Biomagnification of total mercury in the mangrove lagoon foodweb in east coast of Peninsula, Malaysia

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

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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 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 b

article

info

Article history: Received 18 October 2016 Received in revised form 30 July 2017 Accepted 7 August 2017 Available online 12 August 2017 Keywords: Mercury Biotransfer Stable isotope Health risk Mangrove Food web

a b s t r a c t The combined analyses of total mercury (Hg) and stable isotopic (δ 13 C and δ 15 N) ratios were conducted to describe the food web pathways of dietary Hg, from basal food sources to benthic invertebrates and higher trophic level fish, and to determine if biomagnification of Hg is a persistent process in the food 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 values, the variation of gastropod Hg concentrations are likely correspond with local dietary sources of Hg in sediments, while variations in bivalve Hg reflect their exposure to low Hg concentrations in the water body. The combination of depleted δ 13 C values and high Hg concentration in gastropods suggest that microbially produced Hg sources in mangrove sediments play an important role in benthic biotransfer pathways. The isotopic compositions of crustaceans demonstrate the importance of feeding behaviour in Hg bioaccumulation. High bioaccumulation of Hg occurred consistently in carnivorous fish species, 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 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 combustion 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: [email protected], [email protected] (D.Q. Le).

http://dx.doi.org/10.1016/j.rsma.2017.08.006 2352-4855/© 2017 Elsevier B.V. All rights reserved.

Hg bioaccumulation has given rise to extensive surveys of Hg concentrations and speciation in ecosystems, particularly mangrove wetlands (Al-Reasi et al., 2007; Lavoie et al., 2013). Though mangrove 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

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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 concentrations 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 carbon ranges, on average, from 0.0h to 1.3h between consecutive trophic levels, the value of δ 13 C in consumer tissue tends to mirror 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.), sediment 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 sandymud 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 isotopic 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

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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

δ N

δ C

6

0.04 ± 0.01

3.6 ± 0.3

−29.5 ± 1.1

2 2

0.06 ± 0.01 0.05 ± 0.01

2.7 ± 0.4 3.5 ± 0.4

−25.8 ± 0.5 −24.6 ± 0.3

mg/kg dwt. Mangrove leaves Sediments Mangrove interior Mangrove edge Crustacea Perisesarma sp. Thalamita crenata Scylla olivera Bivalve Crassostrea sp. Meretrix lyrata Gastropod Cerithium coralium Faunus ater Cerithidea quadrata Littoraria carinifera Fish Ambassis interrupta Epinephelus bleekeri Ophiocara porocephala Caranx ignobilis Megalops cyprinoides Toxotes jaculatrix Netuma thalassina Terapon jarbua Gerres limbustus Moolgarda perusii

Mean ± SD (h)

3 3 3

a

15

mg/kg wwt.

TL

Feedingb

13

0.12 ± 0.04 0.37 ± 0.03 0.41 ± 0.1

0.03 0.07 0.08

5.4 ± 0.2 8.3 ± 0.5 8.2 ± 0.5

−25.7 ± 0.8 −20.2 ± 0.9 −22.4 ± 1.2

2.1 3.4 3.4

BE, DF BE, PR BE, PR

2 3

0.09 ± 0.02 0.11 ± 0.03

0.02 0.02

6.0 ± 0.3 6.6 ± 0.0

−22.2 ± 1.3 −21.4 ± 0.1

2.4 2.6

BP, FF BP, FF

2 3 3 1

0.11 ± 0.03 0.15 ± 0.02 0.37 ± 0.01 0.41

0.03 0.08 0.03 0.07

4.7 ± 0.3 5.8 ± 0.4 5.0 ± 0.1 4.9 ± 0.4

−19.0 ± 0.5 −22.5 ± 0.2 −25.2 ± 0.1 −24.8 ± 1.2

1.8 2.3 1.9 1.9

BE, DF BE, GR BE, GR BE, GR

0.37 ± 0.03 0.43 ± 0.35 0.41 ± 0.19 2.01 ± 0.82 0.47 ± 0.05 1.40 ± 0.56 1.47 ± 0.31 0.32 0.30 ± 0.07 0.09 ± 0.01

0.08 0.11 0.08 0.40 0.09 0.27 0.29 0.06 0.06 0.02

10.1 ± 0.6 9.7 ± 0.5 8.1 ± 0.6 10.2 ± 0.3 10.9 ± 1.1 9.0 ± 0.6 10.9 ± 0.7 9.8 10.2 ± 0.1 5.5 ± 0.7

−19.8 ± 0.4 −18.9 ± 0.6 −23.2 ± 0.8 −21.6 ± 0.6 −20.7 ± 1.1 −22.1 ± 1.3 −18.6 ± 1.2 −18.4 −20.5 ± 0.5 −19.8 ± 0.6

3.4 3.3 2.8 3.5 3.7 3.1 3.7 3.3 3.5 2.0

PB, PR BE, PR BE, PR PB, PR PB, PR PB, PE, PR PB, PR PB, OM PB, OM PB, HE

3 3 2 4 2 4 2 1 2 2

6.4 ± 0.6 9.0 ± 0.5

38.9 ± 2.1 128.7 ± 26.0

8.9 ± 0.5 15.5 ± 5.8 15.1 ± 3.5 16.0 ± 0.6 27.4 ± 5.3 13.8 ± 0.5 19.0 ± 0.2 11.9 9.4 ± 0.1 11.3 ± 2.1

10.2 ± 0.8 64.6 ± 70.8 29.7 ± 3.0 55.8 ± 3.6 159.2 ± 64.7 52.6 ± 6.5 67.0 ± 11.6 22.6 12.9 ± 0.8 23.4 ± 16.2

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

8

6

4

2

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 fish and crab tissues ranged from 2.4–3.1 and thus, lipid correction was not performed. 2.3. Measurement of Hg and stable isotope ratios Stable isotope ratios (δ 13 C and δ 15 N) were measured using a stable isotope ratio mass spectrometer (IsoPrime100, IsoPrime,

U.K.) connected with a combustion device (vario MICRO cube, elementar, Germany) at the Atmosphere and Ocean Research Institute, University of Tokyo, Japan. Stable isotope compositions are expressed as δ values, which are measured as the ratio of heavy to light isotopes in a sample relative to a known standard, by the following equation:

δ X (h) =

[(

Rsample Rstandard

)

] − 1 × 1000

(1)

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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 traceable 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 reference 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 determined with a cold vapour atomic absorption spectrometer (MA3000, 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 benthic zones (bivalves and gastropods) within the mangrove creek, trophic levels (TL) are determined using equation reported in Jardine et al. (2006): TL = 2 + δ 15 Norganisms − δ 15 Np × Pp + δ 15 Nb

{

(

× 1 − Pp

[

)]}

/115N.

(2)

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, respectively; 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 .

(3)

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 ,

(4)

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 .

(5)

Results are expressed as mean ± SD. One-way ANOVA was performed to reveal any significant differences in metal concentrations 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, mangrove 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 significant 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 sandymud, it contained less total organic carbon than the mangrove interior, 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 deposition of atmospheric Hg is likely to be negligible. Hg residue in leaves was mainly inorganic and could be methylated into organic 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 methylation 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 carbon 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 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 significantly 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 filterfeeding 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 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 concentrations 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 interior 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) presented 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 elevated 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 inside 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 consistent 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 isotopic signatures were analysed to understand the uptake pathways 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 detritus. 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 Terapon 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 limbustus 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 consists 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 omnivorous, 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; Ikemoto et al., 2008; Atwell et al., 1998). Diet routes are a main factor

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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 predominantly 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 bioaccumulation 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. Biomagnification 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 (AlReasi et al., 2007; Lavoie et al., 2010). The highest mean concentration of total mercury was found in fish at high trophic levels (carnivores), followed in decreasing order by portunid crabs, gastropods, 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 THg 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 ecosystems. 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% water 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 dietary 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 Terengganu 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 Education 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 relation to JSPS Core-to-Core Program, B. Asia-Africa Science Platforms. References Agusa, T., Kunito, T., Sudaryanto, A., Monirith, I., Supawat, K.A., Iwata, H., Ismail, A., Sanguansin, J., Muchtar, M., Tana, T.S., Tanabe, S., 2007. Exposure assessment for trace elements from consumption of marine fish in Asia, Environment Pollution 145, 766–777. Ahmad, N.I., Noh, M.F.M., Mahiyuddin, W.R.W., Hamdan, J., Ismail, I., Azmi, W., Veloo, Y., Hairi, M.H., 2015. Mercury levels of marine fish commonly consumed in Peninsular Malaysia. Environ Sci Pollut Res 22, 3672–3686.

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