homogenized samples in a mixture of nitric and
perchloric acids. After centrifugation, the supernatant
was filtered through syringe filter paper (45 m) and
heavy metal concentration was determined for Cu, Pb,
and Zn by using an air-acetylene flame atomic absorption
spectrophotometer (Shimadzu Model 6300 series).

Water quality measurement. Temperature was measured
with a thermometer, pH with a Jenway pH meter, and
salinity levels with an Atago refracto-salinometer.

Organic content measurement. The sediment organic
content (C, S and N) was measured using a TrusPec
CNS Analyzer based on the LECO-USA procedure
[22]. Values were stated as percentage (%).

Data Analysis. Data were analyzed using t-test to
compare the two sites and non-parametric correlation
was used to observe the relationship between the BCF
of Cu, Pb, and Zn and water and sediment quality.

3. Results and Discussion

Environmental availability of metal refers to the ability
of a metal to interact with other environmental matrices
and undergo fate and transport processes [23-24]. It is
specific to the existing environmental conditions and is
a dynamic property, changing with the environmental
conditions. For example, the divalent Cu cation is
available for interaction with the gills of a sediment-
dwelling invertebrate, it can bind to dissolved organic
matter, and can undergo advective transport, whereas
Cu in the form of a sulfide in sediments cannot undergo
any of the above. Resuspension of sediments with
copper sulfide may introduce oxygen and result in the
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26
release of divalent Cu into the water column, making it
environmentally available.

As can be seen in Figure 2a, the temperature in
Garapan, Tanjung Pasir, was higher than in Cibungur,
Panimbang, due to the decomposition of organic matter.
Consequently, the pH was lowered. The lower the pH,
the more metals will dissolve. The Garapan river mouth
had higher heavy metal content compared to Cibungur.
Further, the Garapan river mouth had a lower salinity
compared to Cibungur; the lower the salinity, the easier
the release of metals. Hall (2002) showed that increased
salinity enhances the bioconcentration and bioaccumu-
lation rate of metals by decreasing their solubility [25].

In this study, the heavy metal content was higher in the
Garapan river mouth compared to the Cibungur river
mouth. However, the BCF values for all metals (Cu, Pb,
and Zn) was conversely related to heavy metal content,
meaning that the BCF in the Cibungur river mouth is
higher than in the Garapan river mouth (Figure 3). This
is probably because the content of organic matter in the
Garapan river mouth is higher than in the Cibungur
river mouth (Figure 2d). Several studies have shown
decreased bioavailability of total Hg where sediments
are rich in organic materials [26]. Di Toro et al. (2001)
stated that the amount of metal that binds is determined
by a competition for the biotic ligand and other aqueous
ligands, particularly dissolved organic matter [26]. Doig
and Liber (2006) found that at sub-lethal concentrations
of Hyalella azteca (500 g/l), the bioavailability of Ni
was significantly reduced in the presence of organic
matter/carbon [27].

In this study, the BCF of Cu in the Garapan river mouth
ranged from 0.320.49, while values for Pb and Zn were
0.130.18 and 2.573.61, respectively. In addition, the
BCF of Cu in the Cibungur river mouth ranged from
2.542.81, while values for Pb and Zn were 0.160.26
and 3.413.79, respectively.

According to Mountoris et al. (2002), BCF values of
over 1.2 indicate accumulation of heavy metals [10]. Pb
had the lowest BCF because Pb is non-essential element
and is not required by mollusks [28]. Moreover, the
BCF of metals in A. indica found in the Garapan river
mouth had the same pattern as those in the Cibungur
river mouth, namely Zn>Cu>Pb. Based on size class, it
can be stated that in the Garapan river mouth individual
with small size had higher BCF than individual with
medium and large ones for all metals (Cu, Pb, and Zn).
While in the Cibungur river mouth individual with small
size had higher BCF of Cu and Pb only, and for Zn,
individual with large size did.

Those can be explained that in clam Gafrarium
tumidum, small size tends to accumulate more than
large or medium ones [29]. Physiologically, metabolic

Figure 2. Average Values of Water Quality Parameters:
Temperature, pH, Salinity, and Organic
Content of Sediment at the Garapan (GRP) and
Cibungur (BNG) River Mouths



Figure 3. Bioconcentration Factor (BCF) of Heavy Metals
Cu, Pb, and Zn in A. indica According to Size
Class (Large, Medium, and Small)


rate decreases when age increases and this procees
varies among organisms [30]. The process above is
influenced by filtration rate, O
2
consumption, etc. [30-
31]. Increasing body size can also decrease
surface/volume ratio [29]. Another hypothesis is that
Makara Journal of Science 17/1 (2013) 23-28


27
uptake metal can be controlled by some bioavailable
ligands [32-33] like metallothioneins. Metallothioneins
or MTs known to be able to form a complex binding
with metal such as Hg, Ag, Cu, Zn, and Cd [34-35].
Previous studies reported that those ligands content
were depend on size. It could be abundant in small [36]
or large [34] size.

Based on the t-test, there were differences between
water quality (temperature, salinity, pH) and percentage
of organic matter (C, N, and S) in both locations (p
<0.01). There was a significant difference in BCF for
Cu (p <0.01), however, there were no significant
differences for Pb and Zn.

Non-parametric correlation analysis showed that there
was a significant negative correlation between the BCF
of Cu with percentage of N on medium sized A. indica
(correlation coefficient 0.732; p <0.05), and between
the BCF of Cu with percentage of S (correlation
coefficient 0.810; p <0.05). However, there was a
negative correlation between Cu with percentage of N
(correlation coefficient 0.786; p <0.05) on large size
and between the BCF of Pb and percentage of S
(correlation coefficient 0.862; p <0.01).

Further analysis showed that even though there was a
non-significant correlation between the BCF and C, N,
S percentage, those two variables showed an inverse
relationship. Hence, the higher the percentage of C, N,
or S, the smaller the BCF values.

4. Conclusions

Based on the above results, the BCF values of Cu, Pb,
and Zn in A. indica were higher when there was a low
concentration of organic matter in the sediment.
Meanwhile, the BCF values of Zn were higher than Cu
and Pb in both locations (Garapan and Cibungur river
mouths). Smaller sized A. indica tend to have higher
BCF values of Cu and Zn compared to the medium or
large sized mollusks.

Acknowledgements

The authors would like to thanks Universitas Indonesia
for scholarship on Doctoral Degree Program to NDT in
Marine Sciences at the Post Graduate School of Institut
Pertanian Bogor, Bogor, Indonesia.

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