distribution and accumulation of mercury derived from gold mining in marine environment and its...

Distribution and Accumulation of Mercury Derived from GoldMining in Marine Environment and Its Impact on Residentsof Buyat Bay, North Sulawesi, Indonesia

Markus T. Lasut & Yoshiaki Yasuda &

Evan N. Edinger & Jane M. Pangemanan

Received: 16 April 2009 /Accepted: 14 July 2009 /Published online: 4 August 2009# Springer Science + Business Media B.V. 2009

Abstract Buyat Bay (BB), North Sulawesi, Indone-sia, was a submarine tailings disposal (STD) site foran industrial gold mine that extracted mercury (Hg)-containing ores from 1996 to 2004. To evaluate thedistribution and influence of such a Hg release intothe environment, particularly into BB, we quantifiedthe total mercury (THg) and methyl mercury (MeHg)in the surface sediments (beach, river estuary, andmarine) and biota of the bay, as well as the scalp hairof residents in the adjacent community. A nearbybody of water, Totok Bay, polluted by Hg from

artisanal gold mining, and a reference area of the BajoCoast (Bajo) free of any anthropogenic sources of Hgwere also sampled. Both THg and MeHg weredetected in all samples measured showed concen-trations to be highest at the artisanal mining site,intermediate at the STD site and at their lowest in thecontrol area. THg and MeHg concentrations in marinebiota and human hair increased with trophic levelsand were significantly higher at the STD site thanamong the controls. Besides examining the sourceand distribution of Hg, its accumulation in biota, andits potential impact on humans, we also studied therole of the mine management so as to provide arecommendation for future actions.

Keywords Methyl mercury . Bioaccumulation .

Submarine tailings disposal (STD) . Artisanal mining .

Sulawesi . Indonesia

1 Introduction

Industrial mining of gold and/or cinnabar, whichinvolves the extraction of Hg by the mineralization ofcinnabar (HgS) or as Hg contaminants within other ore-bearing minerals, is considered to be one of the majoranthropogenic sources of Hg into the environment sincethese operations must dispose of tailings containingmercury (Williams et al. 1999; Edinger et al. 2007). AnIndonesian case in point is the Newmont MinahasaRaya gold mine operated in the Buyat–Ratatotok

Water Air Soil Pollut (2010) 208:153–164DOI 10.1007/s11270-009-0155-0

M. T. Lasut (*)Marine Science Department, Faculty of Fisheriesand Marine Science, Sam Ratulangi University,Manado, North Sulawesi, Indonesiae-mail: [email protected]

M. T. Lasut : J. M. PangemananKampus Unsrat Bahu,Manado 95115 Sulawesi Utara, Indonesia

Y. YasudaNational Institute for Minamata Disease,4058-18 Hama,Minamata City, Kumamoto 867-0008, Japan

E. N. EdingerGeography Department,Memorial University of Newfoundland,St. John’s, NL A1B3X9, Canada

J. M. PangemananMedical School, Sam Ratulangi University,Manado, North Sulawesi, Indonesia

district, Minahasa Regency, North Sulawesi, which is asource of Hg through the mineralization of refractorysediment-hosted gold deposits (Turner et al. 1994).

Artisanal gold mining using mercury amalgam-ation is another of the major sources of anthropogenicHg contamination (de Lacerda and Salomons 1998;Malm 1998; Kambey et al. 2001; de Lacerda 2003;Ogola et al. 2002; Limbong et al. 2003), along withacetaldehyde factories (Yasuda et al. 2004), and thefossil-fuel combustion and chlor-alkali industries(Pacyna et al. 2006). Such types of gold miningoperations using mercury amalgamation are wide-spread, especially throughout the developing world(Ogola et al. 2002; de Lacerda 2003), includingIndonesia (James 1994; Kambey et al. 2001; Limbonget al. 2003). In North Sulawesi, Indonesia, environ-mental concerns have arisen based on estimations thatapproximately 200 t of Hg are used annually in suchmining operations (Kambey et al. 2001). Forty to50% of the Hg used in the amalgamation is estimatedto be dumped into rivers as metallic Hg, and anadditional 5% to 10% of the Hg is discharged into theenvironment during the recovery of gold from Hgamalgam. Further estimates have concluded thatapproximately 1.32 kg of Hg is discharged for every1 kg of gold production (Pfeiffer and Lacerda 1988;cf. de Lacerda and Salomons 1998).

In the Buyat–Ratatotok district of North Sulawesi,artisanal gold mining co-exists with industrial goldmining, but involving different watersheds (Edinger etal. 2007). The introduction of Hg into the environ-ment from artisanal mining occurs during the extrac-tion process or through the leaching of waste frombarrels (Kambey et al. 2001), while Hg fromindustrial mines is discharged as tailings high in Hgvia a submarine tailings disposal (STD) system. Theore processing practices of both artisanal and STD-using industrial gold mines carry Hg-containing sedi-ments to the coastal marine eco-system of Totok Bayand Buyat Bay, respectively (Edinger et al. 2007;Fig. 1, map). Although the Hg in industrial minetailings (in the form of synthetic mercuric sulfide) ispurported to be highly insoluble, the stability of Hgand other toxic trace elements in submarine gold minetailings may actually be much lower than previouslyassumed (Blackwood and Edinger 2007). Hg fromboth sources described above potentially enters thefood chain after being methylated at the sediment–water interface (de Lacerda and Salomons 1998) or atthe surface layers of sediment (Goulet et al. 2007).The Hg within processed refractory sulfide ore may bereleased into the air as a result of roasting, or intoseawater from the oxidation of Hg-bearing minerals.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 CoastalWaters, E Buyat Bay

154 Water Air Soil Pollut (2010) 208:153–164

marine system where contamination by any type of Hgor other heavy metals has occurred (Limbong et al.2003; De Luna and Rosales-Hoz 2004; Gemici 2004).

The objective of the present study is to evaluate thedistribution of Hg deposits in sediments and biotaafter Hg is introduced into coastal marine environ-ments through STD, artisanal mining, or the naturalweathering of auriferous rocks. We first document theconcentrations and spatial distributions of total Hg(THg) and methyl Hg (MeHg) in sediments and thelevels of MeHg bioaccumulation in marine biota andhuman hair and then discuss their potential impacts onhuman health.

2 Materials and Methods

2.1 Study Areas

BB is located in the southeastern part of the MinahasaPeninsula, North Sulawesi, Indonesia (Fig. 1) andsituated between two peninsulas, Ratatotok to thenortheast and Bobokan to the southwest. BB opens tothe Maluku Sea (Molucca Sea) to the South andreceives terrigenous runoff from the Buyat catchmentarea (Hendrayana 2005) via the Buyat River (BR). Itmust be emphasized, however, that BR is neveraffected by small-scale gold mining since all the goldin the BR watershed is refractory (Turner et al. 1994;Edinger et al. 2007).

The seabed slope in BB follows the contour of thecoastline and gradually declines to 70–80 m, thendrastically drops to a depth of 100 m approximately700–1,000 m from the coastline; the beach is a sandystretch with rocky shores at either end. The fishingvillage of Buyat Pante (BPV) is located along thebeach front and is inhabited by up to 230 people (54%males and 46% females) comprising 54 households.

A large-scale open pit industrial gold mine usedcyanidation-based extraction to recover gold wasstarted at an area upstream of BR in 1996 (Fig. 1).Approximately 2,000 t day–1 of tailings (45–55%solids, <75-µm-diameter particles) in the form ofslurry containing Hg as fine-grained mercuric sulfidewere disposed of by an STD system throughunderwater pipelines 900 m from the beach, at awater depth of 82 m in BB. The position of thepipeline outfall is around sampling point nos. 8–11,17–19, and 25 as shown in Fig. 1.

Totok Bay (TB) is adjacent to BB, with bothseparated by the Ratatotok Peninsula (Fig. 1). TBreceives water from the Ratatotok catchment areathrough the Totok River (TR), which is a completelydifferent catchment area from that of BR. Since the1980s, TB has been severely affected by artisanalgold mining using Hg amalgamation in the TRwatershed (Hendrayana 2005; Kerebungu 2005),which distributes at the upper land area of theRatatotok, the operation employed a peak level ofabout 5,000 miners during the late 1980s (YayasanLestari, unpublished data).

At the southern part of the Buyat–Ratatotokdistrict, another artisanal gold mining operation hasbeen located at the upland area of Kotabunan (Mintu,Lanut Goropai) since 1974 (Fig. 1). Previous goldmining activity in that area (Tapa Beken and Doup)was conducted by the Dutch from 1936 to 1941,using a hydraulic technique and friable bedrock topartially concentrate the free gold prior to amalgam-ation with Hg (Hendrayana 2005). Approximately500 miners currently work in that area using the sametechniques used at Ratatotok.

At the same time, we also sampled a referencearea, Bajo, on the northwest coast of the MinahasaPeninsula (Fig. 1). Bajo was chosen because it hassimilar characteristics to BB and TB in its beachconditions and habitats, including the fishing com-munities at Bajo Village (BV) where all the residentsconsume fish daily. Although there is no anthropo-genic Hg source in the vicinity of Bajo, the volcanicandesite bedrock present there is similar to much ofthe bedrock in the Buyat–Ratatotok district, and as yetunexploited gold deposits are known to exist in thearea upstream from Bajo (Effendi 1978).

2.2 Sampling Procedure

Sampling of sediments and biota was undertakenduring the dry season in July and August 2004 at thelowest tides in the coastal and marine areas of BB,TB, and Bajo and in the estuarine area of BR,including the BPV and BV for samples of scalp hair.

2.2.1 Sediments

Three groups of sediment samples were collected:beach sediments (<1 m water depth), river sedimentsin the estuary, and seabed sediments (>1 m of water

Water Air Soil Pollut (2010) 208:153–164 155

depth). The beach sediments were collected at fivesites in the intertidal zone in each of the study areas(Fig. 1, nos. 1–5 for BB, nos. 26–30 for TB, and nos.34–38 for Bajo) using a sediment corer made of acommercial 8-cm-diameter polyvinyl chloride pipeable to reach 5 to 10 cm in depth for sampling ofsurface sediment layers. The river sediments werecollected at the BR estuary, about 100 m upstream(Fig. 1, no. 6) and about 250 m upstream (Fig. 1, no.7) from the river mouth using the same corer as notedabove. Each sample was a mixture of five cores (atthe center and four points of a circle 5 m in radius;Yasuda et al. 2004). The seabed sediments werecollected at 12 sites (Fig. 1, nos. 8–11 and 18–25)inside BB, six sites (Fig. 1, nos. 12–17) outside thebay close to Kotabunan and the Kumeke Strait, andthree sites (Fig. 1, nos. 31–33) in TB. The seabedsediment samples were collected using a stainlesssteel Petit Ponar grab sampler (Edinger et al. 2007).

Sampling positions were recorded using a hand-held GPS. The beach samples were thoroughly mixedafter being passed through a 2-mm mesh stainlesssteel sieve (JPHA 2001) to remove pebbles, shells,bits of animal and plant matter, and other foreignobjects. Aliquots (about 500 g) were then placed in asealed polyethylene plastic bag. In the field, allsamples were stored in coolers with chilled coolantgel packs to maintain them at a sufficiently lowtemperature. For Hg analyses, sediment samples wereused after mixing by a quartering method (Yasuda etal. 2004) that divided a pile of sample into four partsand mixed them diagonally, repeating the procedureten times for each sample.

2.2.2 Biota

The soft coral, seaweed, and seagrass samples werecollected using a stainless steel knife to excise parts ofeach sample. Intertidal bivalves Septifer sp., gastro-pods Nerita sp., and crabs were collected manually.Subtidal bivalves, Tridacna sp. and Pinna sp., werecollected using a hammer and chisel while snorkelingat a depth of 1.5 to 2 m. The crabs were collectedalong the beach (Fig. 1, site nos. 1–5, 26–30, and 34–38), while other samples were gathered at selectedsites whenever available (Fig. 1, nos. 1, 30, and 34–38). Fishes were obtained from local fishermen whowere asked to catch them by angling inside the BBareas and along the beach of Bajo. Some sample parts

were usually prepared separately for measurement,e.g., sea grass leaves, seaweed thallus, the basalportions of soft coral, soft body parts of bivalvesand gastropods, and fish muscle. The main body partsof crabs (including the shells) were prepared formeasurement after removing the legs. Further infor-mation regarding samples is presented in Table 1.

All biological samples were freeze-dried prior tomeasurement, with the moisture content of eachrecorded at this step by comparing sampled wetweights and freeze-dried weights. Just prior tomeasurement, biological samples were digested infive to ten times the volume of the sample weight of1 N NaOH placed at 60°C overnight.

2.2.3 Scalp Hair

Sampling of human scalp hair was carried out by asurvey of residents by using a door-to-door orassembly technique in July 2004 at BPV (n=28;male=11, female=17) and BV (n=29; male=15,female=14). Sampling was performed under theprocedures of JPHA (2001). Hair behind the ear wascut 2 cm from the root and placed in individual plasticbags for each participant. Prior to Hg measurements,the samples were rinsed with 1% neutral detergent indistilled water, followed by rinsing twice withdistilled water, ethyl alcohol and acetone, and thendried in desiccators. The dried hair was cut intominute pieces with stainless steel scissors. During haircollection, a questionnaire was administered to eachparticipant covering sex, age, occupation, and food-consumption habits.

2.3 Hg Analysis

All Hg measurements were performed at the NationalInstitute for Minamata Disease, Japan, except forsubmarine sediment samples, which were measured atActivation Labs Inc., in Ancaster, Ontario, Canada. Theseaweed and sea grass samples were stored in arefrigerator, while others were kept in a freezer (−80°C)prior to transportations to the laboratories. All samples(except for hair) were packed in a cooler with coolantgels during transportation.

THg was quantified using cold vapor atomic-absorption spectrophotometry (CV-AAS; Akagi andNishimura 1991; JPHA 2001). Samples (0.3 g or lessof sediment or hair and 0.5 ml or less of 1 N NaOH


digested biological samples) were placed in a 50-mlvolumetric flask, to which 1 ml of water, 2 ml of amixture of nitric acid and perchloric acid (1:1), and5 ml of sulfuric acid were added. The flask washeated at 230°C for 30 min. After cooling, thedigested mixture was diluted up to 50 ml with waterand used as a sample for Hg analysis by CV-AAS. Hgin the aliquot of the sample solution was vaporized byreduction in the presence of 0.l5% (w/v) stannouschloride under vigorous bubbling for 30 s. The Hgvapor was then sent to the atomic-absorption analyzer.This preparation was carried out in an automatedcirculating airflow system (Akagi and Nishimura1991, assembled by Sanso Co. Ltd., Tokyo, Japan).

MeHg concentrations in each sample were deter-mined by an electron-capture detector type gaschromatograph (GC-ECD) after extraction in KOH–

ethanol (1:1) and concentration by dithizone, Na2S,and dithizone extraction (Ikingura and Akagi 1999;JPHA 2001; Matsuyama et al. 2004). According toAkagi et al. (1995), hair MeHg was extracted fromabout 10 mg of each chopped hair sample asdescribed above in 3 ml of 2 N HCl at 100°C for5 min and then transferred from a 1 ml aliquot of 2 NHCl into 4 ml of toluene with vigorous shaking. Eachaliquot of toluene layer was injected into a GC-ECDfor MeHg determination after removing the 2 N HClby suction. Each measurement was conducted withduplicate determination twice.

2.4 Quality Control

As reference materials, we used IAEA-086 (humanhair by IAEA), DORM-2 (dogfish meat by NRC), and

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

Biota Scientificname

CommonEnglish name

Habitat Diet Samplinglocations/sites

No. ofsamples

Tissue sample

Soft coral Sinularia sp. Finger coral Rock/hard bottom Planktonfeeder

BB/no. 1 10 A part

Seaweed Turbinaria sp. Cup coral Coral, rocks, shell,in shallow tropicalreef flats

Producer BB/no. 1 10 Thallus

Seagrass Enhalusacoroides

Eel grass Perennial Producer BB/no. 1 10 Leaf

Bivalve Septifer sp. Box mussel Attached to rocks,dead corals, or theunderside of stones

Suspensionfeeder

BB/no. 1 9 Soft part

Tridacna sp. Giant clam Infaunal inrock/hard bottom

Suspensionfeeder

BB/no. 1BAJO/nos.34–38

34 Soft part

Pinna sp. Penshell Infaunal insand/mudflat

Suspensionfeeder

BAJO/nos.34–38

6 Soft part

Gastropod Nerita sp. Snail Rock/hard bottom Herbivore/omnivore

BB/no. 1 14 Soft partTB/no. 30 9

BAJO/nos.34–38

10

Crabs Uca sp. Fiddler crabs Sandy beach Carnivore BB/nos. 1–5 10 Main part,including shellTB/nos. 26–30 9

BAJO/nos.34–38

10

Fish Epinephelusmerra

Honeycombgrouper

Semi-protectedseaward reefs

Carnivore Inside BB 5 Muscle

Parupeneusmultifasciatus

Manybar goatfish Demersal Carnivore Inside BB 2 Muscle

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


CRM-580 (sediment by BCR) for THg and MeHgdeterminations. Measurements of the reference wereconducted six times for each material. The valuesobtained closely corresponded (about 97%) to thecertified values published by each supplier (Table 2).

2.5 Data Analysis

A comparison of MeHg concentrations and theproportions of MeHg–THg in the beach sedimentfrom all three locations was conducted with a simplestatistical test of one-way analysis of variance (Fowlerand Cohen 1990) applied using the Minitab© statis-tics package. Comparisons of THg concentrations inthe same species of biota from BB and Bajo and ofMeHg concentrations in scalp hair from BPV and BVresidents (location and gender) were done in the samemanner as those for sediment.

3 Results

3.1 Concentration and Distribution of Hg in Sediment

In BB, THg concentrations gradually increased fromthe river estuary (nos. 6–7) to the beach (nos. 1–5)and to the seabed sediment (nos. 8–25). A conversepattern was observed in TB where the beach sediment(nos. 26–30) showed higher THg concentrations thanthe seabed sediment (nos. 32–33). However, thesample at no. 31 had THg concentrations in the rangeof beach sediment (Fig. 2). The concentrations in thebeach sediment samples at Bajo (control; Fig. 1, nos.34–38) were found to be in the same range ofmagnitude, i.e., 10 to 17 ppb.

The highest THg concentrations in BB were foundoutside the bay around site nos. 16 and 12 close tothe Kotabunan and Kumeke Strait areas and at anouter site at the mouth of the bay around nos. 9–10,15, 17–19, and 25. The latter sites were located at theSTD pipeline outfall. Inside the bay, Hg concen-trations tended to increase from the beach to theoutfall areas.

Comparing the THg concentration levels in beachsediment at the three sampling sites, their value werefound to be highest in TB, intermediate in BB, andlowest in Bajo (Fig. 3). The BB samples indicatedmuch lower concentrations of THg than those in TB,though they were ten times higher than that in Bajo.MeHg concentrations were significantly higher in TBthan in BB and at their lowest in Bajo [Fig. 3; one-way ANOVA, F(df, 2)=32.67, p<0.05]. In addition,the ratio of MeHg to THg in average values was 3.2%in Bajo, 2.5% in BB, and 0.4% in TB, which wassignificantly lower in TB than in the other two bays[one-way ANOVA, F(df, 2)=6.38, p<0.05].

3.2 Concentration and Bioaccumulation of Hgin Biota

Concentration of THg in biota derived from BB, TB,and Bajo varied according to the species group anddiet habitat. Although the trophic producer groups,seaweed and sea grass, had low THg concentrationscompared with those of the consumer groups, theywere higher than those of the suspension-feeding softcoral Sinularia sp. Snails (grazers) and bivalves(suspension feeders) showed relatively higher con-centrations than those of intertidal crabs (carnivores),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 ofthe European Communities


THg concentrations in biota of Tridacna sp.(bivalve), Nerita sp. (snail), and Uca sp. (crab) werecompared among the three study areas (Bajo, BB, andTB), as shown in Fig. 4. Except for Tridacna sp. inwhich the THg concentrations from BB were signif-icantly higher (p<0.05) than those from Bajo, thesame pattern of concentrations was exhibited by thosebiota, where TB showed higher concentrations thanthose in BB and Bajo, which was a statisticallysignificant finding (p<0.05). Comparing the concen-trations in biota between BB and Bajo, their valuesshowed an almost 10-fold difference. However, theconcentrations in BB were three to five times lowerthan those in TB.

The concentrations of THg in BB fish (caughtoutside the bay) were higher than those in Bajo, whilethose in BB fish from inside were higher than thosefrom outside. The highest concentrations were foundin the honeycomb grouper, Epinephelus merra, frominside the bay.

THg and MeHg values that accumulated in fishmuscles collected inside BB are depicted in Fig. 5.The average MeHg concentration in fish muscleranged from 46 ppb wet weight in Lutjanus basmirato 359 ppb wet weight in E. merra. The MeHg

0.1

1

10

100

1 10 100 1000 10000THg (ppb)

MeH

g (

pp

b)

Totok

Buyat

Bajo

Fig. 3 Comparison of THg and MeHg concentration levels inthe surface beach sediments from Bajo Coastal Waters, BuyatBay, and Totok Bay

Fig. 2 Concentration of THg in surface sediment samples(river estuary, beach, and seabed) collected from Buyat Bay andthe estuarine area of the Buyat River. The vertical bars indicate

the level of Hg; numbers below are the sampling points;numbers above are the Hg levels (parts per million)


concentrations in E. merra were six times higher thanthose in Lutjanus sp. (42 ppb) and thousands of timeshigher than in Selaroides sp. (0.058 ppb) collected inBajo, whereas MeHg concentrations in L. basmirafrom BB were roughly equivalent to those in Lutjanussp. from Bajo. THg and MeHg were found to bestrongly correlated (r=0.92).

3.3 Concentration of Hg in Hair

Both THg and MeHg were detected in scalp hairsamples collected from BPV and BV residents (30participants aged 20–60 years). The concentrations ofTHg were similar to those of MeHg. The averageMeHg concentration of BPV hair (2.9±0.7 ppm,range 0.5 to 7.8 ppm) was significantly higher thanthat of BV residents (1.0±0.3 ppm, range 0.4 to1.5 ppm; one-way ANOVA, F(df, 1)=28.99, p<0.05).Among BPV residents, the average concentration of

MeHg in adult males (4.2±2.0 ppm, range 0.9 to7.8 ppm) was significantly higher than that in adultfemales (2.2±1.5 ppm, range 0.5 to 6.6 ppm; one-wayANOVA, F(df, 1)=8.87, p<0.05). In BV residents,the average scalp hair MeHg concentration in males(1.0±0.4 ppm, range 0.4 to 1.5 ppm) compared tofemales (0.9±0.2 ppm, range 0.6 to 1.4 ppm) was notsignificantly different [one-way ANOVA, F(df, 1)=1.51, p>0.05, n=29].

4 Discussions

4.1 Source and Distribution of Hg

It was found that those seabed sediment samplescollected inside and outside BB at the area close toKotabunan (nos. 12, 13, and 16) indicated higher levelsof Hg concentration than the area in between (no. 14).Hg deposits outside the bay at the area close toKotabunan may have come from the artisanal goldmining conducted at the upstream area. This source ofHg would scarcely have contributed to Hg depositsinside BB. Therefore, besides the STD as a source, theHg distributed inside BB is considered due to airborneemissions of Hg from the mill, a malfunction occurringwhen the Hg scrubber did not function properly(Edinger et al. 2007). Generally, 40% of Hg in theatmosphere might be deposited in the aquatic envi-ronment as Hg2+ in precipitation, while the remaining60% is deposited on land (Mason et al. 1995).

The ratio of MeHg to THg in sediment varies ateach site. MeHg found in sediments at each samplingsite of the present study is thought to be the result of

0

250

500

750

Con

cent

ratio

ns (

ppb)

THg

MeHg

L. basmira P. multifasciatus E. merra

Fig. 5 Concentration of Hg in fish muscles collected fromBuyat Bay. Correlation rate between THg and MeHg is 0.92

0

250

500

BCW BB BCW BB TB BCW BB TB

Tridacna sp. (Bivalve) Nerita sp. (Gastropod) Uca sp. (Crabs)T

Hg

(ppb

)

Fig. 4 Comparison of THgconcentration in biotacollected from the studyareas. BAJO Bajo CoastalWaters (reference area), BBBuyat Bay, TB Totok Bay.The vertical bars denote95% confidence limits


inorganic mercury methylation mediated by sulfate-reducing bacteria in the sediment (Goulet et al. 2007;Hammerschmidt and Fitzgerald 2004). The ratio ofMeHg to THg in sediment decreased with the increasein THg at the three sampling sites (Fig. 3), indicatingthat the activity of Hg methylation in sediment doesnot necessarily depend on the concentration ofinorganic Hg found in the present study.

4.2 Accumulation of Hg in Marine Biota

The presence of Hg in the sediment inside BB thathad exceeded the natural level (as confirmed by the

seabed sediment samples) caused an increase in Hgaccumulations in the marine biota of the bay sincesediment plays a key role in controlling the metalconcentrations in biota (Blanchette et al. 2001).

Concentrations of Hg in marine biota correlatewith their trophic position (Desta et al. 2007) andhabitat (Bustamante et al. 2006) as predators (con-sumers), showing higher tissue concentrations thanthose in their prey (Bustamante et al. 2006). Thatproved true in the present study (Fig. 6a, b). Intertidalcrabs, however, are an exception within the Hgconcentration hierarchy (see the explanation below).The difference in concentrations between Lutjanus sp.

0.1

1

10

100

1000

TH

g (p

pb)

Sinularia sp. (soft coral)

Turbinaria sp. (seaweed)

E. acoroides (seagrass)

Nerita sp. (gastropod)

Septifer sp. (bivalve)

Tridacna sp. (bivalve)

Uca sp. (Crabs)

L. basmira (fish)

P. multifasciatus (fish)

E. merra (fish)

0.1

1

10

100

1000

TH

g (p

pb)

Nerita sp. (gastropod)

Tridacna sp. (bivalve)

Pinna sp. (bivalve)

Uca sp. (Crabs)

Lutjanus sp. (fish)

Selaroides sp. (fish)

a

b

Fig. 6 a Accumulation ofTHg in biota of BB. bAccumulation of THg inbiota of Bajo


and E. merra reflects the trophic level of each species,and the Hg concentrations in fish meat may reflect theHg level difference at both stations (BB and Bajo).

The low THg concentration in intertidal crabs isprobably under estimated due to some property of thesamples. Hg determination in crabs was conductedusing whole crab bodies since it was nearly impossi-ble to separate their soft parts from their shells. TheHg concentrations in crab shells are 1/10 of that ofcrab muscles (Yasuda, unpublished data). Moreover,the value for crab Hg concentration determined in thepresent study may actually be only around half of thereal value in the soft part of crabs.

In the present study, the processes of methylationand bioaccumulation were found to occur in BB, afinding confirmed by the fact that MeHg was found inboth beach sediment (Fig. 3) and the marine biota(Fig. 4), including fish (Fig. 5). The bioaccumulationprocess also occurred in the study areas of both BB(Fig. 6a) and Bajo (Fig. 6b), as was common innatural marine ecosystems.

4.3 Potential Impact on Humans

Consumption of fish is the main source of MeHg inhumans (Malm 1998; Frery et al. 2001; Yokoo et al.2003; Baker et al. 2004). It is also known that themore fish consumed, the higher the Hg concentrationin human hair (see Dickman et al. 1999; Yokoo et al.2003). In the present study, 29 of 30 participantsreported consuming fish more than four times a week.Finally, our results demonstrating that the hair Hgconcentration in BPV was three times higher than thatin Bajo reflects the difference of Hg concentrations inthe fish of those regions.

4.4 Management Implications

The THg deposited in the sediment around BB persistsat a concentration level ten times higher than that in anuncontaminated environment such as Bajo. Theproblem is that we have confirmed that MeHgaccumulations can be detected in the biota, includingthose in humans through the food web, whichindicates that some Hg methylation mechanism(s) isat work in the coastal environment since all the Hgreleased from anthropogenic sources in this region isinorganic in form. Since the exact kind of Hgmethylation occurring in the BB environment remains

unclear, some appropriate continuous monitoring ofHg methylation and bioaccumulation ought to beestablished as long as Hgwaste disposal activity persistsin BB. Simultaneously, BB residents who had habituallyconsumed fish must be monitored to reduce their Hgintake, and restrictions should be published to promotethe consumption of only fish species lower in Hg.

5 Conclusions

& Hg in the Buyat-Ratatotok area may be traced backto several principal sources: First is the artisanalgold mine activity, second are the tailings of STDfrom industrial mining, and third are the airborneemissions from the industrial gold mine mills.Concentrations of the first two inputs seem to berelatively higher than those of the third. In addition,the riverine input of Hg from the BR due to theterrestrial disturbances associated with industrialmining (Edinger et al. 2007) may be another source.

& Hg in the beach sediment at all three study areas ismethylated in a range of 0.4% to 3.2% of THg.The methyl mercury in BB marine environment,including that in the beach sediment, accumulatesin the marine biota, including in humans, throughthe food web. However, the extent of bioaccumu-lation varies according to species and/or samplinglocation. The concentrations of methyl mercury inthe BB biota are higher than that in the Bajo biota,but lower than in TB.

& Further Hg accumulations are found in BPVresidents’ hair as a reliable evidence of Hg exposure.

Acknowledgments The authors wish to thank the NationalInstitute for Minamata Disease (NIMD), Japan, and the Facultyof Fisheries and Marine Sciences, Sam Ratulangi University,Indonesia, for supporting this investigation. Additional supportwas provided by an NSERC Discovery Grant and by MemorialUniversity internal grants to the third author. We are alsograteful to Mr. Tsuruda who provided variable assistance in thelaboratory at the Natural Sciences Laboratory, NIMD. Thispaper is dedicated to the memory of Baby Andini.

References

Akagi, H., & Nishimura, H. (1991). Speciation of mercury inthe environment. In T. Suzuki, N. Imura & T. W. Clarkson(Eds.), Advances in Mercury Toxicology (pp. 53–76). NewYork: Plenum.


Akagi, H., Malm, O., Branches, F. J. P., Kinjo, Y., Kashima, Y.,Guimaraes, J. R. D., et al. (1995). Human exposure tomercury due to gold-mining in the Tapajos river basin,Amazon, Brazil: Speciation of mercury in human hair,blood and urine. Water, Air and Soil Pollution, 80, 85–94.

Baker, R. F., Blanchfield, P. J., Paterson, M. J., Flett, R. J., &Wesson, L. (2004). Evaluation of nonlethal methods forthe analysis of mercury in fish tissue. Transactions of theAmerican Fisheries Society, 133, 568–576.

Blackwood, G.M., & Edinger, E. N. (2007). Mineralogy and traceelement relative solubility patterns of shallow marine sedi-ments affected by submarine tailings disposal and artisanalgold mining, Buyat–Ratototok district, North Sulawesi,Indonesia. Environmental Geology, 52, 803–818.

Blanchette, M. C., Hynes, T. P., Kwong, Y. T. J., Anderson, M.R., Veinott, G., Payne, J. F., et al. (2001). A chemical andecotoxicological assessment of the impact of marinetailings disposal. Tailings and Mine Waste ‘01. Balkema,Rotterdam, pp. 323–331.

Bustamante, P., Lahaye, V., Durnez, C., Churlaud, C., &Caurant, F. (2006). Total and organic Hg concentrationsin cephalopods from the North Eastern Atlantic waters:Influence of geographical origin and feeding ecology.Science of the Total Environment, 368, 585–596.

De Lacerda, L. D. (2003). Updating global Hg emissions fromsmall-scale gold mining and assessing its environmentalimpacts. Environmental Geology, 43, 308–314.

De Lacerda, L. D., & Salomons, W. (1998). Mercury from goldand silver mining: A chemical time bomb? (p. 146).Berlin: Springer.

De Luna, C. J., & Rosales-Hoz, L. (2004). Heavy metals in tissuesof gray whales Eschrichtius robustus, and in sediments ofOjo de Lebre Lagoon in Mexico. Bulletin of EnvironmentalContamination and Toxicology, 72, 460–466.

Desta, Z., Borgstrøm, R., Rosseland, B. O., & Dadebo, E.(2007). Lower than expected mercury concentration inpiscivorous African sharptooth catfish Clarias gariepinus(Burchell). Science of the Total Environment, 376, 134–142.

Dickman, M. D., Leung, K. M. C., & Koo, L. C. L. (1999).Mercury in human hair and fish: Is there a Hong Kongmale sub-fertility connection? Marine Pollution Bulletin, 9(1–12), 352–356.

Edinger, E. N., Siregar, P. R., & Blackwood, G. M. (2007).Heavy metal concentrations in shallow marine sedimentsaffected by submarine tailings disposal and artisanal goldmining, Buyat–Ratototok district, North Sulawesi, Indo-nesia. Environmental Geology, 52, 701–714.

Effendi, A. C. (1978). Geologic map of the Manado Quadran-gle. North Sulawesi: Geological Survey of Indonesia.

Fowler, J., & Cohen, L. (1990). Practical statistics for fieldbiology (p. 227). England: Wiley.

Frery, N., Maury-Brachet, R., Maillot, E., Deheeger, M., deMerona, B., & Boudou, A. (2001). Gold-mining activitiesand mercury contamination of native Amerindian commu-nities in French Guiana: Key role of fish in dietary uptake.Environmental Health Perspectives, 109(5), 449–456.

Gemici, U. (2004). Impact of acid mine drainage from theabandoned Halikoy Mercury Mine (Western Turkey) onsurface and groundwaters. Bulletin of EnvironmentalContamination and Toxicology, 72, 482–489.

Goulet, R. R., Holmes, J., Page, B., Poissant, L., Siciliano, S.D., Lean, D. R. S., et al. (2007). Mercury transformationsand fluxes in sediments of a riverine wetland. Geochimicaet Cosmochimica Acta, 71, 3393–3406.

Hammerschmidt, C., & Fitzgerald, W. F. (2004). Geochemicalcontrols on the production and distribution of methylmer-cury in near-shore marine sediments. EnvironmentalScience & Technology, 38, 1487–1495.

Hendrayana, H. (2005). Geology of Kotabunan and RatatotkDistricts and relationship with hydrogeology. ConferenceProceeding. International Seminar on Mining, Environ-ment, and Sustainable Development: a lesson from thegold mining controversy in Buyat Bay, North Sulawesi,Indonesia, Manado, Indonesia, 32 pp.

Ikingura, J. R., & Akagi, H. (1999). Methylmercury productionand distribution in aquatic systems. Science of the TotalEnvironment, 234, 109–118.

James, L. P. (1994). The mercury “tromol” mill: An innovativegold recovery technique, and a possible environmentalconcern. Journal of Geochemical Exploration, 50, 493–500.

JPHA (2001). Preventive measures against environmentalmercury pollution and its health effects (p. 112). Japan:Japan Public Health Association.

Kambey, J. L., Farrell, A. P., & Bendell-Young, L. I. (2001).Influence of illegal gold mining on mercury levels in fishof North Sulawesi’s Minahasa Peninsula (Indonesia).Environmental Pollution, 114, 299–302.

Kerebungu, F. (2005). Social environmental study on people ofBuyat. Conference Proceeding. International Seminar onMining, Environment, and Sustainable Development: Alesson from the gold mining controversy in Buyat Bay,North Sulawesi, Indonesia, Manado, Indonesia, 104–111.

Limbong, D., Kumampung, J., Rimper, J., Arai, T., &Miyazaki, N. (2003). Emission and environmental impli-cations of mercury from artisanal gold mining in northSulawesi, Indonesia. Science of the Total Environment,302, 227–236.

Malm, O. (1998). Gold mining as a source of mercury exposurein the Brazilian Amazon. Environmental Research, A7,73–78.

Mason, R. P., Morel, F. M. M., & Hemond, H. F. (1995). Therole of microorganisms in elemental mercury formation innatural waters. Water, Air and Soil Pollution, 80, 775–787.

Matsuyama, A., Liya, Q., Yasutake, A., Yamaguchi, M.,Aramaki, R., Xiaojie, L., et al. (2004). Distribution ofmethylmercury in an area polluted by mercury containingwastewater from an organic chemical factory in China.Bulletin of Environmental Contamination and Toxicology,73, 846–852.

Ogola, J. S., Mitullah, W. V., & Omulo, M. A. (2002). Impactof gold mining on the environmental and human health: Acase study in the Migori Gold Belt, Kenya. EnvironmentalGeochemistry & Health, 24, 141–158.

Pacyna, E. G., Pacyna, J. M., Fudala, J., Strzelecka-Jastrzab, E.,Hlawiczka, S., & Panasiuk, D. (2006). Mercury emissionsto the atmosphere from anthropogenic sources in Europein 2000 and their scenarios until 2020. Science of the TotalEnvironment, 370, 147–156.

Pfeiffer, W. C., & Lacerda, L. D. (1988). Mercury inputs intothe Amazon Region, Brazil. Environmental TechnologyLetters, 9, 325–330.


Turner, S. J., Flindell, P. A., Hendri, D., Hardjana, I.,Lauricella, P. F., Lindsay, R. P., et al. (1994). Sediment-hosted gold mineralisation in the Ratatotok District, NorthSulawesi, Indonesia. Journal of Geochemical Exploration,50, 317–336.

Williams, T. M., Weeks, J. M., Apostol, A. N., Jr., &Miranda, C. R. (1999). Assessment of mercury contam-ination and human exposure associated with coastaldisposal of waste from cinnabar mining operation,Palawan, Philippines. Environmental Geology, 39(1),51–60.

Yasuda, Y., Matsuyama, A., Yasutake, A., Yamaguchi, M.,Aramaki, R., Xiaojie, L., et al. (2004). Mercury distribu-tion in farmlands downstream from an acetaldehydeproducing chemical company in Qingzhen City, Guizhou,People’s Republic of China. Bulletin of EnvironmentalContamination and Toxicology, 72, 445–451.

Yokoo, E. M., Valente, J. G., Grattan, L., Schmidt, S. L., Platt,I., & Silbergeld, E. K. (2003). Low level methylmercuryexposure affects neuropsychological function in adults (p.11). Environmental Health: A Global Access ScienceSource. License BioMed Central Ltd.


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