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Water Air Soil Pollut (2009) 201:918

DOI 10.1007/s11270-008-9922-6

Gastropod Assemblages as Indicators of Sediment Metal


Contamination in Mangroves of Dumai, Sumatra, Indonesia
Bintal Amin & Ahmad Ismail & Aziz Arshad &
Chee Kong Yap & Mohd Salleh Kamarudin

Received: 17 July 2008 / Accepted: 4 November 2008 / Published online: 20 November 2008
# Springer Science + Business Media B.V. 2008

Abstract Impacts of heavy metal concentrations in complemented by significant negative correlations


sediments on the gastropod community structure were p<0.050.01) between concentrations of Cd, Cu, Pb,
assessed in the coastal waters of Dumai, Sumatra, Zn, and Ni in the sediments and gastropod abundance
Indonesia. The objective of this study was to relate and species richness. Among the metals analyzed, Cu
the levels of heavy metal pollution with the changes and Zn had strongest negative correlations with the
of gastropod community structure in the study area. gastropod diversity which suggests that these metals
Concentrations of Cd, Cu, Pb, Zn, Ni, and Fe in may be the most detrimental to gastropod populations
surface sediments collected from five sampling in the mangrove area of Dumai coastal waters.
stations were analyzed and correlated with the
abundance, species richness, and diversity of gastro- Keywords Heavy metals . Sediment contamination .
pod populations. Sediments at stations with more Gastropod . Community structure . Indonesia
anthropogenic activities accumulated higher concen-
trations of heavy metals and consequently displayed
lower abundances, lower species richness and diver- 1 Introduction
sity; while stations with lower heavy metal concen-
trations in sediments showed the opposite pattern in Macrobenthic invertebrate communities are important
gastropod community metrics. The above findings are in terms of biodiversity, ecosystem health and
comprise an important trophic component of detrital-
based estuarine food webs (Coull et al. 1995;
B. Amin : A. Ismail : A. Arshad : C. K. Yap MacFarlane and Booth 2001; Yap et al. 2003; Azrina
Department of Biology, Faculty of Science,
et al. 2006). Benthic communities are often exposed
Universiti Putra Malaysia UPM,
43400 Serdang, Selangor, Malaysia to effluent discharge from numerous anthropogenic
sources and subject to solid disposal wastes. Common
M. S. Kamarudin sources of contaminants in the coastal areas are urban
Department of Aquaculture Technology,
and agricultural runoff, industrial effluents, boating
Faculty of Agriculture, Universiti Putra Malaysia UPM,
43400 Serdang, Selangor, Malaysia and recreational uses, oil and chemical spills, and
dumping of pollutants (Harty 1997; Birch et al. 1998).
B. Amin (*) Heavy metals are usually effectively partitioned to the
Department of Marine Science, Faculty of Fisheries
estuarine intertidal sediments due to its high organic
and Marine Science, University of Riau,
Pekanbaru 28293, Indonesia content and pH (Luoma et al. 1990; Sadiq 1992).
e-mail: b_amin63@yahoo.com Elevated levels of heavy metals in sediments therefore
10 Water Air Soil Pollut (2009) 201:918

might potentially pose an ecotoxicological threat to 2 Materials and Methods


macrobenthic invertebrates. As potential indicators of
environmental stress, gastropod assemblages should Samples of sediments and gastropods were collected
exhibit changes in diversity and community structure from five stations along the intertidal zone of Dumai
through chronic and acute effects of sediment waters in the middle-east coast of Sumatra, Indonesia
contamination by heavy metals (Traunspurger and (Fig. 1). Three replicates of the top 5 cm of sediment
Drews 1996). samples at each station were collected during low tide
Dumai is one of the main gateways for marine from locations near gastropod transect plots and
transportation in the Straits of Malacca to Sumatra, placed in polyethylene plastic bags with a plastic
and like many other developing regions in Indonesia, spatula. Then, the samples of sediments were kept in
its coastal environment is subjected to negative an icebox, transported to the laboratory and stored at
impacts of industrial development and anthropogenic 10C until further analysis.
activities. It is also likely to receive impacts from the Sediment samples for heavy metal analysis were
Straits of Malacca which, according to Abdullah oven dried to constant dry weights at 80C, and the
et al. (1999) and Chua et al. (2000), is one of the samples passed through a 63-m stainless steel sieve.
busiest international shipping lanes in the world. The detailed processes for heavy metal analysis
Around 900 tankers and commercial vessels and 11 followed the procedures outlined by Ismail and Ramli
million barrels of oil flow past through the Straits of (1997) and Yap et al. (2002). Between 0.5 to 1.0 g of
Malacca waters everyday, averaging 70,000 ships the sediment were digested in a mixture of concen-
annually, 29% of which are super tankers passing the trated HNO3 (AnalaR grade, R&M 65%) and HClO4
straits. In addition, the volume of cargo transported (AnalaR grade, R&M 70%) in the ratio of 4:1. They
in both directions through the Malacca Straits has were placed in a hot-block digester at low temperature
increased substantially in the last two decades. The (40C) for 1 h and then fully digested at high
increasing marine traffic and shipping activities pose temperature (140C) for at least 3 h. The digested
an increasing threat of marine pollution to the straits samples were then diluted to a specified volume with
(Nontji 2004). double deionized water (USF Maxima, 18.2 MU
The relationships between the living organisms cm1). After filtration, heavy metals were determined
such as gastropod molluscs and the presence of for Cd, Cu, Pb, Zn, Ni, and Fe by using an air
pollutants such as heavy metals in their habitat where acetylene flame atomic absorption spectrophotometer
they lived are very interesting from ecotoxicological (AAS) Perkin-Elmer Model AAnalyst 800 series. The
point of view. Studies on macrobenthic communities data were presented in micrograms per gram dry
have shown that heavy metal concentrations in the weight, except for Fe in percent (%).
sediments correlate most strongly with the composi- All glassware and equipment used in heavy metal
tion of the biological communities and therefore the analysis were acid-washed with 10% HCl and then
most likely causal agents (Sommerfield et al. 1994; rinsed with double distilled water to avoid possible
Warwick, 2001; Mucha et al. 2005). Marine gastro- contamination. Multiple level calibration standards
pods meet most important requirements of the ideal were used to generate calibration curves against
biomonitor (Phillips 1990). They are abundant which sample concentrations were determined. The
throughout many coastal areas of the world, easy to percentages of recoveries for heavy metal analysis
identify and sample at all times of year, and can were between 96% and 103%. Procedural blanks and
tolerate wide ranges of contaminant concentration and quality control samples were made from standard
of physicochemical variables such as salinity (Langston solutions for Cd, Cu, Pb, Zn, Ni, and Fe. They were
and Spence 1995). No study has yet been reported on prepared from 1,000 mg/L stock solution (BDH
the value of using gastropod assemblages as bioindica- SpectrosoL) of each metal, and every five to ten
tors for Indonesian coastal waters. Therefore, the aim of samples reanalyzed in order to check for sample
this study was to determine whether relationships exist accuracy.
between gastropod community structure and heavy Gastropod samples were collected from transects
metal concentrations in mangrove sediments of Dumai aligned perpendicular to the beach from the highest
coastal waters, Sumatra, Indonesia. tide mark to the waters edge. Along the transect,
Water Air Soil Pollut (2009) 201:918 11
Fig. 1 Map of Dumai and
the sampling stations

P
s
three quadrats (1 m2) were placed on the substratum, 1963): H 0 ni
N log2 nNi ; where H=index of diversity;
i1
from which organisms were quantified. Three trans- ni =the number of individuals for each species; N=total
ects were employed for each of the stations where the number of individuals; pi=ni/N; s=total number of
distance between each transect was about 100 m. Five species, (2) Simpson dominance index (Simpson
Ps  2
stations were selected based on the suspected con- ni
1949): C N ; where C=dominance index; ni =
tamination gradients where higher metal concentra- i1
tions in sediments were reported at stations closed to number of individuals for each species; N=number of
Dumai city center (Amin et al. 2008a, b). total individuals; s=total number of species, (3)
Each transect was divided into three levels Evenness index (Pielou 1966): J logH
2s
; where J=
corresponding to lower (about 15 m above waterline index of species evenness; H=index of species
at the lowest tide), upper (about 15 m below the diversity; s=number of species.
highest water mark), and middle (between the two The Spearmans rank correlation was applied in
former ones). This technique is adapted from methods order to determine the strength and significance of the
outlined by Eleftheriou and Holme (1984), Krebs relationships between the concentrations of heavy
(1989), and Mudjiono et al. (1994). Samples of metals in sediments with the gastropod biodiversity
sediments (up to 5 cm) depth were sieved on site indices using SPSS version 15.
with a 1-mm mesh sieve to collect gastropods. The
organisms were preserved in labeled sample bottles
and fixed with 10% formalin in seawater. In the 3 Results
laboratory, the samples were sorted and transferred
into 70% alcohol for later identification and enumer- The mean values of physicochemical parameters in the
ation. Samples of gastropods were enumerated and study area are shown in Table 1. Salinities at Pelintung,
identified to the species level where possible. Identi- Sg. Dumai, and Sg. Mesjid were lower when compared
fications were based on Hayward and Rayland to other stations as these three stations were located
(1996), Plaziat (1984), and Dharma (1988). Addition- within the river estuary (Table 1). Also, transparency,
al environmental parameters measured at each station pH, and dissolved oxygen, as well as sediment pH, were
included pH, dissolved oxygen, salinity, temperature, lower at Pelintung and Sg. Dumai than other stations.
transparency, current speed, and sediment organic The highest mean percentage of organic matter was
matter. found in Bangsal Aceh and the lowest in Lubuk Gaung.
The following biodiversity indices were calculated: Higher abundances of gastropods were found in
(1) ShannonWiener index (Shannon and Wiever the middle part of the intertidal area of Pelintung, Sg.
12 Water Air Soil Pollut (2009) 201:918

Table 1 Mean water quality parameters at each station and water quality standard

Parameters Station Mean Standard men-LH/51/2004

Pelintung Sg. Dumai Sg. Mesjid Bangsal Aceh Lubuk Gaung

Current (m/s) 0.05 0.03 0.02 0.06 0.06 0.04


Temperature (C) 29.50 29.00 29.50 29.00 30.00 29.40 2832

Transparency 
(cm) 17.00 20.50 42.00 63.00 45.00 37.50
Salinity 0=00 23.00 24.50 25.00 28.00 28.00 25.70 Up to 34
pH (water) 5.50 6.50 7.00 8.00 8.50 7.10 78.5
pH (sediment) 4.50 5.00 6.50 6.00 5.50 5.50
DO (ppm) 4.00 4.20 5.50 4.40 4.60 4.54 5
Organic matter (%) 9.62 9.85 11.88 21.66 7.98 12.20

Dumai, and Sg. Mesjid), but abundances at Bangsal lowest was found at Sg. Dumai (C=0.78). In contrast
Aceh and Lubuk Gaung were higher in the lower to previous indices, higher dominance occurred at
intertidal area (Table 2). Higher gastropod species stations with more anthropogenic activities. The high-
richness occurred in the middle part of the intertidal est dominance index was found at Pelintung (C=0.59),
area (7.20 species), followed by the upper part (6.60 and the lowest was found at Lubuk Gaung (C=0.18).
species) and the lower part (5.00 species). The highest In general, as the concentrations of Cd, Cu, Pb, Zn,
number of gastropod species occurred at Bangsal Ni, and Fe increased, the abundance of gastropods
Aceh (15 species), and the lowest occurred at decreased, except for Fe (Table 3; Fig. 2). In
Pelintung (four species). Stations considered to have particular, from Fig. 2, Cd and Zn concentrations
better water quality (Sg. Mesjid, Bangsal Aceh, showed the strongest relationship (p<0.01), followed
Lubuk Gaung) also had higher numbers of species by Cu and Ni (p<0.05). Meanwhile, although Pb and
(1215 species) when compared to stations with Fe were correlated with gastropod abundances (neg-
poorer water quality (Pelintung and Sg. Dumai), with ative correlation for Pb and positive correlation for
only four to nine species. Fe), they were not significant (p>0.05).
The highest diversity index was found at Lubuk Negative relationships were also found between
Gaung, followed by Bangsal Aceh, and the lowest heavy metal concentrations in sediments with the
was found at Pelintung. Higher diversity (H values number of gastropod species (Fig. 3). Moreover, the
2.64 and 2.88, respectively) was noted at stations strongest negative relationships occurred for Cu and Ni
which had less anthropogenic activities further away (p<0.01), followed by Pb and Zn (p<0.05). Cd was
from the Dumai city center (Bangsal Aceh and Lubuk also negatively correlated, while Fe was uncorrelated
Gaung) compared to diversity values at stations with with the number of gastropod species (p>0.05).
more anthropogenic activities (Pelintung, Sg. Dumai, In general, as the concentrations of Cd, Cu, Pb, Zn,
and Sg. Mesjid), which had H values of 0.93; 1.54, and Ni increased, species diversity decreased. Cu
and 1.98, respectively. Evenness values showed a showed the strongest negative relationship with
similar trend to that in diversity, in which the highest diversity (p<0.01), followed by Zn (p<0.05), Cd,
value was found at Bangsal Aceh (C=0.86), and the Pb, Ni, and Fe; which were not statistically significant

Table 2 Abundance (ind/m2) of gastropod at each station and sampling site

Sampling site Station

Pelintung Sg. Dumai Sg. Mesjid Bangsal Aceh Lubuk Gaung

Lower 6 11 28 59 51
Middle 12 57 47 55 41
Upper 8 20 38 47 35
Mean 9 29 38 53 42
Water Air Soil Pollut (2009) 201:918 13

Table 3 Heavy metal concentrations (g/g) in sediments, number of species, abundance, and biodiversity indices of gastropod at each
station

Station Cd Cu Pb Zn Ni Fe Number of Gastropod Diversity Index Evenness


Gastropod Abundance (H) Dominance (C) (J)
species (ind/m2)

Pelintung 1.31 10.55 37.39 75.26 17.38 2.91 4 9 0.93 0.59 0.79
Sg. Dumai 0.90 8.62 28.19 55.98 11.14 3.01 9 29 1.54 0.44 0.78
Sg. Mesjid 0.92 5.32 30.59 48.11 9.15 3.06 12 38 1.98 0.30 0.82
Bangsal Aceh 0.64 3.64 28.45 41.55 8.76 2.93 15 53 2.64 0.17 0.86
LubukGaung 0.81 3.84 26.25 47.17 8.98 2.94 13 42 2.88 0.18 0.85

(p>0.05). Negative relationships also occurred be- Gaung were slightly better than those at stations
tween heavy metal concentrations in sediments and closed to the Dumai city center, where more indus-
the evenness index. However, only Cu showed a tries and other anthropogenic activities are concen-
strong negative relationship (p<0.05). In contrast to trated. High percentage of total organic matter in
the other diversity matrices, concentrations of heavy Bangsal Aceh might be attributed to the mangrove
metals in sediments were inversely related to the forest and finer sediment in this area as well as inputs
dominance index (Fig. 4). from agricultural runoff through some streams.
Meanwhile, the low percentage of organic matter in
Lubuk Gaung was due to the sandy sediment
4 Discussion substrate and less anthropogenic activities. Ironically,
sediment contamination levels were counter to levels
Generally, all the parameters measured in the present of sediment organic content at these stations.
study were still within the tolerable levels for the Lower abundances of gastropods at stations Pel-
coastal aquatic organisms set by The Ministry of intung and Sg. Dumai might be attributed to the
Environment of Indonesia (Men 2004) (Table 1). The relatively lower quality of physicochemical parame-
water quality parameters at Bangsal Aceh and Lubuk ters at these stations which were not statistically

Fig. 2 Correlation between 60 60


y= -1.25x 101.36
metal concentrations in sed- 50 66.27x 9 9 50 (r= -0.985; p 0.01)
0973 p 0.01)
iment with gastropods 40 40
abundance in Dumai 30 30
20 20
10 10
0 0
0.40 0.60 0.80 1.00 1.20 1.40 30.00 40.00 50.00 60.00 70.00 80.00
Cd concentration in sediment (g/g) Zn concentration in sediment (g/g)

60 60 -4.30x 81.95
-5.17x 67.30
50 -0.950;p 0.05) 50 -0.940; p 0.05)
40 40
30 30
20 20
10 10
0 0
2.00 4.00 6.00 8.00 10.00 12.00 5.00 10.00 15.00 20.00
Cu concentration in sediment (g/g) Ni concentration in sediment (g/g)

60 60 40.74x - 86.77
-3.19x 130.40
50 50 0.159; p 0.05)
-0.817;p 0.05)
40 40
30 30
20 20
10 10
0 0
25.00 30.00 35.00 40.00 2.85 2.90 2.95 3.00 3.05 3.10
Pb concentration in sediment (g/g) Fe concentration in sediment (g/g)
14 Water Air Soil Pollut (2009) 201:918
Fig. 3 Correlation between 16 16
metal concentrations in sed- 14 14 0.05)
12 12
iment with number of gas- 10 10
tropods species in Dumai 8 8
6 6
4 4
2 2
0 0
0.4 0.6 0.8 1 1.2 1.4 30 40 50 60 70 80
Cd concentration in sediment (g/g) Zn concentration in sediment (g/g)

16 16
19.19
14 -0.961; 14
12 12
10 10
8 8
6 6
4 4
2 2
0 0
2 4 6 8 10 12 6 8 10 14 14 16 18 20
Cu concentration in sediment (g/g) Ni concentration in sediment (g/g)

16 16
14 14
12 12
10 10
8 8
6 6
4 4
2 2
0 0
20 25 30 35 40 2.85 2.9 2.95 3 3.05 3.1
Pb concentration in sediment (g/g) Fe concentration in sediment (g/g)

significant. Benthic communities have been frequent- gastropod community structure in the study area.
ly employed in environmental monitoring and assess- Clements (1991) explained that metal-impacted ben-
ment of heavy metal and organic contaminants in thic communities are generally characterized by
estuaries, and often demonstrate changes in macro- reduced abundance, lower species diversity, and shifts
benthic community structure and composition in in community composition from sensitive to tolerant
response to pollutant impacts (Gray et al. 1990; taxa. According to Reynoldson (1987), the most
Warwick, 1993). Stark (1998) found correlations obvious impact of contaminated sediments to marine
between concentrations of heavy metals and the benthic invertebrates was direct acute toxicity causing
patterns of benthic assemblages in polluted and the death of organisms. Warwick (1993) also men-
unpolluted areas in estuaries in the Sydney region tioned that macrobenthic invertebrates are in direct
Australia. Ward and Hutchings (1996) also found and continual contact with sediments and are rela-
characteristic patterns in species related to a strong tively immobile. Consequently, they often possess a
pollution gradient comprising a variety of heavy limited capacity to evade pollutant impacts.
metals in various habitats around Port Pirrie, South Stations with higher metal concentrations in the
Australia. Morrisey et al. (1996) also found changes sediments such as Pelintung and Sg. Dumai exhibited
in the abundances and taxonomic composition of lower evenness (J 0.780.79) when compared to
fauna in Cu-treated sediments under field conditions stations with lower metal concentrations in the sedi-
in Botany Bay, Australia. ments such as Bangsal Aceh and Lubuk Gaung
According to Teles (1994), diversity indices give (e 0.850.86). Numerous studies have identified that
better information on the environmental conditions community dissimilarities at the species level are
under which the organisms lived than a consideration highest in polluted areas or areas in which environ-
of individual taxa alone. Pett (1974) mentioned that mental change was marked (Warwick 1988). A marked
the diversity indices are also suitable for addressing decrease in evenness could be regarded as a symptom
any question that a heterogeneity index can answer. of pollution (Warwick 2001). Yap et al. (2003) also
The strong negative correlations (p<0.01) between reported higher biodiversity indices in the unpolluted
the Cd, Cu, Zn, and Ni concentrations in sediments upstream portion of Sg. Semenyih (Malaysia) than in
with the numbers of gastropod species and gastropod the polluted downstream portion receiving domestic
abundances suggest that these metals affected the effluents. Weaker correlations between species diver-
Water Air Soil Pollut (2009) 201:918 15

4.57
p 0.05)

p 0.05)

15

p 0.05) p 0.05)

Fig. 4 Correlation between Cd, Cu, Pb Zn, Ni, and Fe concentrations in sediment with H, C, and J values of gastropod from Dumai
coastal waters

sity and environmental pollution are found in less studies and is expressed by the community diversity
disturbed areas indicating commensurate changes in (Shannon and Wiever 1963). In polluted environ-
faunal patterns with the severity of pollution (Olsgard ments, dominance by a low number of species
et al. 1998). produces low values of a typical species diversity
Analysis of the distribution and abundance of index. Conversely, environments composed of a large
benthic organisms is routinely used in biomonitoring number of species with evenly distributed abundances
16 Water Air Soil Pollut (2009) 201:918

produce large diversity index values. Diversity index Among the metals analyzed, Cu and Zn had strongest
values less than 1.0 have been reported from polluted negative correlations with the species diversity index
waters (Wilhm and Doris 1968), and values above 3.0 which may suggest that these metals are the most
have been reported from oligotrophic waters (Ransom detrimental metals in the bottom sediments to
and Doris 1972). In the present study, the stations gastropod populations in the study area. It is,
with relatively higher heavy metal concentrations, therefore, important for the local authority to imple-
such as Pelintung had lower diversity (H: 0.93) and ment and enforce an appropriate strategy to monitor
higher dominance (C 0.59) of gastropods when and routinely control the pollutant discharges in order
compared to stations with lower heavy metal concen- to save the biodiversity of Dumai coastal waters from
trations, such as Bangsal Aceh, which had high more serious degradation in the future. Gastropod
diversity (H 2.64) and low dominance (C 0.17). assemblage status may provide an effective ecosys-
These findings are in agreement with Gray et al. tem-based management indicator for this purpose.
(1990), Clements (1991), Rakocinski et al. (2000),
Bu-Olayan and Thomas (2005), Medina et al. (2005), Acknowledgement The authors thank anonymous referees
for their critical reading, valuable suggestions, and corrections
and Mucha et al. (2005) who noted that high species of the original manuscript.
diversity was usually associated with unimpacted or
unpolluted conditions, while lower species diversity
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