Water Air Soil Pollut DOI 10.1007/s11270-009-0155-0

Distribution and Accumulation of Mercury Derived from Gold Mining in Marine Environment and Its Impact on Residents of Buyat Bay, North ,

Markus T. Lasut & Yoshiaki Yasuda & Evan N. Edinger & Jane M. Pangemanan

Received: 16 April 2009 /Accepted: 14 July 2009 # Springer Science + Business Media B.V. 2009

Abstract Buyat Bay (BB), , Indone- artisanal gold mining, and a reference area of the Bajo sia, was a submarine tailings disposal (STD) site for Coast (Bajo) free of any anthropogenic sources of Hg an industrial gold mine that extracted mercury (Hg)- were also sampled. Both THg and MeHg were containing ores from 1996 to 2004. To evaluate the detected in all samples measured showed concen- distribution and influence of such a Hg release into trations to be highest at the artisanal mining site, the environment, particularly into BB, we quantified intermediate at the STD site and at their lowest in the the total mercury (THg) and methyl mercury (MeHg) control area. THg and MeHg concentrations in marine in the surface sediments (beach, river estuary, and biota and human hair increased with trophic levels marine) and biota of the bay, as well as the scalp hair and were significantly higher at the STD site than of residents in the adjacent community. A nearby among the controls. Besides examining the source body of water, Totok Bay, polluted by Hg from and distribution of Hg, its accumulation in biota, and its potential impact on humans, we also studied the M. T. Lasut (*) role of the mine management so as to provide a Marine Science Department, Faculty of Fisheries recommendation for future actions. and Marine Science, Sam Ratulangi University, , North Sulawesi, Indonesia Keywords Methyl mercury. Bioaccumulation . e-mail: [email protected] Submarine tailings disposal (STD) . Artisanal mining . : M. T. Lasut J. M. Pangemanan Sulawesi . Indonesia Kampus Unsrat Bahu, Manado 95115 Sulawesi Utara, Indonesia 1 Introduction Y. Yasuda National Institute for Minamata Disease, 4058-18 Hama, Industrial mining of gold and/or cinnabar, which Minamata City, Kumamoto 867-0008, Japan involves the extraction of Hg by the mineralization of cinnabar (HgS) or as Hg contaminants within other ore- E. N. Edinger Geography Department, bearing minerals, is considered to be one of the major Memorial University of Newfoundland, anthropogenic sources of Hg into the environment since St. John’s, NL A1B3X9, Canada these operations must dispose of tailings containing mercury (Williams et al. 1999; Edinger et al. 2007). An J. M. Pangemanan Medical School, Sam Ratulangi University, Indonesian case in point is the Newmont Minahasa Manado, North Sulawesi, Indonesia Raya gold mine operated in the Buyat–Ratatotok Water Air Soil Pollut district, Minahasa Regency, North Sulawesi, which is a In the Buyat–Ratatotok district of North Sulawesi, source of Hg through the mineralization of refractory artisanal gold mining co-exists with industrial gold sediment-hosted gold deposits (Turner et al. 1994). mining, but involving different watersheds (Edinger et Artisanal gold mining using mercury amalgam- al. 2007). The introduction of Hg into the environ- ation is another of the major sources of anthropogenic ment from artisanal mining occurs during the extrac- Hg contamination (de Lacerda and Salomons 1998; tion process or through the leaching of waste from Malm 1998; Kambey et al. 2001; de Lacerda 2003; barrels (Kambey et al. 2001), while Hg from Ogola et al. 2002; Limbong et al. 2003), along with industrial mines is discharged as tailings high in Hg acetaldehyde factories (Yasuda et al. 2004), and the via a submarine tailings disposal (STD) system. The fossil-fuel combustion and chlor-alkali industries ore processing practices of both artisanal and STD- (Pacyna et al. 2006). Such types of gold mining using industrial gold mines carry Hg-containing sedi- operations using mercury amalgamation are wide- ments to the coastal marine eco-system of Totok Bay spread, especially throughout the developing world and Buyat Bay, respectively (Edinger et al. 2007; (Ogola et al. 2002; de Lacerda 2003), including Fig. 1, map). Although the Hg in industrial mine Indonesia (James 1994; Kambey et al. 2001; Limbong tailings (in the form of synthetic mercuric sulfide) is et al. 2003). In North Sulawesi, Indonesia, environ- purported to be highly insoluble, the stability of Hg mental concerns have arisen based on estimations that and other toxic trace elements in submarine gold mine approximately 200 t of Hg are used annually in such tailings may actually be much lower than previously mining operations (Kambey et al. 2001). Forty to assumed (Blackwood and Edinger 2007). Hg from 50% of the Hg used in the amalgamation is estimated both sources described above potentially enters the to be dumped into rivers as metallic Hg, and an food chain after being methylated at the sediment– additional 5% to 10% of the Hg is discharged into the water interface (de Lacerda and Salomons 1998)orat environment during the recovery of gold from Hg the surface layers of sediment (Goulet et al. 2007). amalgam. Further estimates have concluded that The Hg within processed refractory sulfide ore may be approximately 1.32 kg of Hg is discharged for every released into the air as a result of roasting, or into 1 kg of gold production (Pfeiffer and Lacerda 1988; seawater from the oxidation of Hg-bearing minerals. cf. de Lacerda and Salomons 1998). Therefore, adverse biological effects may occur in a

Fig. 1 Map of the study areas and the sampling sites. A Indonesia, B Minahasa Peninsula, C Ratatotok–Buyat areas, D Bajo Coastal Waters, E Buyat Bay Water Air Soil Pollut marine system where contamination by any type of Hg Totok Bay (TB) is adjacent to BB, with both or other heavy metals has occurred (Limbong et al. separated by the Ratatotok Peninsula (Fig. 1). TB 2003; De Luna and Rosales-Hoz 2004; Gemici 2004). receives water from the Ratatotok catchment area The objective of the present study is to evaluate the through the Totok River (TR), which is a completely distribution of Hg deposits in sediments and biota different catchment area from that of BR. Since the after Hg is introduced into coastal marine environ- 1980s, TB has been severely affected by artisanal ments through STD, artisanal mining, or the natural gold mining using Hg amalgamation in the TR weathering of auriferous rocks. We first document the watershed (Hendrayana 2005; Kerebungu 2005), concentrations and spatial distributions of total Hg which distributes at the upper land area of the (THg) and methyl Hg (MeHg) in sediments and the Ratatotok, the operation employed a peak level of levels of MeHg bioaccumulation in marine biota and about 5,000 miners during the late 1980s (Yayasan human hair and then discuss their potential impacts on Lestari, unpublished data). human health. At the southern part of the Buyat–Ratatotok district, another artisanal gold mining operation has been located at the upland area of Kotabunan (Mintu, 2 Materials and Methods Lanut Goropai) since 1974 (Fig. 1). Previous gold mining activity in that area (Tapa Beken and Doup) 2.1 Study Areas was conducted by the Dutch from 1936 to 1941, using a hydraulic technique and friable bedrock to BB is located in the southeastern part of the Minahasa partially concentrate the free gold prior to amalgam- Peninsula, North Sulawesi, Indonesia (Fig. 1) and ation with Hg (Hendrayana 2005). Approximately situated between two peninsulas, Ratatotok to the 500 miners currently work in that area using the same northeast and Bobokan to the southwest. BB opens to techniques used at Ratatotok. the Maluku Sea () to the South and At the same time, we also sampled a reference receives terrigenous runoff from the Buyat catchment area, Bajo, on the northwest coast of the Minahasa area (Hendrayana 2005) via the Buyat River (BR). It Peninsula (Fig. 1). Bajo was chosen because it has must be emphasized, however, that BR is never similar characteristics to BB and TB in its beach affected by small-scale gold mining since all the gold conditions and habitats, including the fishing com- in the BR watershed is refractory (Turner et al. 1994; munities at Bajo Village (BV) where all the residents Edinger et al. 2007). consume fish daily. Although there is no anthropo- The seabed slope in BB follows the contour of the genic Hg source in the vicinity of Bajo, the volcanic coastline and gradually declines to 70–80 m, then andesite bedrock present there is similar to much of drastically drops to a depth of 100 m approximately the bedrock in the Buyat–Ratatotok district, and as yet 700–1,000 m from the coastline; the beach is a sandy unexploited gold deposits are known to exist in the stretch with rocky shores at either end. The fishing area upstream from Bajo (Effendi 1978). village of Buyat Pante (BPV) is located along the beach front and is inhabited by up to 230 people (54% 2.2 Sampling Procedure males and 46% females) comprising 54 households. A large-scale open pit industrial gold mine used Sampling of sediments and biota was undertaken cyanidation-based extraction to recover gold was during the dry season in July and August 2004 at the started at an area upstream of BR in 1996 (Fig. 1). lowest tides in the coastal and marine areas of BB, Approximately 2,000 t day–1 of tailings (45–55% TB, and Bajo and in the estuarine area of BR, solids, <75-µm-diameter particles) in the form of including the BPV and BV for samples of scalp hair. slurry containing Hg as fine-grained mercuric sulfide were disposed of by an STD system through 2.2.1 Sediments underwater pipelines 900 m from the beach, at a water depth of 82 m in BB. The position of the Three groups of sediment samples were collected: pipeline outfall is around sampling point nos. 8–11, beach sediments (<1 m water depth), river sediments 17–19, and 25 as shown in Fig. 1. in the estuary, and seabed sediments (>1 m of water Water Air Soil Pollut depth). The beach sediments were collected at five were usually prepared separately for measurement, sites in the intertidal zone in each of the study areas e.g., sea grass leaves, seaweed thallus, the basal (Fig. 1, nos. 1–5 for BB, nos. 26–30 for TB, and nos. portions of soft coral, soft body parts of bivalves 34–38 for Bajo) using a sediment corer made of a and gastropods, and fish muscle. The main body parts commercial 8-cm-diameter polyvinyl chloride pipe of crabs (including the shells) were prepared for able to reach 5 to 10 cm in depth for sampling of measurement after removing the legs. Further infor- surface sediment layers. The river sediments were mation regarding samples is presented in Table 1. collected at the BR estuary, about 100 m upstream All biological samples were freeze-dried prior to (Fig. 1, no. 6) and about 250 m upstream (Fig. 1, no. measurement, with the moisture content of each 7) from the river mouth using the same corer as noted recorded at this step by comparing sampled wet above. Each sample was a mixture of five cores (at weights and freeze-dried weights. Just prior to the center and four points of a circle 5 m in radius; measurement, biological samples were digested in Yasuda et al. 2004). The seabed sediments were five to ten times the volume of the sample weight of collected at 12 sites (Fig. 1, nos. 8–11 and 18–25) 1 N NaOH placed at 60°C overnight. inside BB, six sites (Fig. 1, nos. 12–17) outside the bay close to Kotabunan and the Kumeke Strait, and 2.2.3 Scalp Hair three sites (Fig. 1, nos. 31–33) in TB. The seabed sediment samples were collected using a stainless Sampling of human scalp hair was carried out by a steel Petit Ponar grab sampler (Edinger et al. 2007). survey of residents by using a door-to-door or Sampling positions were recorded using a hand- assembly technique in July 2004 at BPV (n=28; held GPS. The beach samples were thoroughly mixed male=11, female=17) and BV (n=29; male=15, after being passed through a 2-mm mesh stainless female=14). Sampling was performed under the steel sieve (JPHA 2001) to remove pebbles, shells, procedures of JPHA (2001). Hair behind the ear was bits of animal and plant matter, and other foreign cut 2 cm from the root and placed in individual plastic objects. Aliquots (about 500 g) were then placed in a bags for each participant. Prior to Hg measurements, sealed polyethylene plastic bag. In the field, all the samples were rinsed with 1% neutral detergent in samples were stored in coolers with chilled coolant distilled water, followed by rinsing twice with gel packs to maintain them at a sufficiently low distilled water, ethyl alcohol and acetone, and then temperature. For Hg analyses, sediment samples were dried in desiccators. The dried hair was cut into used after mixing by a quartering method (Yasuda et minute pieces with stainless steel scissors. During hair al. 2004) that divided a pile of sample into four parts collection, a questionnaire was administered to each and mixed them diagonally, repeating the procedure participant covering sex, age, occupation, and food- ten times for each sample. consumption habits.

2.2.2 Biota 2.3 Hg Analysis

The soft coral, seaweed, and seagrass samples were All Hg measurements were performed at the National collected using a stainless steel knife to excise parts of Institute for Minamata Disease, Japan, except for each sample. Intertidal bivalves Septifer sp., gastro- submarine sediment samples, which were measured at pods Nerita sp., and crabs were collected manually. Activation Labs Inc., in Ancaster, Ontario, Canada. The Subtidal bivalves, Tridacna sp. and Pinna sp., were seaweed and sea grass samples were stored in a collected using a hammer and chisel while snorkeling refrigerator, while others were kept in a freezer (−80°C) at a depth of 1.5 to 2 m. The crabs were collected prior to transportations to the laboratories. All samples along the beach (Fig. 1, site nos. 1–5, 26–30, and 34– (except for hair) were packed in a cooler with coolant 38), while other samples were gathered at selected gels during transportation. sites whenever available (Fig. 1, nos. 1, 30, and 34– THg was quantified using cold vapor atomic- 38). Fishes were obtained from local fishermen who absorption spectrophotometry (CV-AAS; Akagi and were asked to catch them by angling inside the BB Nishimura 1991;JPHA2001). Samples (0.3 g or less areas and along the beach of Bajo. Some sample parts of sediment or hair and 0.5 ml or less of 1 N NaOH Water Air Soil Pollut

Table 1 Biota samples, habitat, sampling locations, and number of samples

Biota Scientific Common Habitat Diet Sampling No. of Tissue sample name English name locations/sites samples

Soft coral Sinularia sp. Finger coral Rock/hard bottom Plankton BB/no. 1 10 A part feeder Seaweed Turbinaria sp. Cup coral Coral, rocks, shell, Producer BB/no. 1 10 Thallus in shallow tropical reef flats Seagrass Enhalus Eel grass Perennial Producer BB/no. 1 10 Leaf acoroides Bivalve Septifer sp. Box mussel Attached to rocks, Suspension BB/no. 1 9 Soft part dead corals, or the feeder underside of stones Tridacna sp. Giant clam Infaunal in Suspension BB/no. 1 34 Soft part rock/hard bottom feeder BAJO/nos. 34–38 Pinna sp. Penshell Infaunal in Suspension BAJO/nos. 6 Soft part sand/mudflat feeder 34–38 Gastropod Nerita sp. Snail Rock/hard bottom Herbivore/ BB/no. 1 14 Soft part omnivore TB/no. 30 9 BAJO/nos. 10 34–38 Crabs Uca sp. Fiddler crabs Sandy beach Carnivore BB/nos. 1–5 10 Main part, TB/nos. 26–30 9 including shell BAJO/nos. 10 34–38 Fish Epinephelus Honeycomb Semi-protected Carnivore Inside BB 5 Muscle merra grouper seaward reefs Parupeneus Manybar goatfish Demersal Carnivore Inside BB 2 Muscle multifasciatus Lutjanus basmira Snapper Demersal Carnivore Inside BB 3 Muscle Lutjanus sp. Snapper Demersal Carnivore BAJO 8 Muscle Selaroides sp. Scad Demersal Carnivore BAJO 10 Muscle

BB Buyat Bay, TB Totok Bay, BAJO Bajo Coastal Waters, SD standard deviation

digested biological samples) were placed in a 50-ml ethanol (1:1) and concentration by dithizone, Na2S, volumetric flask, to which 1 ml of water, 2 ml of a and dithizone extraction (Ikingura and Akagi 1999; mixture of nitric acid and perchloric acid (1:1), and JPHA 2001; Matsuyama et al. 2004). According to 5 ml of sulfuric acid were added. The flask was Akagi et al. (1995), hair MeHg was extracted from heated at 230°C for 30 min. After cooling, the about 10 mg of each chopped hair sample as digested mixture was diluted up to 50 ml with water described above in 3 ml of 2 N HCl at 100°C for and used as a sample for Hg analysis by CV-AAS. Hg 5 min and then transferred from a 1 ml aliquot of 2 N in the aliquot of the sample solution was vaporized by HCl into 4 ml of toluene with vigorous shaking. Each reduction in the presence of 0.l5% (w/v) stannous aliquot of toluene layer was injected into a GC-ECD chloride under vigorous bubbling for 30 s. The Hg for MeHg determination after removing the 2 N HCl vapor was then sent to the atomic-absorption analyzer. by suction. Each measurement was conducted with This preparation was carried out in an automated duplicate determination twice. circulating airflow system (Akagi and Nishimura 1991, assembled by Sanso Co. Ltd., Tokyo, Japan). 2.4 Quality Control MeHg concentrations in each sample were deter- mined by an electron-capture detector type gas As reference materials, we used IAEA-086 (human chromatograph (GC-ECD) after extraction in KOH– hair by IAEA), DORM-2 (dogfish meat by NRC), and Water Air Soil Pollut

CRM-580 (sediment by BCR) for THg and MeHg The highest THg concentrations in BB were found determinations. Measurements of the reference were outside the bay around site nos. 16 and 12 close to conducted six times for each material. The values the Kotabunan and Kumeke Strait areas and at an obtained closely corresponded (about 97%) to the outer site at the mouth of the bay around nos. 9–10, certified values published by each supplier (Table 2). 15, 17–19, and 25. The latter sites were located at the STD pipeline outfall. Inside the bay, Hg concen- 2.5 Data Analysis trations tended to increase from the beach to the outfall areas. A comparison of MeHg concentrations and the Comparing the THg concentration levels in beach proportions of MeHg–THg in the beach sediment sediment at the three sampling sites, their value were from all three locations was conducted with a simple found to be highest in TB, intermediate in BB, and statistical test of one-way analysis of variance (Fowler lowest in Bajo (Fig. 3). The BB samples indicated and Cohen 1990) applied using the Minitab© statis- much lower concentrations of THg than those in TB, tics package. Comparisons of THg concentrations in though they were ten times higher than that in Bajo. the same species of biota from BB and Bajo and of MeHg concentrations were significantly higher in TB MeHg concentrations in scalp hair from BPV and BV than in BB and at their lowest in Bajo [Fig. 3; one- residents (location and gender) were done in the same way ANOVA, F(df, 2)=32.67, p<0.05]. In addition, manner as those for sediment. the ratio of MeHg to THg in average values was 3.2% in Bajo, 2.5% in BB, and 0.4% in TB, which was significantly lower in TB than in the other two bays 3 Results [one-way ANOVA, F(df, 2)=6.38, p<0.05].

3.1 Concentration and Distribution of Hg in Sediment 3.2 Concentration and Bioaccumulation of Hg in Biota In BB, THg concentrations gradually increased from the river estuary (nos. 6–7) to the beach (nos. 1–5) Concentration of THg in biota derived from BB, TB, and to the seabed sediment (nos. 8–25). A converse and Bajo varied according to the species group and pattern was observed in TB where the beach sediment diet habitat. Although the trophic producer groups, (nos. 26–30) showed higher THg concentrations than seaweed and sea grass, had low THg concentrations the seabed sediment (nos. 32–33). However, the compared with those of the consumer groups, they sample at no. 31 had THg concentrations in the range were higher than those of the suspension-feeding soft of beach sediment (Fig. 2). The concentrations in the coral Sinularia sp. Snails (grazers) and bivalves beach sediment samples at Bajo (control; Fig. 1, nos. (suspension feeders) showed relatively higher con- 34–38) were found to be in the same range of centrations than those of intertidal crabs (carnivores), magnitude, i.e., 10 to 17 ppb. but relatively lower than fish groups.

Table 2 Reference materials of Hg and measured values

Materials Reference Number Certified values (ppb) Measured values [average (ppb)±95% CI]

Human hair by IAEA IAEA-086 THg 573±39 554±10 MeHg 258±21 261±15 Dogfish meat by NRC DORM-2 THg 4,640±260 4,670±110 MeHg 4,470±320 4,260±100 Sediment by BCR CRM-580 THg 132,000±3,000 132,000±2,000 MeHg 75.5±3.7 76.0±2.6

CI confidence interval, IAEA International Atomic Energy Agency, NRC National Research Council of Canada, BCR Commission of the European Communities Water Air Soil Pollut

Fig. 2 Concentration of THg in surface sediment samples the level of Hg; numbers below are the sampling points; (river estuary, beach, and seabed) collected from Buyat Bay and numbers above are the Hg levels (parts per million) the estuarine area of the Buyat River. The vertical bars indicate

THg concentrations in biota of Tridacna sp. THg and MeHg values that accumulated in fish (bivalve), Nerita sp. (snail), and Uca sp. (crab) were muscles collected inside BB are depicted in Fig. 5. compared among the three study areas (Bajo, BB, and The average MeHg concentration in fish muscle TB), as shown in Fig. 4. Except for Tridacna sp. in ranged from 46 ppb wet weight in Lutjanus basmira which the THg concentrations from BB were signif- to 359 ppb wet weight in E. merra. The MeHg icantly higher (p<0.05) than those from Bajo, the same pattern of concentrations was exhibited by those 100 biota, where TB showed higher concentrations than Totok those in BB and Bajo, which was a statistically Buyat Bajo significant finding (p<0.05). Comparing the concen- 10 trations in biota between BB and Bajo, their values showed an almost 10-fold difference. However, the concentrations in BB were three to five times lower MeHg (ppb) 1 than those in TB. The concentrations of THg in BB fish (caught 0.1 outside the bay) were higher than those in Bajo, while 1 10 100 1000 10000 those in BB fish from inside were higher than those THg (ppb) from outside. The highest concentrations were found Fig. 3 Comparison of THg and MeHg concentration levels in in the honeycomb grouper, Epinephelus merra, from the surface beach sediments from Bajo Coastal Waters, Buyat inside the bay. Bay, and Totok Bay Water Air Soil Pollut

Fig. 4 Comparison of THg 500 concentration in biota collected from the study areas. BAJO Bajo Coastal Waters (reference area), BB Buyat Bay, TB Totok Bay. The vertical bars denote 95% confidence limits 250 THg (ppb)

0 BCW BB BCW BB TB BCW BB TB

Tridacna sp. (Bivalve) Nerita sp. (Gastropod) Uca sp. (Crabs) concentrations in E. merra were six times higher than MeHg in adult males (4.2±2.0 ppm, range 0.9 to those in Lutjanus sp. (42 ppb) and thousands of times 7.8 ppm) was significantly higher than that in adult higher than in Selaroides sp. (0.058 ppb) collected in females (2.2±1.5 ppm, range 0.5 to 6.6 ppm; one-way Bajo, whereas MeHg concentrations in L. basmira ANOVA, F(df, 1)=8.87, p<0.05). In BV residents, from BB were roughly equivalent to those in Lutjanus the average scalp hair MeHg concentration in males sp. from Bajo. THg and MeHg were found to be (1.0±0.4 ppm, range 0.4 to 1.5 ppm) compared to strongly correlated (r=0.92). females (0.9±0.2 ppm, range 0.6 to 1.4 ppm) was not significantly different [one-way ANOVA, F(df,1)= 3.3 Concentration of Hg in Hair 1.51, p>0.05, n=29].

Both THg and MeHg were detected in scalp hair samples collected from BPV and BV residents (30 4 Discussions participants aged 20–60 years). The concentrations of THg were similar to those of MeHg. The average 4.1 Source and Distribution of Hg MeHg concentration of BPV hair (2.9±0.7 ppm, range 0.5 to 7.8 ppm) was significantly higher than It was found that those seabed sediment samples that of BV residents (1.0±0.3 ppm, range 0.4 to collected inside and outside BB at the area close to 1.5 ppm; one-way ANOVA, F(df, 1)=28.99, p<0.05). Kotabunan (nos. 12, 13, and 16) indicated higher levels Among BPV residents, the average concentration of of Hg concentration than the area in between (no. 14). Hg deposits outside the bay at the area close to 750 Kotabunan may have come from the artisanal gold

THg mining conducted at the upstream area. This source of MeHg Hg would scarcely have contributed to Hg deposits inside BB. Therefore, besides the STD as a source, the 500 Hg distributed inside BB is considered due to airborne emissions of Hg from the mill, a malfunction occurring when the Hg scrubber did not function properly 250 (Edinger et al. 2007). Generally, 40% of Hg in the Concentrations (ppb) atmosphere might be deposited in the aquatic envi- ronment as Hg2+ in precipitation, while the remaining

0 60% is deposited on land (Mason et al. 1995). L. basmira P. multifasciatus E. merra The ratio of MeHg to THg in sediment varies at Fig. 5 Concentration of Hg in fish muscles collected from each site. MeHg found in sediments at each sampling Buyat Bay. Correlation rate between THg and MeHg is 0.92 site of the present study is thought to be the result of Water Air Soil Pollut inorganic mercury methylation mediated by sulfate- seabed sediment samples) caused an increase in Hg reducing bacteria in the sediment (Goulet et al. 2007; accumulations in the marine biota of the bay since Hammerschmidt and Fitzgerald 2004). The ratio of sediment plays a key role in controlling the metal MeHg to THg in sediment decreased with the increase concentrations in biota (Blanchette et al. 2001). in THg at the three sampling sites (Fig. 3), indicating Concentrations of Hg in marine biota correlate that the activity of Hg methylation in sediment does with their trophic position (Desta et al. 2007) and not necessarily depend on the concentration of habitat (Bustamante et al. 2006) as predators (con- inorganic Hg found in the present study. sumers), showing higher tissue concentrations than those in their prey (Bustamante et al. 2006). That 4.2 Accumulation of Hg in Marine Biota proved true in the present study (Fig. 6a, b). Intertidal crabs, however, are an exception within the Hg The presence of Hg in the sediment inside BB that concentration hierarchy (see the explanation below). had exceeded the natural level (as confirmed by the The difference in concentrations between Lutjanus sp.

Fig. 6 a Accumulation of THg in biota of BB. b a 1000 Accumulation of THg in Sinularia sp. (soft coral) biota of Bajo Turbinaria sp. (seaweed)

E. acoroides (seagrass)

100 Nerita sp. (gastropod)

Septifer sp. (bivalve)

Tridacna sp. (bivalve)

Uca sp. (Crabs) 10 L. basmira (fish)

THg (ppb) P. multifasciatus (fish)

E. merra (fish)

1

0.1 b 1000 Nerita sp. (gastropod)

Tridacna sp. (bivalve)

Pinna sp. (bivalve)

100 Uca sp. (Crabs)

Lutjanus sp. (fish)

Selaroides sp. (fish)

10 THg (ppb)

1

0.1 Water Air Soil Pollut and E. merra reflects the trophic level of each species, unclear, some appropriate continuous monitoring of and the Hg concentrations in fish meat may reflect the Hg methylation and bioaccumulation ought to be Hg level difference at both stations (BB and Bajo). established as long as Hg waste disposal activity persists The low THg concentration in intertidal crabs is in BB. Simultaneously, BB residents who had habitually probably under estimated due to some property of the consumed fish must be monitored to reduce their Hg samples. Hg determination in crabs was conducted intake, and restrictions should be published to promote using whole crab bodies since it was nearly impossi- the consumption of only fish species lower in Hg. ble to separate their soft parts from their shells. The Hg concentrations in crab shells are 1/10 of that of crab muscles (Yasuda, unpublished data). Moreover, 5 Conclusions the value for crab Hg concentration determined in the present study may actually be only around half of the & Hg in the Buyat-Ratatotok area may be traced back real value in the soft part of crabs. to several principal sources: First is the artisanal In the present study, the processes of methylation gold mine activity, second are the tailings of STD and bioaccumulation were found to occur in BB, a from industrial mining, and third are the airborne finding confirmed by the fact that MeHg was found in emissions from the industrial gold mine mills. both beach sediment (Fig. 3) and the marine biota Concentrations of the first two inputs seem to be (Fig. 4), including fish (Fig. 5). The bioaccumulation relatively higher than those of the third. In addition, process also occurred in the study areas of both BB the riverine input of Hg from the BR due to the (Fig. 6a) and Bajo (Fig. 6b), as was common in terrestrial disturbances associated with industrial natural marine ecosystems. mining (Edinger et al. 2007) may be another source. & Hg in the beach sediment at all three study areas is 4.3 Potential Impact on Humans methylated in a range of 0.4% to 3.2% of THg. The methyl mercury in BB marine environment, Consumption of fish is the main source of MeHg in including that in the beach sediment, accumulates humans (Malm 1998; Frery et al. 2001; Yokoo et al. in the marine biota, including in humans, through 2003; Baker et al. 2004). It is also known that the the food web. However, the extent of bioaccumu- more fish consumed, the higher the Hg concentration lation varies according to species and/or sampling in human hair (see Dickman et al. 1999; Yokoo et al. location. The concentrations of methyl mercury in 2003). In the present study, 29 of 30 participants the BB biota are higher than that in the Bajo biota, reported consuming fish more than four times a week. but lower than in TB. Finally, our results demonstrating that the hair Hg & Further Hg accumulations are found in BPV concentration in BPV was three times higher than that residents’ hair as a reliable evidence of Hg exposure. in Bajo reflects the difference of Hg concentrations in the fish of those regions. Acknowledgments The authors wish to thank the National Institute for Minamata Disease (NIMD), Japan, and the Faculty 4.4 Management Implications of Fisheries and Marine Sciences, Sam Ratulangi University, Indonesia, for supporting this investigation. Additional support was provided by an NSERC Discovery Grant and by Memorial The THg deposited in the sediment around BB persists University internal grants to the third author. We are also at a concentration level ten times higher than that in an grateful to Mr. Tsuruda who provided variable assistance in the uncontaminated environment such as Bajo. The laboratory at the Natural Sciences Laboratory, NIMD. This problemisthatwehaveconfirmedthatMeHg paper is dedicated to the memory of Baby Andini. accumulations can be detected in the biota, including those in humans through the food web, which References indicates that some Hg methylation mechanism(s) is at work in the coastal environment since all the Hg released from anthropogenic sources in this region is Akagi, H., & Nishimura, H. (1991). Speciation of mercury in the environment. In T. Suzuki, N. Imura & T. W. Clarkson inorganic in form. Since the exact kind of Hg (Eds.), Advances in Mercury Toxicology (pp. 53–76). New methylation occurring in the BB environment remains York: Plenum. Water Air Soil Pollut

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