Article pubs.acs.org/est
Tracking the Fate of Mercury in the Fish and Bottom Sediments of Minamata Bay, Japan, Using Stable Mercury Isotopes Steven J. Balogh,*,†,‡ Martin Tsz-Ki Tsui,§ Joel D. Blum,∥ Akito Matsuyama,⊥ Glenn E. Woerndle,§ Shinichiro Yano,# and Akihide Tada∇ †
Moyau Consulting Engineering and Science, St. Paul, Minnesota 55116, United States Metropolitan Council Environmental Services, St. Paul, Minnesota 55106, United States § Department of Biology, University of North Carolina at Greensboro, Greensboro, North Carolina 27402, United States ∥ Department of Earth & Environmental Sciences, University of Michigan, Ann Arbor, Michigan 48109, United States ⊥ National Institute for Minamata Disease, Minamata, Kumamoto 867-0008, Japan # Kyushu University, Faculty of Engineering, Fukuoka, Fukuoka 819-0395, Japan ∇ Nagasaki University, Faculty of Engineering, Nagasaki, Nagasaki 852-8521, Japan ‡
S Supporting Information *
ABSTRACT: Between 1932 and 1968, industrial wastewater containing methylmercury (MeHg) and other mercury (Hg) compounds was discharged directly into Minamata Bay, Japan, seriously contaminating the fishery. Thousands of people who consumed tainted fish and shellfish developed a neurological disorder now known as Minamata disease. Concentrations of total mercury (THg) in recent fish and sediment samples from Minamata Bay remain higher than those in other Japanese coastal waters, and elevated concentrations of THg in sediments in the greater Yatsushiro Sea suggest that Hg has moved beyond the bay. We measured stable Hg isotope ratios in sediment cores from Minamata Bay and the southern Yatsushiro Sea and in archived fish from Minamata Bay dating from 1978 to 2013. Values of δ202Hg and Δ199Hg in Yatsushiro Sea surface sediments were indistinguishable from those in highly contaminated Minamata Bay sediments but distinct from and nonoverlapping with values in background (noncontaminated) sediments. We conclude that stable Hg isotope data can be used to track Minamata Bay Hg as it moves into the greater Yatsushiro Sea. In addition, our data suggest that MeHg is produced in bottom sediments and enters the food web without substantial prior photodegradation, possibly in sediment porewaters or near the sediment-water interface.
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INTRODUCTION The Shin Nippon Chisso Fertilizer Company (Chisso) produced acetaldehyde at their plant in Minamata, Japan, from 1932 through 1968.1 The process involved contacting acetylene gas with a sulfuric acid (H2SO4) solution containing mercury(II) oxide (HgO) as a catalyst.2 Wastewater from the operation was discharged without treatment directly into Minamata Bay, a small embayment on the Yatsushiro Sea. In the mid-1950s, as acetaldehyde production increased, fish-kills in Minamata Bay became common, and cats and birds in coastal villages died in large numbers. In late April, 1956, two young sisters were admitted to a hospital in Minamata, having developed difficulty walking and speaking.3 Days later, on May 1, local health authorities announced “an epidemic of an unknown disease of the central nervous system,” marking the first official recognition of what is now known as Minamata disease. Many other individuals suffering from this disease were soon discovered, and most of them, like these two young girls, were residents of fishing villages along the shores of Minamata Bay. Efforts to uncover the origins of the disease began immediately, ultimately concluding that Minamata disease was methylmercury (MeHg) poisoning due to the consumption of contaminated fish and shellfish. © XXXX American Chemical Society
Mercury (Hg) and MeHg in the Chisso wastewater had contaminated the fishery,1 and fishing villages were the epicenter of the tragic consequences.4 As of 2010, 2,271 individual cases of Minamata disease had been certified, and more than 40,000 people showing partial symptoms had received medical benefits.5 Subsequent studies suggested that 70−150 t of Hg had been discharged to Minamata Bay,6 including 0.6−6 t of MeHg.5 Total Hg (THg) concentrations in the bottom sediments of Minamata Bay were found to exceed 25 μg g−1 (dry weight) over a large area (2.1 km2). Concentrations over 100 μg g−1 were not uncommon, and contamination to a sediment depth of 4 m was observed.1 As part of a comprehensive remediation project initiated in 1977, the portion of the bay closest to Chisso’s Hyakken discharge outlet was sealed off from the rest of the bay by a watertight revetment.7 The enclosed area (0.58 km2) isolated the most highly contaminated sediments, and sediments outside this area with THg concentrations exceeding 25 μg g−1 were suctionReceived: February 4, 2015 Revised: April 9, 2015 Accepted: April 15, 2015
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DOI: 10.1021/acs.est.5b00631 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
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Figure 1. Map showing the sediment sampling sites (⊗) and fish sampling locations in Minamata Bay and the Yatsushiro Sea, Japan.
biogeochemical transformations of that Hg. Particular sources of Hg to the environment may have distinguishable isotopic signatures, allowing Hg from those sources to be traced. A number of recent studies have used the mass-dependent fractionation (MDF) signature of Hg in sediments to trace the sources and track the movement of Hg in aquatic systems.15−21 In addition to MDF, mass-independent fractionation (MIF) can also provide clues about sources and transformations of Hg in environmental compartments. In particular, MIF can provide evidence of photochemical processes (e.g., Hg(II) photoreduction and MeHg photodegradation) in aquatic systems and can inform studies of MeHg uptake in aquatic food webs.22−24 Here, we measured THg, MeHg, and stable Hg isotope ratios (both MDF and MIF) in sediment cores and recent and archived fish from Minamata Bay and in sediment cores from the southern Yatsushiro Sea. We use the data to examine whether a distinct Hg isotope signal can be discerned in the highly contaminated sediments of Minamata Bay and what this can tell us about either the movement of the contaminant Hg outside of Minamata Bay or its uptake into the local aquatic food web.
dredged and deposited within the enclosure. Upon project completion in 1990, the enclosed area was capped and covered with clean topsoil and developed for recreational use. In samples taken in 2002, concentrations of THg in surface sediments in Minamata Bay were generally less than 6 μg g−1 and varied little within the top 6−8 cm, indicating that the most highly contaminated sediments had been removed but suggesting also that substantial sediment resuspension, mixing, and subsequent redeposition had occurred since the dredging project.8 Fish Hg concentrations decreased following remediation9 but remain near the Japanese regulatory limit of 0.4 μg g−1 (wet weight basis) and higher than those found in many other coastal Japanese fisheries. The fate of Hg in the bottom sediments of Minamata Bay, and particularly its export to the greater Yatsushiro Sea, has been a long-standing concern. Early surveys of sediments within and outside Minamata Bay found that THg levels decreased with increasing distance from the discharge point, indicating that Hg was moving out of the bay.1,10 Background concentrations of THg in the sediments of the Yatsushiro Sea are less than 0.1 μg g−1, and levels higher than this have been cited as evidence of Minamata-derived contamination there.11 The southern section of the Yatsushiro Sea (where Minamata Bay is located) was found to have elevated THg levels in sediments (>0.4 μg g−1), attributed to export from Minamata Bay, whereas concentrations in the northern section were near 0.1 μg g−1, apparently uninfluenced by Hg from Minamata Bay.12 While these studies indicated that Hg has been exported out of Minamata Bay and into the southern portion of the Yatsushiro Sea, they could not definitively resolve the provenance of Hg in samples with THg concentrations close to the nominal background concentration of 0.1 μg g−1, such as those in the northern Yatsushiro Sea. Recent advances in the high precision determination of stable Hg isotope ratios provide a powerful new way of addressing questions in Hg biogeochemistry.13,14 The isotopic composition of a particular environmental pool of Hg can be considered a signature of that Hg; it bears evidence of the history of the
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EXPERIMENTAL SECTION Environmental Setting. The Yatsushiro Sea is a semienclosed sea on the west-central margin of Kyushu Island, southwestern Japan (Figure 1). It has a surface area of approximately 1,200 km2 and an average depth of 22 m. Minamata City (2010 population: 27,000) is located on the coast of the Yatsushiro Sea in southern Kumamoto Prefecture. Minamata Bay is a small embayment there, sheltered on the northwestern side by Koiji Island; Fukuro Bay opens on the southern side. The total area of Minamata Bay is approximately 3.82 km2, and the average depth is 16.7 m.25 No rivers flow into the bay, and, historically, the primary point source input to the bay was the wastewater discharged by the Chisso company through the Hyakken drainage ditch at the northeast corner of B
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sediment and fish samples were thermally combusted in a twostage furnace; the gaseous Hg(0) released was oxidized to Hg(II) and trapped in an acidified 1% KMnO4 solution. Removal of matrix interferences from this trap solution was accomplished by additional purge-and-trap steps. All final solutions were adjusted to Hg concentrations between 1.8 and 5.0 ng g−1, and isotope standard (NIST SRM 3133) concentrations were matched (±5%) to sample concentrations for stable isotope measurements. Sample Hg(II) was continuously mixed and reduced with 2% SnCl2. The Hg(0) produced was separated from bulk solution in a frosted glass phase separator and introduced to a Nu Instruments multicollector inductively coupled plasma mass spectrometer (MC-ICP-MS) with a stream of Ar. On-peak zero corrections were applied, and instrumental mass bias was corrected using an internal Tl standard (NIST SRM 997) and sample-standard bracketing at uniform Hg concentration and matrix.30 MDF is reported as δ202Hg and MIF is reported as Δ199Hg, both in permil (‰) and referenced to NIST SRM 3133.14,30 Based on analyses of the UM-Almadén standard, reproducibility statistics (2 SD) for the δ202Hg and Δ199Hg measurements were estimated to be 0.08‰ and 0.04‰, respectively. Quality assurance data are provided in Table S3, and complete data compilations are presented in Tables S4 (sediments) and S5 (fish) in the SI. Fish samples were also analyzed for δ15N (relative to atmospheric N2), δ13C (relative to Vienna Pee Dee Belemnite), %C, %N, and C/N at the Colorado Plateau Stable Isotope Laboratory (CPSIL) at Northern Arizona University (Flagstaff, Arizona, USA). See the SI for details.
the bay. A large portion (1.51 km2) of Minamata Bay was dredged during the sediment remediation project (1977−1990), and the dredge spoils were deposited within the reclaimed landfill area (0.58 km2) at the mouth of the Hyakken drainage. Sediment Sampling and Analysis. In a previous study,25 a total of 67 sediment cores and an additional 40 surface sediment samples were collected in May 2012 from sites within and just outside Minamata Bay. All cores were sectioned at 2.5 cm intervals, and subsamples were analyzed for THg. A complete summary of the methods and results of this project is described in Matsuyama et al.25 Two cores from this sample set were selected here for analysis of stable Hg isotopes. Both cores, labeled “11-8” and “12-5”, were taken at sites on the southern side of the bay at water depths of approximately 10−12 m. Geospatial coordinates for the coring sites are shown in Table S1 (Supporting Information (SI)). Core 12-5 was collected outside the area that had been dredged during the remediation project (Figure 1). This core was selected because the THg concentration-depth profile indicated a subsurface peak exceeding 10 μg g−1, which we thought could be used to characterize the stable Hg isotope signature of the Chisso Hg waste. Core 11-8 was collected from a site within the dredged area. Analysis of this core showed lower THg concentrations than in core 12-5 and background (0.1 μg g−1) and decrease with distance from Minamata Bay, suggesting movement of Hg from the bay into the wider sea.11,12 Water depths in this part of the sea are approximately 20 m. Coring and sample handling procedures were as described previously.25 All cores were sectioned at 2.5 cm intervals, and all subsamples were analyzed for THg. Select subsamples were analyzed for MeHg and stable Hg isotopes. Total Hg concentrations in the Minamata Bay sediments were analyzed during the original project at the National Institute for Minamata Disease (NIMD) by Matsuyama et al.25 In order to obtain directly comparable data for both the Minamata Bay and Yatsushiro Sea sediment THg concentrations, the Minamata Bay samples were reanalyzed along with the Yatsushiro Sea samples for both THg and MeHg in the Balogh lab (St. Paul, Minnesota, USA). Complete details of the analytical procedures and QA data are provided in the SI. Fish Sampling and Analysis. An archive of fish caught in Minamata Bay has been maintained at NIMD since 1978.9 We selected 14 fish spanning the years 1978−2013 for stable Hg isotope analysis. Twelve of the fish were Sebastiscus marmoratus (Japanese Kasago) and two were Sillago japonica (Japanese Shiro-gisu). All fish samples were freeze-dried fillets. Complete length and weight data and locations of capture for all the fish are shown in Table S2 (SI). All fish samples were analyzed for THg and MeHg using procedures described in detail in the SI. Stable Isotope Analyses. The sample processing and analytical methods for stable Hg isotopes have been described previously.26−29 Stable Hg isotope measurements were carried out in the Biogeochemistry and Environmental Isotope Geochemistry Laboratory at the University of Michigan (Ann Arbor, Michigan, USA). Briefly, representative subsamples of the dried
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RESULTS AND DISCUSSION Sediments - Minamata Bay Cores. Concentrations of THg in core 11-8 decreased in a smooth profile with increasing sediment depth, ranging from 3.34 μg g−1 at the sediment-water interface to less than 0.10 μg g−1 below 22.5 cm (Figure 2a; Table
Figure 2. Variation with sediment depth of THg concentration (filled symbols) and δ202Hg (open symbols) for cores 11-8 (a) and 12-5 (b) from Minamata Bay. The error bars for δ202Hg indicate ±1 standard deviation (SD). The uncertainty associated with the THg concentrations is ±2%.
S4, SI). This core was collected within the dredged area; the mean THg concentration in surface sediments (0−2.5 cm) inside the dredged-area was estimated to be 2.74 ± 1.49 μg g−1 in 2012 (mean ±1 SD; A. Matsuyama, unpublished data). The mean THg concentration for the three deepest samples (at 22.5, 25.0, and 27.5 cm) in core 11-8 was 0.090 μg g−1 (SD = 0.006 μg g−1, n = 3), which is less than the nominal background concentration of C
DOI: 10.1021/acs.est.5b00631 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
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Environmental Science & Technology 0.10 μg g−1 for sediments in the Yatsushiro Sea12 but slightly higher than the value of 0.068 ± 0.012 μg g−1 reported by Tomiyasu et al.8 for background sediments in Minamata Bay. Data from 2012 showed a mean THg concentration of 0.092 ± 0.053 μg g−1 in samples below 30 cm depth (n = 26; A. Matsuyama, unpublished data). Using our background concentration of 0.090 μg g−1, naturally occurring background Hg accounts for only about 3% of the THg in our two uppermost samples, with the remaining 97% representing an anthropogenic input. Given the documented magnitude of the historical Chisso Hg discharge into Minamata Bay, all or nearly all of the anthropogenic Hg in these sediments is thought to have originated with Chisso; no other significant point sources have been reported. Atmospheric inputs of Hg to Minamata Bay were recently estimated at 24 μg m−2 year−1 or 92 g year−1.31 Even if it were markedly higher in the past, the relative contribution of atmospheric deposition to Hg levels in Minamata Bay sediments would still have been insignificant due to the sheer magnitude of the Chisso input. The sediment remediation project reduced THg concentrations in sediments throughout the dredged area from >25 μg g−1 to 8.75 μg g−1 or less.7 THg concentrations remain particularly high, however, in some areas outside the dredging limits, especially around Koiji Island and in Fukuro Bay.25 Core 12-5 was collected outside the dredged area, and THg concentrations in this core (Figure 2b) were much higher than those in core 11-8. The highest concentration in this core was 11.1 μg g−1 at a depth of 12.5 cm, and the deepest sample (20 cm) had a concentration of 0.86 μg g−1, well above the background level. Values of δ202Hg in core 11-8 varied with depth, from −0.67‰ in the surface sediment layer (0−2.5 cm) to less than −1.00‰ at depths below 22.5 cm (Figure 2a). Such downcore variation in the Hg isotope composition could result from in situ isotope fractionation processes followed by redistribution or loss of Hg from the sediment column, but a more likely explanation is that this isotopic profile is the consequence of the mixing of two or more sources of Hg of different isotopic compositions.20 As indicated above, the Chisso discharge into Minamata Bay has been the dominant Hg input to sediments there, and the downcore variation in Hg isotope composition in this core is thought here to result from the mixing of Chisso Hg with naturally occurring background Hg. The two uppermost samples we analyzed for stable Hg isotopes, at 0 and 5 cm, each had δ202Hg values of −0.67‰ ± 0.04‰ (the uncertainty represents the mean standard deviation of duplicate measurements performed on 12 sediment samples). As indicated above, these two samples contain 97% anthropogenic Hg, and so these δ202Hg values may be considered signals of the legacy Chisso Hg in this core. The mean value of δ202Hg for the three background samples at the base of core 11-8 was −1.03‰ (SD = 0.02‰, n = 3); this background value is clearly distinct in comparison to δ202Hg values in the contaminated sediments at the top of the core. Values of δ202Hg in core 12-5 (Figure 2b) varied much less than those in core 11-8. The high THg concentrations throughout core 12-5 indicate that almost all of the Hg in this core is contaminant Hg, and the δ202Hg data here are thus mostly representative of the contaminant Hg, showing little of the background isotopic signal. A Two-Component Sediment Mixing Model. If the Hg in Minamata Bay sediments is a mixture of these two components (contaminant and background), then the stable Hg isotope ratios of samples with THg concentrations between these extremes
should fall on a mixing line with background and contaminant values as end-members. In a simple two-component mixing model, the δ202Hgx at a given THg concentration ([THg]x) can be estimated using the δ202Hg values of contaminant Hg (δ202Hgc) and background Hg (δ202Hgbg) as end-members. Using this simple model, we derived the following equation relating the sediment δ202Hg value to the THg concentration (see the SI for details) δ 202 Hg x = δ 202 Hgc + Kδ/[THg]x
where Kδ = [THg]bg × (δ 202 Hg bg − δ 202 Hgc)
and [THg]bg is the background THg concentration. A plot of the δ202Hg data for the Minamata Bay sediment samples vs 1/[THg] is shown in Figure 3a. A linear least-squares
Figure 3. Two-component mixing plots for the Minamata Bay sediments: a) δ202Hg vs 1/[THg]; linear least-squares fit of all data, δ202Hg = −0.031 * 1/[THg] − 0.69, r2 = 0.93 and b) Δ199Hg vs 1/ [THg]; linear least-squares fit of all data, Δ199Hg = 0.013 * 1/[THg] − 0.07, r2 = 0.84. The error bars indicate the uncertainty (±1 SD) in the δ202Hg and Δ199Hg measurements. The uncertainty associated with the THg concentrations is ±2%. Data symbols: □- core 11-8; ○- core 12-5.
fit of the data yields an equation with a y-intercept of −0.69‰ (SE = 0.014‰) and a slope of −0.031‰ μg g−1 (SE = 0.002‰ μg g−1); the adjusted r2 value for the fit is 0.93. Thus, the modelderived estimate for δ202Hgc is −0.69‰. Using our mean background THg concentration for the three deepest samples from core 11-8 ([THg]bg = 0.090 μg g−1), the model yields a value of −1.03‰ for δ202Hgbg, identical to the mean of the three measured δ202Hg values. Similarly, a linear least-squares fit of the Δ199Hg vs 1/[THg] data for the Minamata Bay sediment samples yields an equation with a slope of 0.013‰ μg g−1 (SE = 0.002‰ μg g−1), a yintercept of −0.07‰ (SE = 0.009‰), and an adjusted r2 value of 0.84 (Figure 3b). From this, we estimate Δ199Hgc = −0.07‰ and Δ199Hgbg = 0.07‰. Thus, the parameters of the fitted lines provide estimates of the characteristic δ202Hg and Δ199Hg values in the background Hg and contaminant Hg components of the Minamata Bay sediments. We conclude that this two-component mixing model is sufficient for describing δ202Hg and Δ199Hg values in these Minamata Bay sediment cores. The δ202Hg and Δ199Hg values derived above for both the contaminated sediments and the background sediments in Minamata Bay fall within the ranges of data reported previously for similar sediment matrices. Blum et al.32 reviewed published MDF and MIF data for freshwater and marine sediments, D
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ours. The contaminated YS sediments in our study have the same isotopic composition as the contaminated Minamata Bay source sediments (Figure S1b, SI), indicating that no measurable Hg fractionation has occurred in transit. Sample 3-10 also may contain Hg from another source, but in this case the contributed Hg would have had a more negative δ202Hg value than our background samples from Minamata Bay. Sample 3-10 initially appeared as though it might represent the local background Hg; however, the THg concentration is more than twice the apparent background concentration, and the δ202Hg value seems too low. In contrast to our finding above for the more contaminated YS samples, the far negative δ202Hg value for this lightly contaminated sample could possibly indicate that this is contaminant Hg from Minamata Bay that has undergone fractionation during sediment transport.21 We tentatively conclude that sample 3-10 is not representative of local background conditions, but additional work is needed to adequately characterize the stable Hg isotope properties of background samples in Yatsushiro Sea sediments. The δ202Hg values in Minamata Bay and YS sediments are plotted vs 1/[THg] in Figure S2 (SI). Overall, the twocomponent mixing model for the Minamata Bay samples adequately describes the stable Hg isotope compositions of YS sediments, but further work is needed to characterize the stable Hg isotope properties of background Yatsushiro Sea sediments. Additional samples will also be needed to clarify the possibility of other localized Hg inputs to bottom sediments there. In summary, the data presented here indicate that the stable Hg isotope composition of sediments in the Yatsushiro Sea can be used to track the ongoing efflux of Chisso Hg from Minamata Bay. Minamata Bay Fish. Very high concentrations of THg in fish and shellfish in Minamata Bay were measured following the recognition of Minamata disease in humans in 1956.1,33 THg concentrations in fish were greater than 10 μg g−1 w.w. (multispecies average) in 1960 but dropped to 0.40 μg g−1 w.w. in 1970 following the termination of the Chisso discharge.34 Recent monitoring (2008−2010) found a mean concentration in Kasago of 0.36 μg g−1 (w.w.).35 Descriptive data, THg and MeHg concentrations, and δ13C and δ15N values for the Minamata Bay fish samples are presented in Table S2 (SI). (THg and MeHg concentrations for these fish are reported there and in what follows on a dry weight basis.) MeHg concentrations ranged from 0.08 to 3.92 μg g−1 (dry weight), and the %MeHg (= 100 × [MeHg]/[THg]) ranged from 73 to 104%. Because the two fish species, Kasago and Shirogisu, may differ substantially in their food sources, which could influence the amounts and isotope composition of the Hg they consume and retain, their data are treated here separately. Two fish among the Kasago (#49 and #1371) stand out for their particularly low MeHg and THg concentrations; their THg concentrations (0.27 μg g−1, #49, and 0.11 μg g−1, #1371) were much lower than the mean THg concentration for the other 10 fish (mean = 2.38 μg g−1, SD = 0.74 μg g−1, n = 10). These two fish also had δ13C values (−17.9‰, #49, and −20.3‰, #1371) that were much lower than the mean δ13C value for the other 10 Kasago (mean = −14.7‰, SD = 0.64‰, n = 10). In addition, the δ15N value observed for #1371 was 10.6‰, far lower than the mean value for the other 10 fish (13.9‰, SD = 0.85‰); for #49, δ15N = 13.9‰, the same as the mean of the other 10 fish. Kasago are a demersal fish, typically found on rocky bottoms near shore; adults feed primarily on benthic crustaceans, crabs, and smaller fish. Since they feed in the benthic environment, the δ13C values
reporting summarized data for both point source contaminated sediments (mean δ202Hg = −0.67‰, 1 SD = 0.78‰; mean Δ 199 Hg = −0.01‰, 1 SD = 0.09‰; n = 185) and uncontaminated background sediments (mean δ202Hg = −1.00‰, 1 SD = 0.48‰; mean Δ199Hg = 0.00‰, 1 SD = 0.13‰; n = 51). Thus, the stable Hg isotope compositions of both the contaminated and background sediments in Minamata Bay fall well within the range of compositions found for other similar samples. A plot of Δ199Hg vs δ202Hg for all analyzed sediment samples in the two Minamata Bay cores is shown in Figure S1a (SI). Contaminated sediments in these cores display distinct and nonoverlapping δ202Hg and Δ199Hg values relative to the uncontaminated background sediments. The mean δ202Hg value of the contaminant Hg is statistically distinguishable from that of the background Hg (p < 0.001). Similarly, the mean Δ199Hg value of the contaminant Hg is statistically distinguishable from that of the background Hg (p < 0.01). Sediments - Yatsushiro Sea Cores. The distinct dissimilarity between the stable Hg isotope signals characterizing the contaminated and background sediments in Minamata Bay was used to track the movement of Chisso Hg from Minamata Bay into the wider Yatsushiro Sea (YS). Our data at the five sampling sites in the YS (Table S4, SI) show a mean THg concentration of 0.55 μg g−1 (SD = 0.20 μg g−1; n = 5) in the surface samples (0−2.5 cm) of the five cores. The least concentrated sample from these cores was 3-10 with a THg concentration of 0.12 μg g−1, which was well above the mean background level ([THg]bg = 0.053 μg g−1; SD = 0.010 μg g−1, n = 9) we calculated for the southern YS from the data of Tomiyasu et al.11 The Δ199Hg vs δ202Hg data for the YS sediments are shown in Figure S1b (SI) along with the comparable data for the Minamata Bay sediments. Nine of the 12 YS samples cluster in the same region of the plot as the contaminated Minamata Bay samples. In Table S4 (SI), the “anthropogenic mass fraction” (AMF) column shows estimates of the portion of the total amount of Hg in each sample that is of anthropogenic origin (i.e., not naturally occurring); it is calculated as AMFx = 100 × ([THg]x − [THg]bg)/[THg]x. The AMF values in these nine YS samples were all greater than 80%, indicating substantial anthropogenic inputs of Hg to these sediments. The mean δ202Hg and Δ199Hg values for these nine samples were −0.71‰ (SD = 0.04‰) and −0.06‰ (SD = 0.03‰), respectively. If we consider only the six most contaminated YS samples (#3-1, 3-4, 4-1, 5-4, 6-1, and 6-4; mean AMF = 92%), the mean δ202Hg and Δ199Hg values are −0.69‰ (SD = 0.06‰) and −0.07‰ (SD = 0.03‰), respectively. These values are indistinguishable from the values for the contaminated Minamata Bay samples (δ202Hgc = −0.69‰ and Δ199Hgc = −0.07‰) derived from the twocomponent mixing model. The two least contaminated YS samples (3-10, [THg] = 0.12 μg g−1, AMF = 56%; and 5-8, [THg] = 0.16 μg g−1, AMF = 68%) fall outside this cluster, toward the background values, as expected. Sample 3-1 ([THg] = 0.59 μg g−1), on the other hand, plots rather far to the higher δ202Hg side of the data for Minamata Bay. This may indicate that another source of Hg has contributed to sample 3-1. Overall, however, the Hg isotope signatures for the most contaminated YS sediments are indistinguishable from those of the heavily contaminated sediments of Minamata Bay. Natural geochemical processes (e.g., Hg(II) photoreduction and adsorption) may lead to Hg fractionation during sediment transport in some systems,21 but these processes do not appear to be critically important in E
DOI: 10.1021/acs.est.5b00631 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
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Environmental Science & Technology in Kasago should reflect those at the base of the benthic food chain. France36 found that marine benthic algae (mean δ13C = −17‰) are more positive in δ13C values compared to marine phytoplankton (mean δ13C = −22‰) due to lower water turbulence in the benthic environment. The very low δ13C values for #49 and #1371 indicate that they foraged at a higher position in the water column compared to the other fish. The very low THg concentration and low δ15N value in #1371 suggest that this fish was feeding at a lower trophic level than the other Kasago. This fish also had the lowest %MeHg (73%), further indication that it occupied a lower trophic position.37 Neither the δ15N value nor the %MeHg (98%) for fish #49 suggest that this fish ate at a different trophic level than the other 10 Kasago. Takai et al.38 studied δ13C and δ15N in demersal fish and invertebrates in the Seto Inland Sea, Japan, finding more positive δ13C values (−17.0 to −13.0‰) in 92% of the fish; the values were similar to those of benthic crustaceans, epilithic microphytobenthos, and macroalgae and different from δ13C ranges for pelagic particulate organic matter and zooplankton. Our data suggest that 10 of our Kasago fit this description for demersal fish, but the two fish with lower δ13C values likely were feeding at a higher position in the water column, and #1371 occupied a lower trophic level than the others. Minamata Bay Fish − Stable Hg Isotopes. Kwon et al.39,40 demonstrated the absence of stable Hg isotope fractionation during trophic transfer in freshwater and marine fish raised in captivity, finding that the Hg isotope composition in food sources at the bottom of the food web was displayed in consumers at higher trophic positions. Thus, the isotopic composition of Hg in our Minamata Bay fish was set when that MeHg was taken up into the food web. Photochemical reactions of MeHg have been found to result in substantial levels of both MDF and MIF. In laboratory experiments, Bergquist and Blum26 found that MeHg remaining in fresh water during the photochemical demethylation of MeHg complexed with natural dissolved organic carbon (DOC, 1 mg L−1) maintained a Δ199Hg/δ202Hg ratio of 2.43 ± 0.10 and a Δ199Hg/Δ201Hg ratio of 1.34 ± 0.04. Similar data for photochemical MeHg degradation in seawater at typical marine MeHg/DOC ratios are not available, but Blum et al.23 found a Δ199Hg/δ202Hg ratio of 2.64 ± 0.24 in 28 fish of nine different species captured in the central North Pacific Subtropical Gyre near Hawaii, attributing it to photochemical demethylation. Several studies of Hg MIF in marine fish23,27,41,42 have found that Δ199Hg varies linearly with Δ201Hg with a slope of 1.20 ± 0.01, somewhat less than the value of 1.34 ± 0.04 experimentally observed by Bergquist and Blum26 for photodemethylation of MeHg (DOC, 1 mg L−1). The discrepancy may be attributed to different ligands binding the MeHg in the laboratory experiments versus those in natural waters.23,43 Kasago, 1993−2010. Our data for Δ199Hg vs δ202Hg in the three Kasago caught during the sediment remediation project (1978−1990) in Minamata Bay are shown with filled diamonds in Figure 4, while data for nine Kasago caught after the completion of the project (1993−2010, i.e., “postproject”) are shown with open diamonds. A compilation of all the Hg isotope data is provided in Table S5, SI. We consider the postproject fish here first. A linear least-squares fit of the postproject fish data yields a slope of 2.42 (SE = 0.15, r2 = 0.99), close to the value of 2.43 ± 0.10 found for photodemethylation of MeHg by Bergquist and Blum.26 A plot of Δ199Hg vs Δ201Hg for the postproject data also shows a linear variation, and a fitted slope of 1.17 (SE = 0.03, r2 = 0.99), close to the value of 1.20 found in
Figure 4. Plot of Δ199Hg vs δ202Hg for the Minamata Bay sediment and fish samples. The uncertainty (2 SD) associated with the isotope measurements is 0.08‰ for δ202Hg and 0.04‰ for Δ199Hg. See the text for a description of the fitted lines.
previous studies of marine fish (Figure S3, SI). Thus, our data for the postproject fish, caught between 1993 and 2010, indicate that MeHg in these fish underwent some degree of photodemethylation prior to its incorporation into their food web. We estimated the extent of this MeHg photodemethylation based on the MIF levels in the fish (see the SI, Table S6).22,44 The MeHg in fish #49 and #1371 had similar and relatively high extents of photodemethylation, 26% and 25%, respectively, reflecting the higher MIF observed in these fish. As described above, these two fish were also distinguished by their particularly low THg concentrations and δ13C values. The higher photodemethylation indicated in these fish probably resulted from their feeding in shallower water, where light penetration and photodegradation of MeHg were greater.23 The other seven postremediation fish had much lower degrees of photodemethylation, all less than 10%, with a mean of 6.3% (SD = 2.3%, n = 7). The extent of photodemethylation is very low, perhaps indicating that the MeHg has not mixed thoroughly into the water column, but has been incorporated into the food web soon after production, without substantial exposure to sunlight. As MeHg production in coastal waters is thought to take place primarily in bottom sediments,45 the MeHg in these fish may have been transferred directly into the food web either within the sediments themselves or soon after transfer from the sediments to the water column, i.e., in the bottom water. Kwon et al.42 reported similar observations for the food webs of five estuaries in the northeastern United States. Photochemical degradation of MeHg imparts both MIF and MDF to the residual MeHg prior to its incorporation into the food web. The level of the MDF is directly proportional to that of the MIF. For our postproject fish, the proportionality factor for Δ199Hg vs δ202Hg is 2.42, as seen above. We used this ratio to calculate the increase of δ202Hg in fish due to photodemethylation, assuming Δ199Hgsediment = −0.07‰, the value for contaminated surface sediments in Minamata Bay (see the SI). From this, we estimated the δ202Hg value of the MeHg prior to photodemethylation (Table S7, SI). The range of estimated δ202Hg values for the postproject fish was −0.03‰ to −0.21‰ (mean = −0.11‰, SD = 0.06‰, n = 9). The mean value of δ202Hg of MeHg prior to demethylation is offset from that of THg in the contaminated sediments by 0.58‰ (= −0.11‰ − (−0.69‰)), with individual offset values ranging from 0.48‰ to 0.66‰. If we assume that the MeHg in these fish originated in F
DOI: 10.1021/acs.est.5b00631 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Article
Environmental Science & Technology
production and transfer to biota is different for these fish compared to the Kasago. Additional Shiro-gisu samples are needed to confirm this. The data shown here demonstrate that the stable Hg isotope composition of sediments in the Yatsushiro Sea can be used to track the continuing efflux of Chisso Hg from Minamata Bay. In addition, our results suggest that MeHg in the fish of Minamata Bay currently originates in the bottom sediments and enters the food web without substantial prior photoreduction, possibly in sediment porewaters or near the sediment-water interface. Further work is needed to test some of the conclusions outlined here and to extend the use of stable Hg isotopes to answering other questions related to the Minamata Hg issue.
the contaminated sediments of the bay, this δ202Hg offset represents the MDF that was imparted to the MeHg by the physical, chemical, and biological transformations leading from inorganic Hg in the sediments to MeHg in the water column or porewater prior to any photodemethylation.27 The processes operating here are not completely known or understood, and their MDF characteristics have not all been determined. Nevertheless, the δ202Hg offset may be useful as an indicator of the net MDF during the production of MeHg in these sediments. Our offset value for the postproject Kasago (0.58‰) compares well to the offset value of 0.60 ± 0.16‰ observed for fish and sediment in San Francisco Bay27 and that found by Sherman et al.44 in Florida lakes (mean = 0.45‰, SD = 0.19‰, n = 11). Kasago, 1978−1990. The Δ199Hg vs δ202Hg data for the three Kasago caught during the sediment remediation project (the “inproject” fish) do not fall on the line fitted to the data for the postproject fish (Figure 4). The δ202Hg values for these three fish became steadily more positive, but the Δ199Hg values decreased, from 1978 to 1990. The Δ199Hg values are higher than the contaminated sediment value, indicating some MIF has occurred, which we assume was due to photodemethylation of MeHg prior to uptake in the food web. The degree of photodemethylation indicated by this MIF was less than 5% and similar to that in the most recent (2010) Kasago samples (see the SI). A linear least-squares fit to these three data points yields a line with r2 = 1.00. The remarkable linearity and temporal progression in these data suggest these points may fall on a mixing line connecting two different pools of MeHg that have contributed to MeHg in Minamata Bay fish over the years. This line intersects the line describing the postproject data, which are representative of recent MeHg prior to uptake in the food web, at δ202Hg = −0.01‰, Δ199Hg = 0.16‰. This point may be one end-member of the proposed mixing line, representing the MeHg originating in bottom sediments and being taken up in the food chain. MeHg originally discharged by Chisso is most likely the other end-member of the mixing line for the in-project data. It is well established that large quantities of MeHg were discharged directly into Minamata Bay, especially in the 1950s and early 1960s.46 Some of this MeHg would have been carried out of the bay with the tidal water exchange; but some of it would have been captured in the solids deposited in the bay, and it is this pool that may have contributed MeHg to Minamata Bay fish over an extended period. The quantity of MeHg in this pool would have been depleted over time as loss to the water column and biodegradation in the sediments occurred, and the dredging operation would have removed large quantities of MeHg with the bottom sludge between 1983 and 1987 (the years of active dredging). Based on this proposed scenario, our data would indicate that soon after 1990, when the in-project mixing line intersected the postproject photodemethylation line, the “Chisso pool” of MeHg would have been nearing exhaustion, and subsequently MeHg in Minamata fish would come predominantly from in situ production. Additional Kasago samples from 1978 to 1990 will need to be analyzed to test this proposal. Shiro-gisu. The stable Hg isotopic compositions in Shiro-gisu are shown as diamonds with internal crosses in Figure 4. The data indicate very little MIF in these fish, and essentially no photodemethylation (
