Regional Studies in Marine Science 16 (2017) 49–55

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Regional Studies in Marine Science

journal homepage: www.elsevier.com/locate/rsma

Biomagnification of total mercury in the mangrove lagoon foodweb in

east coast of Peninsula, Malaysia
Dung Quang Le a, *, Kentaro Tanaka b , Luu Viet Dung c , Yin Fui Siau a , Liam Lachs a ,
Siti TafzilMeriam Sheikh Abdul Kadir a , Yuji Sano b , Kotaro Shirai b
a
Institute of Oceanography and Environment, Universiti Malaysia Terengganu, 21030 Kuala Terengganu, Terengganu, Malaysia
b
Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5, Kashiwanoha, Kashiwa-shi, Chiba 277-8564, Japan
c
VNU Key Laboratory of Geoenvironment and Climate change Response, Vietnam National University, Hanoi, 334 Nguyen Trai, Thanh Xuan, Hanoi,
Viet Nam

article info a b s t r a c t
Article history: The combined analyses of total mercury (Hg) and stable isotopic (δ 13 C and δ 15 N) ratios were conducted
Received 18 October 2016 to describe the food web pathways of dietary Hg, from basal food sources to benthic invertebrates and
Received in revised form 30 July 2017
higher trophic level fish, and to determine if biomagnification of Hg is a persistent process in the food
Accepted 7 August 2017
Available online 12 August 2017
web in a mangrove creek in Setiu Lagoon. The study showed that Hg concentrations were relatively low
in mangrove litter and sediment, but elevated gradually in higher trophic level consumers. Based on δ 13 C
Keywords: values, the variation of gastropod Hg concentrations are likely correspond with local dietary sources of Hg
Mercury in sediments, while variations in bivalve Hg reflect their exposure to low Hg concentrations in the water
Biotransfer body. The combination of depleted δ 13 C values and high Hg concentration in gastropods suggest that
Stable isotope microbially produced Hg sources in mangrove sediments play an important role in benthic biotransfer
Health risk pathways. The isotopic compositions of crustaceans demonstrate the importance of feeding behaviour
Mangrove in Hg bioaccumulation. High bioaccumulation of Hg occurred consistently in carnivorous fish species,
Food web particularly piscivorous Caranx ignobilis. The enriched δ 13 C of fish species reflects a small contribution
of mangrove-derived organic carbon to the fish food web in the mangrove creek, accordingly the fish
community may intake dietary sources of Hg via trophic relay or bioadvection, however further studies are
needed to elucidate such factors. A positive relationship was found between Hg concentration and trophic
level (derived from δ 15 N, trophic magnification factor of 1.5) even at low Hg concentration in the base of
the food web, providing evidence for Hg biomagnification in the mangrove food web of Setiu lagoon.
Whilst Hg concentrations in fish and commercial crabs did not present a risk for human consumption, the
Hg concentration of Caranx ignobilis approached the official permitted level. In the future, there is a need
for Hg biomonitoring designed to assess carnivorous fish in order to comprehensively assess the potential
effects of human activities and land use around the upper reaches of the Setiu ecosystem.
© 2017 Elsevier B.V. All rights reserved.

1. Introduction Hg bioaccumulation has given rise to extensive surveys of Hg con-

Mercury (Hg) is a potentially toxic metal when released into the
environment by natural or anthropogenic sources. Atmospheric
deposition is among the main routes by which Hg enters aquatic
ecosystems (US EPA, 1997). Recently, the Hg emission from com-
bustion of industrial and municipal solid waste has been of great
concern, and because of long-range atmospheric transport and
deposition, elevated levels of Hg are being observed even in remote
areas and pristine habitats (Chen et al., 2013; Wiedinmyer et al.,
2014; Fitzgerald et al., 1998). The toxicological concern regarding
* Corresponding author.
E-mail addresses: le.dung@umt.edu.my, lqdungimer@gmail.com (D.Q. Le).
centrations and speciation in ecosystems, particularly mangrove
wetlands (Al-Reasi et al., 2007; Lavoie et al., 2013). Though man-
grove wetlands act as important nurseries and support biodiversity
and aquatic productivity, they also provide ideal conditions for the
microbial conversion of inorganic Hg into methylmercury, one of
the most toxic forms of Hg, in enriched dissolved organic matters
and anoxic sediments (Hall et al., 2008). Another source of Hg in
mangroves may derive from litter-fall due to the ability of plants to
absorb atmospheric Hg to their tissues (Fleck et al., 1999). Although
plant litter is an important food source for invertebrates and some
fish species in the mangrove (Bouillon et al., 2003; Nyunja et al.,
2009), through decomposition it is also considered a major source
of mercury (Hg) flux to the mangrove forest food web (Ding et al.,
2011). The trophic route is considered to be the main Hg uptake

http://dx.doi.org/10.1016/j.rsma.2017.08.006
2352-4855/© 2017 Elsevier B.V. All rights reserved.
50 D.Q. Le et al. / Regional Studies in Marine Science 16 (2017) 49–55
Fig. 1. The sampling area from Setiu lagoon.
pathway in apex animals and even humans (Hall et al., 1997;
Campbell et al., 2003; Lavoie et al., 2013). Even at low aquatic con-
centrations of Hg, biomagnification has been consistently observed
in freshwater and marine food webs (Lavoie et al., 2010, 2013;
Kehrig et al., 2001; Edwards et al., 1999).
The analysis of dual stable isotope ratios (δ 15 N and δ 13 C) can be
used as proxies for constructing food webs. The advantage of stable
isotope analysis is to provide information on feeding relationships
and trophic levels. Carbon isotope ratios (δ 13 C) are used to track
dietary sources for consumers. Since trophic fractionation of car-
bon ranges, on average, from 0.0h to 1.3h between consecutive
trophic levels, the value of δ 13 C in consumer tissue tends to mir-
ror that of lower trophic level organisms in the vegetation-based
habitats (photosynthetic pathways, C3 vs. C4 plants) wherein they
have grown (Post, 2002). Nitrogen isotope ratios (δ 15 N) can be
used to estimate the trophic level because the stepwise enrichment
of δ 15 N ranges, on average, from 2.0h to 3.5h between each
trophic transfer (Fry and Sherr, 1984; Post, 2002). Accordingly, the
combined analyses of Hg and stable isotopes can elucidate dietary
exposure and biomagnification of Hg in the mangrove food web,
and hence provide a tool of integral importance to ecological risk
assessments.
The study was conducted in Setiu Lagoon, an aquatic ecosystem
surrounded by 154 ha of mangrove forest, which is dominated
by Rhizophora sp., Avicennia sp., and Nypa sp. Invertebrate and
juvenile fish are abundant in the lagoon and are an important
natural resource for local people and their livelihoods. Mangrove
wetlands are vulnerable to the impacts of Hg contamination, and
recently potential risks of environmental contaminations in the
Setiu lagoon system have been emphasised due to the increasing
activities of local artisan mining and agriculture including palm oil
plantations in the upper zone of the lagoon (Suratman and Latif,
2015). Sultan and Shazili (2010) detected high concentrations of
various heavy metals in sediment from a lake and river in the upper
reach of the region. Furthermore, Agusa et al. (2005) found high Hg
concentrations in bigeye scad (Selar crumenophthalmus) collected
on the east coast of Peninsular Malaysia, even though there is less
human activity on the east coast compared to the west coast. There
is insufficient data on Hg concentrations in estuarine and coastal
areas of the east coast. Such data would help to delineate spatial
connectivity of Hg contamination between these locations and
aid in comprehending the mechanism of Hg biotransfer through
feeding linkages.
The objective of this study is to describe the links of trophic
Hg exchange and exposure and to determine the extent of Hg
biomagnification in the mangrove food web of Setiu Lagoon.
2. Materials and methods
2.1. Sampling
Surveys were conducted during three days in June and July
2015 at the mangrove creek in Setiu Lagoon. Samples collected
along the creek include mangrove leaves (Rhizophora spp.), sed-
iment organic matter (SOMs), benthic invertebrates (gastropods,
bivalves, and crustaceans) and fish (Fig. 1). Fresh and senescent
mangrove leaves were collected by hand from the trees and the
sediment surface, respectively. SOMs were collected in the upper
10 mm of surface sediment during low tide at the mangrove edge
and the mangrove interior. There were different sediment types
between sites; mangrove interior was under vegetative cover and
sediment on the surface was muddy, whereas mangrove edge
sediment was composed of a superficial layer (1 cm) of sandy-
mud overlying coarse sand. Benthic invertebrate specimens were
manually collected during low tide at the mangrove edge and
interior and include gastropod and sesarmid crabs (Table 1). While
mangrove oysters were taken from prop roots of Rhizophora sp., the
hard clams, Meretrix lyrata, were collected at the tidal creek. Mud
crabs, Scylla olivera, and Thalamita crenata were obtained using bait
trap on the mangrove floor at high tide. Traps contained chicken
heads as bait and were deployed for 8–12 h. Fish samples were
obtained in traps and gill nets (2 cm mesh size, 40 m long and 2 m
depth). The gill nets were deployed at the mangrove edge. Fish total
length and wet weight were measured. Similar size of individuals
for each fish and invertebrate species were selected for analysis
to reduce the influence of size on Hg content, feeding habits and
trophic position. All samples were packed in labelled polyethylene
bags and immediately kept in a cool box, transported to the field
laboratory, washed and frozen at −20 ◦ C for further processing.
2.2. Sample preparation
In the laboratory, mangrove leaves were washed gently with
distilled water and observed under a stereo microscope to remove
any residuals of sediments or epiphytes. Before drying, the samples
were rinsed again with deionised water (Millipore Corporation,
USA). Muscle tissue of gastropods and bivalves were carefully
removed from their shells. Small invertebrates were pooled with
3–20 individuals per sample to ensure enough material for iso-
topic and Hg analysis. For large crab species, carapace length and
body weight were recorded and muscle tissue was taken from the
chelae. Fish were dissected and white dorsal muscle tissue was
taken for further analyses. All samples were dried at 60 ◦ C until
weight was constant before grinding to a fine powder with mortar
and pestle. For δ 13 C and elemental (C: N) analysis, invertebrate
samples were treated with HCl 10% (Fisher Scientific) to remove
 D.Q. Le et al. / Regional Studies in Marine Science 16 (2017) 49–55 51

Table 1
Stable isotope composition, trophic levels and Hg concentrations from the mangrove food web in Setiu lagoon.
Content n Total length (cm) Body weight (g) Hg levels Mean ± SD (h) TL Feedingb
mg/kg dwt. mg/kg wwt. a
δ N
15
δ C13

Mangrove leaves 6 0.04 ± 0.01 3.6 ± 0.3 −29.5 ± 1.1

Sediments
Mangrove interior 2 0.06 ± 0.01 2.7 ± 0.4 −25.8 ± 0.5
Mangrove edge 2 0.05 ± 0.01 3.5 ± 0.4 −24.6 ± 0.3
Crustacea
Perisesarma sp. 3 0.12 ± 0.04 0.03 5.4 ± 0.2 −25.7 ± 0.8 2.1 BE, DF
Thalamita crenata 3 6.4 ± 0.6 38.9 ± 2.1 0.37 ± 0.03 0.07 8.3 ± 0.5 −20.2 ± 0.9 3.4 BE, PR
Scylla olivera 3 9.0 ± 0.5 128.7 ± 26.0 0.41 ± 0.1 0.08 8.2 ± 0.5 −22.4 ± 1.2 3.4 BE, PR
Bivalve
Crassostrea sp. 2 0.09 ± 0.02 0.02 6.0 ± 0.3 −22.2 ± 1.3 2.4 BP, FF
Meretrix lyrata 3 0.11 ± 0.03 0.02 6.6 ± 0.0 −21.4 ± 0.1 2.6 BP, FF
Gastropod
Cerithium coralium 2 0.11 ± 0.03 0.03 4.7 ± 0.3 −19.0 ± 0.5 1.8 BE, DF
Faunus ater 3 0.15 ± 0.02 0.08 5.8 ± 0.4 −22.5 ± 0.2 2.3 BE, GR
Cerithidea quadrata 3 0.37 ± 0.01 0.03 5.0 ± 0.1 −25.2 ± 0.1 1.9 BE, GR
Littoraria carinifera 1 0.41 0.07 4.9 ± 0.4 −24.8 ± 1.2 1.9 BE, GR
Fish
Ambassis interrupta 3 8.9 ± 0.5 10.2 ± 0.8 0.37 ± 0.03 0.08 10.1 ± 0.6 −19.8 ± 0.4 3.4 PB, PR
Epinephelus bleekeri 3 15.5 ± 5.8 64.6 ± 70.8 0.43 ± 0.35 0.11 9.7 ± 0.5 −18.9 ± 0.6 3.3 BE, PR
Ophiocara porocephala 2 15.1 ± 3.5 29.7 ± 3.0 0.41 ± 0.19 0.08 8.1 ± 0.6 −23.2 ± 0.8 2.8 BE, PR
Caranx ignobilis 4 16.0 ± 0.6 55.8 ± 3.6 2.01 ± 0.82 0.40 10.2 ± 0.3 −21.6 ± 0.6 3.5 PB, PR
Megalops cyprinoides 2 27.4 ± 5.3 159.2 ± 64.7 0.47 ± 0.05 0.09 10.9 ± 1.1 −20.7 ± 1.1 3.7 PB, PR
Toxotes jaculatrix 4 13.8 ± 0.5 52.6 ± 6.5 1.40 ± 0.56 0.27 9.0 ± 0.6 −22.1 ± 1.3 3.1 PB, PE, PR
Netuma thalassina 2 19.0 ± 0.2 67.0 ± 11.6 1.47 ± 0.31 0.29 10.9 ± 0.7 −18.6 ± 1.2 3.7 PB, PR
Terapon jarbua 1 11.9 22.6 0.32 0.06 9.8 −18.4 3.3 PB, OM
Gerres limbustus 2 9.4 ± 0.1 12.9 ± 0.8 0.30 ± 0.07 0.06 10.2 ± 0.1 −20.5 ± 0.5 3.5 PB, OM
Moolgarda perusii 2 11.3 ± 2.1 23.4 ± 16.2 0.09 ± 0.01 0.02 5.5 ± 0.7 −19.8 ± 0.6 2.0 PB, HE
Bold numbers: high Hg concentration in fish tissue approached the permitted level; TL: trophic level.
a
Converted mean of Hg levels from dry weight to wet weight.
b
Feeding habitat: PE = pelagic; BE = benthic; PB = benthopelagic, feeding mode: FF = filter-feeder; PR = predator; OM = omnivore; HE = herbivore; GR = grazer; DF =
detritus-feeder.

12

10

0
-32 -30 -28 -26 -24 -22 -20 -18

Fig. 2. Stable isotope compositions of primary producers and consumers from the mangrove creek of Setiu lagoon.

carbonates and re-dried until weight was constant. C: N ratios in U.K.) connected with a combustion device (vario MICRO cube,
fish and crab tissues ranged from 2.4–3.1 and thus, lipid correction elementar, Germany) at the Atmosphere and Ocean Research In-
was not performed. stitute, University of Tokyo, Japan. Stable isotope compositions are
expressed as δ values, which are measured as the ratio of heavy
2.3. Measurement of Hg and stable isotope ratios to light isotopes in a sample relative to a known standard, by the
following equation:
Stable isotope ratios (δ 13 C and δ 15 N) were measured using a
[( ) ]
Rsample
stable isotope ratio mass spectrometer (IsoPrime100, IsoPrime,
δ X (h) = − 1 × 1000 (1)
Rstandard
52 D.Q. Le et al. / Regional Studies in Marine Science 16 (2017) 49–55
where X is the isotope value in permil (h) and R is the ratio of
the heavy to the light isotope for both the sample (Rsample ) and the
standards (Rstandard ), international reference materials namely air
(N2 ) for δ 15 N and PeeDee belemnite for δ 13 C.
The sample output was calibrated to δ values, using the trace-
able standards, ammonium sulphate (IAEA-N-1) for δ 15 N (0.4h)
and sucrose (IAEA-CH-6) for δ 13 C (−10.5h). The standard ref-
erence material, NIST-SRM2976 (National Institute of Standards
and Technology, USA), was analysed for monitoring instrumental
condition during the course of the analysis. The error of the analysis
was estimated from the reproducibility of the SRM2976, and the
values were 0.05h and 0.02h for δ 13 C and δ 15 N, respectively.
The mercury concentrations of sub-powder samples were de-
termined with a cold vapour atomic absorption spectrometer (MA-
3000, Nippon Instruments Corp., Japan) with a detection limit for
MA3000 of 0.0002 mg/kg. The accuracy of the method was also
assessed with NIST-SRM2976 and recoveries of Hg ranged from
105%–110%.
2.4. Calculations and statistical analysis
Due to variability of baseline δ 15 N between pelagic and ben-
thic zones (bivalves and gastropods) within the mangrove creek,
trophic levels (TL) are determined using equation reported in Jar-
dine et al. (2006):
TL = 2 + δ 15 Norganisms − δ 15 Np × Pp + δ 15 Nb
{ [
/115N.
( )]}
× 1 − Pp
TL is the trophic level of the organism; δ 15 Norganisms is average δ 15 N
of consumers; δ 15 Np and δ 15 Nb are stable nitrogen isotope ratios
of primary consumers from pelagic and benthic habitats, respec-
tively; 115N is the isotopic enrichment factor for invertebrate
(2.2h) and fish (3.4h) (Post, 2002; McCutchan et al., 2003).
The proportion of the pelagic food source (Pp ) was assumed
to be equal to the δ 13 C values of seston, which were analysed in
the same area (Le et al., 2017); δ 13 Corganisms is the average δ 13 C
of consumers; δ 13 Cp and δ 13 Cb are the baseline carbon isotope
ratios for pelagic and benthic sources, respectively. The baseline
of the pelagic food source is the average δ 13 C values of 2 bivalve
species, while the baseline of the benthic food source is the average
δ 13 C values of the gastropods Cerithium coralium and Littoraria
carinifera, which we assumed to occupy TL 2 as primary consumers.
Pp = δ 13 Corganisms − δ 13 Cb δ 13 Cp − δ 13 Cb .
( )( )
The biomagnification factor of Hg was determined for the entire
food web based on the relationship of full data between trophic
levels and Hg concentrations using simple linear regression:
Log10 [Hg] = a δ 15 N + c ,
( )
where c is an intercept and a is the slope for biomagnification
power of Hg. The slope of Eq. (4) was used to calculate the trophic
biomagnification factor (TMF) as follows:
TMF = 10a .
Results are expressed as mean ± SD. One-way ANOVA was per-
formed to reveal any significant differences in metal concentra-
tions among groups. Simple linear regressions between log10 -
transformed metal concentrations in taxa and their trophic level
(using δ 15 N) were run to evaluate the potential for contaminant
biomagnification in the lagoon food web. Statistical analyses were
performed using IBM SPSS Statistics 22, Release 22.0.0.0.
3. Result and discussion
3.1. Total Hg concentrations and trophic routes
3.1.1. Basal food web members
Concentrations of Hg determined in surface sediments, man-
grove litter, nine benthic invertebrate species and ten fish species
ranged between 0.04 ± 0.01 and 2.01 ± 0.82 mg/kg dry weight
(Table 1). The lowest Hg concentrations were found in mangrove
litter (0.04 mg/kg DW) and sediments (0.05 and 0.06 mg/kg DW at
the mangrove edge and interior, respectively) at the base of food
web. The Hg concentrations in sediment were comparable with
background concentrations (Buchman, 2008). There was no signifi-
cant difference between mean Hg concentrations in sediments the
mangrove interior and edge; the difference was likely due to Hg
speciation. Because the sediment at the mangrove edge was sandy-
mud, it contained less total organic carbon than the mangrove in-
terior, which had less ideal conditions for MeHg formation through
microbial activity (Oliveira et al., 2015). Lower MeHg formation has
been recorded in subtidal sandy sediments in uncovered mangrove
areas compared to muddy sediments in covered mangrove areas
(Oliveira et al., 2015). Further investigation will be needed to clarify
the role of Hg species in sediment on a large-scale.
The mean Hg concentration in mangrove litter was relatively
lower than that described by Ding et al. (2011), but was comparable
with other terrestrial plants in less polluted areas (Moore et al.,
1995). Thus, Hg concentration in mangrove leaves due to depo-
sition of atmospheric Hg is likely to be negligible. Hg residue in
leaves was mainly inorganic and could be methylated into organic
(2) Hg by microorganisms such as sulphate reducing bacteria in the
rhizosphere of mangrove roots and decaying litter in the superficial
(0–2 cm depth) layer of sediment (Oliveira et al., 2015). Therefore,
mangrove leaves were likely to contribute a portion of the total
Hg source in sediment under mangrove cover (Ding et al., 2011).
Correia and Guimarães (2016) also found that mercury methyla-
tion was significantly higher in the root region than in the tidal
flat. Thus, organic Hg formed in mangrove sediments may be an
important Hg source to benthic infauna, consequently resulting in
the biomagnification of Hg in mangrove food web (Morel et al.,
1998; Chen et al., 2008). Additionally, due to the difference of car-
bon isotopic signature between mangrove litter and SOMs, these
carbon sources can be considered as end-members at the base of
mangrove food web, in which low δ 13 C values in mangrove litter
(−30.1 ± 1.1h) are indicative of terrestrial C3-plants (Lamb et al.,
2006). The δ 13 C values of SOMs ranged from −25.8 to −24.6h at
the mangrove interior and edge, respectively (Fig. 2). The relatively
(3) higher δ 13 C value of SOMs at the edge compared to the interior
might reflect the contribution of autochthonous and allochthonous
carbon sources (Bouillon et al., 2003).
3.1.2. Bivalves and gastropods
The Hg concentrations in benthic invertebrates were signifi-
(4)
cantly higher than those at the base of the food web (P<0.001),
ranging from 0.09 to 0.41 mg/kg DW. For bivalves, both filter-
feeding species at similar trophic levels showed identically low
Hg concentrations, which might reflect low Hg exposure from the
water body. The stable isotopic signature of these species showed
(5) relatively similar ranges (6.0 ± 0.3h and 6.8 ± 0.0h for δ 15 N,
and −22.2 ± 1.3h and −21.4 ± 0.1h for δ 13 C) (Fig. 2), indicating
the same dietary Hg uptake (phytoplankton or organic matters)
from the water body. Unlike bivalves, the mean Hg concentra-
tions in gastropods varied relative to their habitat use and local
dietary Hg sources rather than to trophic levels in the food web.
Both Cerithidea quadrata and Littoraria carinifera grazing on inte-
rior mangrove sediment showed relatively high Hg concentration,
whereas Cerithium coralium and Faunus ater feeding on surface
 D.Q. Le et al. / Regional Studies in Marine Science 16 (2017) 49–55
sediment at the mangrove edge (mangrove uncovered area) pre-
sented low Hg concentrations. The spatial difference in gastropod
Hg concentrations between these areas may relate to Hg forms
in sediment, as explained above, because organic mercury readily
bioaccumulates and has a long biological half-life in organisms.
The slow elimination of organic Hg also played a role in the ele-
vated concentrations of Hg in organisms (Tsui and Wang, 2004).
Meanwhile, the stable isotopic signatures of gastropods supports
the evidence that food sources differ between the areas. Indeed,
main food sources for C. quadrata and L. carinifera, which show
the most negative δ 13 C value among gastropod species (−25.2
h and −24.8h, respectively), are derived from mangrove litter
and SOMs inside mangrove (Fig. 2). Conversely, C. coralium, with
more positive δ 13 C values of −19.0 ± 0.3h, relies on a mixture
of SOMs at mangrove edge and allochthonous carbon sources. F.
ater showed a moderate isotopic signature (−22.5 ± 0.2h) among
gastropod species, suggesting a mix of carbon sources from in-
side and outside of the mangrove (Fig. 2). By comparing bivalves
(pelagic-feeders) and gastropods (benthic-feeders), it is clear that
bioaccumulation of Hg was lower in pelagic sources than benthic
sources (P<0.001), suggesting that water has less bioavailable Hg
than sediment sources, however further investigations are needed
to elucidate evidence for this.
3.1.3. Crustaceans
Variability of Hg concentrations among crustacean species may
relate to both diet source and trophic level. Sesarmid crabs are
known to consume litter-fall (Thongtham and Kristensen, 2005),
this study has shown that their main diet is mangrove leaves and
detritus since the δ 13 C value of crabs (−25.7 ± 0.8h) reflects that
of mangrove-derived carbon sources. Furthermore, the δ 15 N value
(5.4 ± 0.2h) of sesarmid crabs indicates a low trophic level (TL
2) and is hence considered a primary consumer (Fig. 2). Thus, the
relatively low Hg concentration of sesarmid crabs clearly shows
the Hg transfer link from mangrove litter. Portunid crabs, S. olivera
and T. crenata, accumulate higher Hg concentration (0.41 mg/kg
and 0.37 mg/kg, respectively) than sesarmid crabs (0.12 mg/kg)
(p<0.001), because the portunid crabs are predators at a high
trophic level (≥3) in the food web and rely on a variety of prey
in the system (Cannici et al., 1996; (Thimdee et al., 2004)). Their
stable isotope signatures also reflect their heterogeneous diets,
although there were different δ 13 C values between species. The
δ 13 C values of the crenate crab T. crenata (−20.2h) were higher
than that of S. olivera (−22.4h), indicating that there is no overlap
of food sources between these species (Fig. 2). The finding is con-
sistent with the fact that Scylla species tend to feed on available
prey in the mangrove area nearby their niches (Nesakumari and
Thirunavukkarasu, 2014), while crenate crabs T. crenata inhabit
the extreme seaward edge of the mangrove and shallow intertidal
areas (Cannicci et al., 1996). Furthermore, the feeding pattern of
T. crenata is more active during the daytime, whereas Scylla crabs
tend to feed at night (Thimdee et al., 2004).
3.1.4. Fish
For each sample of fish both Hg concentration and stable iso-
topic signatures were analysed to understand the uptake path-
ways of Hg and nutrients, which have been previously shown to
come mainly from dietary sources (Hall et al., 1997). Although
the data shows a wide range (0.09 to 2.01 mg/kg DW for Hg
concentration; −18.4h to −23.2h for δ 13 C; and 5.4 to 10.9 for
δ 15 N) (Table 1, Fig. 2), Hg concentration in fish muscle showed
relevance to feeding strategies and trophic level. High trophic level
carnivorous fish (TL ≥ 3), such as Caranx ignobilis, T. jaculatrix and
N. thalassina, had significantly higher Hg concentrations than low
trophic level herbivorous fish (TL ≈ 2), such as Moolgarda perusii,
that rely directly on low Hg concentration benthic algae and detri-
tus. Conversely, since carnivorous species accumulate Hg through
53
a variety of prey they may be exposed to higher Hg concentrations.
Thus, the difference in Hg concentrations among carnivorous fish
depends on their prey type, prey quality, and the proportion of
organic Hg and total Hg bioaccumulation in prey tissue. For most
carnivorous fish, Hg was almost entirely accumulated as the highly
toxic form, MeHg (>95%), which has a long biological half-life in
muscle tissue, whereas Hg in omnivorous and herbivorous species
at low trophic levels varied greatly, ranging from 5 to 80% (Kehrig
et al., 2001; Le et al., 2010).
The semi-diurnal tidal regime is likely to influence the potential
foraging habitats of the fish community, as shown by Dorenbosch
et al. (2004) in shallow tropical areas of the Indo-Pacific. Indeed,
the mangrove forest in the study area was often drained during
low tidal periods, which prevents some fish species from foraging
in the mangrove interior. Since fish are motile and flexibly feed on
a variety of food sources in a wide range of the habitats, the Hg
concentration in fish may relate to the availability of food sources
along the mangrove edge and in adjacent habitats in the lagoon.
Interestingly, the stable isotopic signature of almost all fish showed
more δ 13 C enrichment than those of basal food sources (mangrove
litters and SOMs), suggesting that the fish may not be dependent on
mangrove-derived carbon sources, with the exception of the mud
gudgeon O. porocephala (−23.2 ± 0.8h) and T. jaculatrix (−22.1
± 1.3h) which most likely rely solely on mangrove-derived food
sources (Fig. 2). Epinephelus bleekeri, Netuma thalassina and Ter-
apon jarbua had more enriched δ 13 C values (range from −19.7 to
−18.4h) than other fish implying that they obtain food sources
from the mangrove edge or outside the mangrove, or may even
use the mangrove exclusively for shelter. Conversely, Gerres lim-
bustus and Megalops cyprinoides showed lower δ 13 C values (−20.7
to −20.5h), indicating that their diet was made up of a higher
proportion of mangrove-derived carbon sources. The narrow range
in isotopic signatures suggests that these two species assimilate
the same dietary Hg sources.
For the mud gudgeon O. porocephala, Toxotes jaculatrix and
giant trevally Caranx ignobilis, isotope signatures show the most
negative among fish species, suggesting these species diets con-
sists of a high portion of mangrove-derived carbon sources. The
differences in Hg concentration and isotopic signature between
these species may be due to their feeding behaviour and habitat
use. Indeed the piscivorous giant trevally, Caranx ignobilis, occupy
a high trophic level, and are therefore at a relatively high risk
of Hg contamination from bioaccumulation (Lavoie et al., 2013).
During juvenile stages they can inhabit a wide range of mixohaline
conditions in estuarine areas (Sudekum et al., 1991) including
upstream areas that may cause higher exposure to contaminated
Hg food sources (Suratman and Latif, 2015). Unlike giant trevally, O.
porocephala are resident species, mainly feeding on small benthic
mangrove invertebrates (Wilson and Sheaves, 2001). Hg transfer to
O. porocephala is closely associated with the consumption of local
mangrove carbon sources, as the δ 13 C signatures of O. porocephala
are similar to those of mangrove invertebrates such as Perisesarma
sp., and other mangrove gastropods. Juvenile archerfishes, Toxotes
jaculatrix, reside in highly tidal mangrove habitats and are omnivo-
rous, feeding on a variety of food items comprised of plant matters,
insects, crustaceans and even small fish, however the sub-adult
and adult stages tend to be more carnivorous (Simon and Mazlan,
2010). Thus, the high Hg concentrations measured in archerfish
may relate to their growth stage.
3.2. Biomagnification of Hg in the food web and health risk assessment
The combined analyses of contaminants and stable isotopic
composition in biota provided reliable insights into contaminant
sources and concentrations in consumers (Lavoie et al., 2013; Ike-
moto et al., 2008; Atwell et al., 1998). Diet routes are a main factor
54 D.Q. Le et al. / Regional Studies in Marine Science 16 (2017) 49–55
in Hg exposure, and δ 13 C signatures can help to understand the
ecological link between consumers and their diets. For instance,
Chen et al. (2009) found that higher Hg concentrations occur in pre-
dominantly pelagic feeding species (more depleted δ 13 C values),
indicating important pathways for the biotransfer of Hg. In our
study, the data clearly showed the Hg transfer link between basal
mangrove food sources and the benthic invertebrate food web,
whereas the link between mangrove-derived carbon and the fish
food web was considerably weaker. Many fish species are motile
and they can forage in one or more habitats during their lives,
therefore the Hg concentration in fish may relate to the diverse
prey Hg content available in the mangrove or habitats adjacent to
the lagoon. Fish species can either be exposed to mangrove-derived
Hg directly through contact with water, or indirectly due to trophic
relay or bioadvection of MeHg (the major speciation from bioaccu-
mulation in fish) from mangrove sediment to resident subtidal or
intertidal species and finally to transient higher trophic level tidal
species (Hammerschmidt and Fitzgerald, 2006; Kneib, 2000). For
this reason, data from all fish species was used to assess the extent
of biomagnification of total Hg in the study area. The δ 15 N values
were generally used as proxies for determining the trophic levels
of organisms in the food web (Post, 2002). The slope of the linear
regression between Hg concentrations and δ 15 N associations is an
essential component to the realisation of biomagnification trends
in aquatic systems (Lavoie et al., 2013).
An attempt was made to assess whether biomagnification of
mercury (Hg) exists in the food web from the lagoon. Biomag-
nification of Hg occurs when an increasing accumulation of Hg
corresponds to increases in trophic level, and has been identified
in various trophic food webs and predator–prey relationships (Al-
Reasi et al., 2007; Lavoie et al., 2010). The highest mean concen-
tration of total mercury was found in fish at high trophic levels
(carnivores), followed in decreasing order by portunid crabs, gas-
tropods, sesarmid crabs, filter-feeders, SOMs and mangrove litter.
Therefore biomagnification of Hg most likely occurs across trophic
levels. To confirm biomagnification of Hg in the food web, simple
linear regressions were examined between log-transformed Hg
concentration in organisms’ tissue and δ 15 N and δ 13 C values. A
significant positive correlation (R2 = 0.67) was found between
δ 15 N and Hg concentration, with a biomagnification power (slope
of regression) of 0.163 {Log10 [THg]=0.163(δ 15 N)−1.678} (Fig. 3),
however the correlation between δ 13 C and Hg concentration was
not significant (R2 = 0.19) and implies that different food sources
with variable Hg burdens were available to consumer species in
the lagoon. The food web magnification factor (TMF) calculated for
THg was 1.5 (>1), indicating that Hg was transferred up to higher
trophic levels in the food web.
The slope of the regression (0.163) of the log-transformed T-
Hg concentrations and 15 N values is substantially smaller than
the values determined by Jarman et al. (1996) (0.32) and Atwell
et al. (1998) (0.20) from temperate and arctic marine ecosys-
tems. The slope value from this study did however fall within the
ranges described by Al-Reasi et al. (2007), Bisi et al. (2012), and
Campbell et al. (2003) from tropical marine environments. This
assessment conforms to previous studies (Al-Reasi et al., 2007;
Bisi et al., 2012) which state that rates of Hg biomagnification
in the tropical marine region are somewhat lower than that in
polar and temperate marine ecosystems because of higher growth
rates and Hg excretion rates in tropical organisms compared to
temperate organisms, even at high trophic levels (Ikemoto et al.,
2008). Furthermore, high diversity (larger choice of prey for a given
consumer) in tropical mangroves could reduce the efficiency of Hg
trophic transfer (Lavoie et al., 2013).
Since the Hg concentrations of biota were based on dry weight,
they were converted to wet weight (w.wt), with 70%–80% wa-
ter contained in muscle tissues. Almost all Hg concentrations in
Fig. 3. Relationships between δ 15 N and log [Hg concentrations] of abiotic and biotic
samples from the mangrove creek of Setiu lagoon.
aquatic animals show similar or lower values than those in the
earlier studies of Agusa et al. (2007) and Ahmad et al. (2015),
however notably high Hg concentrations were found in Caranx
ignobilis (0.4 mg/kg converted w.wt), Toxotes jaculatrix (0.28 mg/kg
converted w.wt) and Netuma thalassina (0.29 mg/kg converted
w.wt). Additionally, carnivorous fish regularly presented >95% of
methylmercury (MeHg) in the total Hg in their muscle (Le et al.,
2010; Kehrig et al., 2001). Thus, the mean Hg concentration of
Caranx ignobilis closely approached the permitted value (0.5 mg/kg
w.wt of MeHg in fish) of Malaysian and JECFA guidelines (MFR,
1985). Although Hg concentrations in fish have not presented a
great concern for human consumption, a carnivore species based
design for Hg biomonitoring is proposed. Such a monitoring design
would be the most sensitive method of efficiently assessing the
effects and potentials threats of human activities and land use in
the upper reaches of Setiu lagoon in the future.
Assessing toxicological effects and dietary habits by combined
analyses of Hg concentrations and stable isotope compositions can
help to link contaminants in consumers to their original sources.
Further integrated studies are needed to elucidate the major di-
etary sources of fish communities associated with Hg biotransfer
at large scales within the lagoon and to determine whether trophic
relay is a potential biotransfer pathway of Hg outside the lagoon.
Acknowledgements
The authors are grateful to staff in University Malaysia Tereng-
ganu for their kind assistance in field work. We truly appreciate the
constructive comments and suggestions of three reviewers on our
manuscript. This work was supported by the Ministry of Higher Ed-
ucation Malaysia, under the Fundamental Research Grant Scheme
(FRGS) project number 59425 (FRGS/1/2016/WAB09/UMT/02/5).
This work was (partially) supported by JSPS Core-to-Core Program,
B. Asia-Africa Science Platforms. This work was performed in rela-
tion to JSPS Core-to-Core Program, B. Asia-Africa Science Platforms.
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