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May 2, 2012 - In December 2007, a mass mortality of isaza (Gymnogobius isaza), a goby fish in Lake Biwa, Japan, was observed under severe hypoxia...
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Hypoxia-Induced Exposure of Isaza Fish to Manganese and Arsenic at the Bottom of Lake Biwa, Japan: Experimental and Geochemical Verification Takaaki Itai,*,† Daisuke Hayase,† Yuika Hyobu,† Sawako H. Hirata,‡ Michio Kumagai,§ and Shinsuke Tanabe† †

Center for Marine Environmental Studies (CMES), Ehime University, 2-5 Bunkyo-Cho, Matsuyama, Ehime 790-8577, Japan Faculty of Regional Sciences, Tottori University, 4-101 Koyama-Minami, Tottori 680-8551, Japan § Lake Biwa Environmental Research Institute, 5-34 Yanagasaki, Otsu, Shiga 520-0022, Japan ‡

S Supporting Information *

ABSTRACT: In December 2007, a mass mortality of isaza (Gymnogobius isaza), a goby fish in Lake Biwa, Japan, was observed under severe hypoxia. Considering the level of manganese and arsenic in the dead isaza during the event was much higher than that in live isaza, hypoxia-induced mobilization of manganese and arsenic and subsequent exposure could be the reason for this adverse effect. However, secondary accumulation of manganese and arsenic after the mortality event could not be ruled out. To test this hypothesis, we conducted tissue distribution/speciation analysis and absorption tests on dead specimens. All the results, particularly the limited absorption of arsenic in the absorption tests, indicated that the isaza were exposed to arsenic before the mortality event. Parallel to this, the geochemical behavior of manganese and arsenic in oxygen-rich conditions (June) and oxygen-poor conditions (December) was investigated to verify the mechanism of exposure. Considerable enrichment of manganese and arsenic in a thin surface layer of sediment was a common feature in all seven stations studied. In the water at the bottom of the lake, a clear increase of arsenite in December was observed, and the manganese level was several hundred times higher in both seasons than the average level of the lake. Although further verification is needed, the data provided here support exposure to manganese and arsenic under hypoxia.

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isaza (Gymnogobius isaza), an endemic goby fish in Lake Biwa, in December 2007 may be an important phenomenon from this perspective.13 At the time of this event, in which about 1 million isaza died, the minimum DO level in the lake bottom was 0.57 mg/L. According to a report detailing the chemical analysis of fish specimens, a clear enrichment of Mn and As in the dead isaza compared with live isaza was observed, with the enrichment of Mn and As in the entire body being (on average) 104 and 14 times, respectively.13 The objective of this study was to verify the possible exposure of isaza to Mn and As under hypoxia. We conducted experimental and geochemical approaches to test this hypothesis. In the experimental approach, absorption tests on dead isaza were conducted to test the “secondary accumulation scenario”, supposing that Mn and As had accumulated from the surrounding media after death. The tissue distribution and speciation of Mn and As in the dead specimens during the mortality event were also investigated. In the geochemical

INTRODUCTION The development of hypoxia in coastal regions and lakes has become a serious problem around the world.1,2 This problem is expected to persist because of the increasing prevalence of hypoxia owing to the combined effects of eutrophication and the rise in temperature caused by climate change.2,3 The latter effect often reduces the ventilation of waters by affecting stratification patterns. This is notably prominent in monomictic lakes that are generally found in temperate regions.4−6 In Lake Biwa, the largest lake in Japan, an annual decrease in the minimum dissolved oxygen (DO) level has been reported (see Supporting Information, Section S1).6 Hypoxia causes various adverse effects in aquatic organisms. The most direct effect is oxygen deficiency. Release of hydrogen sulfide from bottom sediments accelerates several adverse effects.7−9 Similarly, some nutrients and toxic metals can be released from these sediments with the subsequent progression of hypoxia. Hence, the adverse effect of hypoxia on ecosystems is of concern. Mobilization of redox-sensitive elements, e.g., Fe, Mn, and As, in oxygen-depleted lakes has been reported for various regions,10−12 and exposure of benthic organisms to these elements may occur. However, limited evidence of this exposure is available in the literature. The mass mortality of © 2012 American Chemical Society

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January 31, 2012 May 2, 2012 May 2, 2012 May 2, 2012 dx.doi.org/10.1021/es300376y | Environ. Sci. Technol. 2012, 46, 5789−5797

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−25 °C until analysis. The lake bottom water (LBW), defined as the water layer that existed within a depth of 15 cm above the sediment, was also collected. The LBW was simultaneously recovered with the core sampler then collected using a Tygon tube. The water samples were filtered through a membrane filter (0.45 μm) and acidified to pH < 2 with nitric acid immediately after collection. Water samples acidified with HCl were also prepared for high-performance liquid chromatography (HPLC) and inductively coupled plasma mass spectrometry (ICP-MS) analysis according to the procedure recommended by Gault et al.14 Absorption Tests. Artificial Lake Biwa water samples (hereafter ALBW) were prepared first. MgSO4·7H2O (8.7 × 10−5 mol/L), Na2SO4 (2.4 × 10−5 mol/L), NaHCO3 (2.53 × 10−4 mol/L), CaCl2·2H2O (1.42 × 10−4 mol/L), Ca(OH)2 (1.34 × 10−4 mol/L), and KHCO3 (4.2 × 10−5 mol/L) were dissolved in ultrapure water. The pH was adjusted to match the pH of the LBW (pH = 7.8) by purging the samples with CO2 gas. The ALBW were filtered through a 0.45-μm filter before the absorption tests were carried out. Working standard solutions of Mn2+, arsenate, and arsenite were prepared by dissolving MnCl2·4H2O, NaH2AsO4, and NaAsO2, respectively, in anaerobic ALBW in a glovebox purged with Ar gas. Three different levels of Mn2+, arsenite, and arsenate were used in our experiments, in which the middle level of each standard (i.e., Mn = 5000 μg/L and As = 5 μg/L) was adjusted to the highest LBW concentrations observed in this study. Standard solutions with concentrations that were 10 times higher and those with lower concentration levels compared with the standard solutions were also prepared for the absorption tests. Consequently, we prepared solutions with concentrations of 500, 5000, and 50 000 μg/L for Mn, and 0.5, 5, and 50 μg/L for both arsenate and arsenite. Three dead isaza were placed in each of the Mn, arsenite, and arsenate solutions. Three specimens were also placed in the Mn- and As-free ALBW solutions as control samples. These experimental containers were kept for 3 days at 8 °C in a refrigerator, which was the same temperature as that recorded at the bottom of Lake Biwa. After the absorption experiments had been carried out, each isaza specimen was gently rinsed with Milli-Q water and the muscle, skin, gill, viscera, and carcass were dissected. The Mn and As levels in each tissue and in test waters after the experiments, were determined to assess the rate of absorption. The same chemical analysis was conducted on the three dead specimens that had not been immersed in Mn and As solutions, as “raw” samples. Chemical Analysis. The sediment and tissue samples were freeze-dried and homogenized followed by acid digestion using a microwave oven (Ethos D, Milestone Srl, Sorisole, BG, Italy). The concentration of Mn, As, and Fe in the sediment and tissues was measured using ICP-MS (7500cx, Agilent Technologies, Tokyo, Japan). The speciation of Mn and As in the sediment and tissues was measured using X-ray absorption near edge structure (XANES). The concentration of Mn, As, and Fe in the LBW was also measured using ICPMS, and the As speciation was determined using ICP-MS coupled with high-performance liquid chromatography (HPLC; LC10A Series, Shimadzu, Kyoto, Japan). Details of the procedures of the chemical analysis, and the quality of the measurements are given in the Supporting Information (Section S2). Statistical Analysis. Statistical analysis was performed using the data analysis tool contained in the Microsoft Excel

approach, the Mn and As profiles in the sediments and in the water from the lake bottom collected from seven stations at Lake Biwa were assessed, together with the seasonal variation between June and December in 2009. Combining these two approaches, the possible exposure of isaza to Mn and As and their toxic effects were evaluated.

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MATERIALS AND METHODS Sample Collection. In December 2007, 10 dead isaza (DI) were collected from the bottom of the lake (around Station D in Figure 1) using an autonomous underwater vehicle.

Figure 1. (A) Sampling stations at Lake Biwa. (B) Depth profiles of the DO levels in June and December 2009. The dotted and solid lines represent the DO profile in June and December, respectively.

Although the time difference between the mortality event and fish collection could not be determined precisely, it was not very long (e.g., > 1 month) considering the good condition of the DI collected from the lake bottom. Trace element levels in five dead specimens had already been reported previously,1 and three of these specimens were used in this study. Seven live isaza (LI) were collected in March 2007 using a fixed net to compare the trace element distribution between the dead and live specimens. The muscle, skin, gill, viscera, and carcass (mostly bones) of both the DI and LI were dissected to obtain samples for the tissue distribution and speciation analysis. In addition, approximately 80 isaza were caught in Lake Biwa in March 2009 for absorption tests. More than half of these died soon after collection. The dead isaza were immediately stored in a refrigerator at −25 °C until the absorption tests were conducted. Sediment core and lake water samples were collected from seven stations in the northern basin in June and December 2009 (Figure 1A). Before sampling, the core, temperature depth profile, pH, electric conductivity, fluorescence intensity, and turbidity were measured using a fine-scale conductivity− temperature−depth probe. Approximately 30 cm of sediment core was collected in an acrylic column (ID = 10 cm) fitted to a sediment core sampler (Rigosha, Tokyo, Japan). The sediment cores were sliced into 5-mm sections within a day of sampling. Subsamples for X-ray absorption fine structure (XAFS) measurements were contained within an oxygen-impermeable film along with an oxygen absorber to avoid oxidation. These samples were immediately frozen after collection and kept at 5790

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Figure 2. Concentrations of Mn and As in muscle and viscera after exposure to Mn, arsenate, and arsenite. Plots along the “mortality” column are the reference values and represent the Mn content in each tissue, DI-1, DI-2, and DI-3 (Table S1). Results for the other tissues are given in Figures S2− S4.

software package. t-Tests were used to detect statistically significant differences between two groups. A value of p < 0.05 was considered significant.

compared with the control level (p < 0.05) except for the results from gills exposed to a solution containing 500 μg/L of Mn (Figures 2 and S2). The results of each test showed generally high reproducibility with the relative standard deviation of triplicate tests being 10 μg/L) in the test water of the control experiment indicated possible leaching from dead specimens into the water during the test. Similarly, the increase in the level of As in the tissues after exposure to arsenite was mostly insignificant (Figures 2 and S4). Only the skin and carcass after exposure to 50 μg/L of arsenite showed a significant increase (p < 0.05). However, a statistically significant decrease in As from the raw specimen in the control experiment was observed (p < 0.01). The level of As after exposure to arsenite and arsenate was much lower than the level observed in the raw DI, even in the experiments in which a concentration level 10 times higher than the concentration in the water in the bottom of the lake was employed. The concentration of As in the test waters after exposure to arsenate did not decrease after exposure to solutions with concentrations of 0.5 and 5 μg/L of arsenite (Figure 3). A slight decrease in the concentration of arsenite after exposure to the solution with a concentration of 50 μg/L of arsenite indicated some penetration into the dead specimen. The clearly different trend in the absorption behavior of Mn and As in the absorption tests was attributed to the difference in the electrical charge of the dissolved species. Thermodynamic calculations using the visual MINTEQ software package15 indicated that the dominant Mn species in the water at the bottom of the lake was positively charged Mn2+ ions, whereas arsenate existed as negatively charged oxyanions (HAsO42− and H2AsO4−) and arsenite as a neutral molecule (H3AsO3) in the experimental waters. As the surface of freshwater fish is covered with a negatively charged mucus from 5792

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speciation, and absorption tests. The decisive evidence seen in the absorption tests was the limited absorption of arsenite and arsenate from the surrounding water. Neither species was accumulated into the dead specimen even when a solution with a concentration 10 times higher than the concentration of the environmentally relevant level was employed. The tissue distribution and speciation of As also supported the lifetime exposure scenario. If the effect of a secondary accumulation were large, then the concentration of As should have been higher in the surface tissues than in the internal tissues. However, the highest concentration of As was observed in the muscles, and an accumulation in the viscera was also confirmed (Table S1). In addition, speciation of As was clearly different between the DI and the surrounding media. The dominant As species in the water at the bottom of the lake and in the sediments was arsenite and arsenate, whereas the majority of As was possibly associated with sulfur in the isaza, according to the speciation data by XANES (Figures S1 and S5). This difference indicates that the As detected in the DI may not be just contamination obtained through sediment particles. In addition, the XANES data are also consistent with the extraction analysis conducted in a previous study, which suggested that approximately half the As in the DI was unextractable using hexane and water/methanol extractions.13 Muñoz et al. suggested that unextractable As using water/ methanol extraction is strongly bound via As−S bonds in the sulfhydryl groups of proteins.18 Such bonding has been confirmed in freshwater fish in previous studies.19,20 Hence, the XANES data suggest that inorganic As from aqueous exposure is associated with the sulfhydryl groups of some proteins, and hence, the proposition of a lifetime exposure is supported. Geochemical Characteristics of the Bottom of the Lake. The experimental approaches shown above indicated that the isaza were plausibly exposed to As in the water, and to Mn was also suspected as well. On the other hand, the mechanism of exposure and its relationship to hypoxia need to be clarified. Because the mortality event of the isaza occurred in December 2007, we expected that the release of Mn and As would be noticeable in the winter period. The data collected during 2009 indicated that the thermocline shifted downward from June to December, and the DO level exhibited a similar change in profile (Figure 1B). This change showed a vertical mixing with the surface water, and a subsequent recovery of the DO level. Because this mixing was still incomplete below the thermocline, we believe that the DO levels near the bottom of the lake decreased from June to December at all the stations, even though no data for December were available for Stations F and G. However, the lowest DO level found in this study (2.4 mg/L) was still higher than that recorded in 2007 (0.57 mg/L). Despite an apparent decrease in the DO level from June to December, the seasonal change in the level of Mn and As in the LBW was not always consistent with the predictions. In general, both elements were mobilized from the sediments to the water column with decreasing oxygen levels because of the reduction of MnO2 to Mn2+ and arsenate to arsenite.21 Although higher Mn levels were observed in December for Stations A, C, D, E, and G, the opposite trend was observed for Stations B and F (Table 1). Regardless of this seasonal variation pattern, it is noteworthy that the level of Mn in the LBW was at least 14 times higher than the average value in the northern basin (1.76 μg/L)22 in both seasons, except at Station A in June.

Table 1. pH, DO, Mn, and As Levels in LBW in June and December 2009 station A June December station B June December station C June December station D June December station E June December station F June December station G June December

pHa

DOa (mg/L)

Mn (μg/L)

Fe (μg/L)

As (μg/L)

8.1 7.9

8.4 5.4

0.72 180

5.5 18

1.3 1.5

7.8 7.8

5.4 3.7

1500 360

33 28

3.6 1.9

7.8 7.8

6.0 2.4

33 1000

7.6 130

3.1 4.8

7.8 7.8

6.7 3.7

560 690

9.7 51

1.8 2.7

7.8 7.9

7.4 4.7

1900 3900

8.0

8.3

560 25

6.2 21

1.9 1.4

7.9

7.8

140 580

4.4 13

1.5 1.4

18 180

3.9 6.8

a

pH and DO were measured by CTD and the values found at the deepest depth (ca. 1 m above the sediment surface) were used.

In a manner similar to Mn, the level of As in the LBW was higher in June at Stations A, C, D, and E, and higher in December at Stations B, F, and G. Nevertheless, consistently higher levels were found in December when we considered only arsenite (Figure S6). In December, the level of arsenite was markedly high at Stations C, D, and E around the deepest part of the lake. Iron is a key element that controls the behavior of As, as iron (oxy)hydroxide is the most important natural adsorbent of both arsenate and arsenite.23 An increase in the level of Fe in the LBW from June to December indicated a reduction in the Fe (oxy)hydroxide content owing to a decrease in the DO level. This is consistent with a possible increase in arsenite from June to December (from summer to winter). The depth profiles of Mn and As in the sediments measured in this study showed a clear surface enrichment of these elements over a depth of ca. 2 cm (Figures 4 and S7). These elements are probably of natural origin, and accumulate by the upward diffusion of reduced species (Mn2+ and arsenite) and subsequent oxidation on the surface of the sediments,24−26 although the speciation results of these elements in the sediments suggested that this scenario is somewhat oversimplified (see SI, Section S7). This considerable enrichment of Mn and As in the thin surface is the most important geochemical characteristic of the lake. If the DO level decreased to a sufficiently low level to reduce MnO2, then a high concentration of Mn and As would probably be released into the water column. Possible Exposure of the Isaza to Mn and As. The levels of Mn and As in the dead isaza collected from the bottom of Lake Biwa during the mortality event in 2007 were, on an average value basis, 104 and 14 times higher, respectively, than those in the specimens captured alive.13 This enrichment is also supported by the tissue distribution analysis in this study (Table S1). Several reports have shown that the trace element level in the northern basin of Lake Biwa is generally stable in 5793

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Figure 4. Depth profiles of Mn, Fe, and As from sediments in Stations B, D, and G. Solid circle and triangle represent the data in July and December2009, respectively.

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fathead minnow is 50 000, 53 000, and 18 000 μg/L, respectively, and the 96-h LC50 value of arsenite for fathead minnow is 1 000 000 μg/L.31 The level of arsenate and arsenite observed in our study was much lower than these threshold levels. Hence, even if higher concentrations of As were released from the sediments in December 2007, exposure to As cannot be the primary factor in the mortality event. However, it would be reasonable to test for some synergic effects.32 For example, excessive mucus production induced by exposure to metals can cause suffocation in fish,32−34 or it can induce direct detrimental effects on the gill epithelium.35 In addition, based on our XANES analysis of five tissues (muscle, skin, gill, viscera, and carcass) in the dead isaza, the majority of the As in the internal tissues formed As−S bonds (Figure S1). Because the toxicity of trivalent arsenic is related to its high affinity for the sulfhydryl groups of biomolecules, such as GSH, lipoic acid, and the cysteinyl residues of many enzymes,36 the toxic effect of exposure to As is still an important test. Implications for Other Lakes. The results of this study suggest that a possible ecotoxicological effect of a hypoxiainduced mobilization of trace elements is a valuable focus of research for various aquatic ecosystems. From a geochemical point of view, Lake Biwa has two important factors that suggest the bottom of the lake is an environment with a high risk of exposure to Mn and As. First, the background level of Mn and As in the sediments is high. The level of Mn and As below the enriched layer was found to be 4000−5500 mg/kg and 40−60 mg/kg, respectively (Figure 4), whereas the average level in the upper continental crust is 600 and 1.5 mg/kg, respectively.37 This feature may allow these elements to accumulate in the enriched layer to considerably higher levels. Second, Lake Biwa is a monomictic lake, but vertical mixing will gradually decrease as global warming intensifies.6,38 This will constitute a very important change, because the formation of a Mn- and Asenriched layer is unlikely if an anoxic layer prevails at the bottom of the lake. In some holomictic lakes, deoxygenation of the bottom water has already occurred because of climate change.39,40 Lake Ikeda in Japan has such a history, and the bottom of this lake has been permanently anoxic since 1986.41 In such environments, the release of Mn and As is possible during the transition period from being holomictic to meromictic. That a similar event may occur in Lake Biwa in the near future is of great concern. Furthermore, similar phenomena may arise in other holomictic lakes.

winter, when a vertical circulation of the lake water occurs, except in zones close to the atmosphere−water and water− sediment interfaces.22,27 As the isaza undertake a daily migration from the bottom to the surface of the lake, then their general level of exposure should be close to the average value.27 Hence, we assumed that the waterborne level of Mn and As in winter represented the average exposure value. These values were 0.21 and 0.70 μg/L for Mn and As, respectively.22 The level of manganese in the LBW at all seven stations was considerably higher than this level. This result suggests that organisms living at the bottom of the lake have a high risk of exposure to Mn. Although the absorption tests indicated that a secondary accumulation of Mn after death could have made a contribution, exposure to Mn was likely to have been important, based on the geochemical perspective. The level of As at all the stations was also higher than the average value of dissolved As in the northern basin of Lake Biwa (0.70 μg/L).22 The highest concentration of As observed at Station E in December (6.8 μg/L) was 9.7 times higher than the average value. This enrichment was moderate compared with the enrichment of Mn. Hence, from a geochemical point of view, the risk of exposure to As was not high compared with that for Mn. Nevertheless, the results of our absorption tests and the different speciation of As between the dead isaza and the sediments indicate that As enrichment in the dead isaza cannot be explained by secondary accumulation. Two factors need to be considered to explain the accumulation. First, the lowest level of DO observed in this study (2.4 mg/L) was still higher than that observed in 2007 (down to 0.57 mg/L). A higher level of As in the LBW is observed with decreasing level of DO. Second, the speciation of As needs to be considered. Despite a small seasonal variation in the total level of As in the LBW, the level of arsenite was 3.4−19 times higher at Stations C, D, and E in December than in June (Figure S6). Furthermore, arsenite has a greater ability to be absorbed gastrointestinally in biota than arsenate does,28 and has a high affinity toward thiol-rich peptides and proteins.29,30 Hence, arsenite can be more bioaccumulative than arsenate. Laboratory experiments need to be conducted to assess the potential release of arsenite as a function of the level of DO. Finally, we have to consider other possible pathways for exposure to Mn and As. Diet and sediment particles are possible candidates. As mentioned in the SI (Section S8), the released Mn and As will be returned to the sediment surface by precipitation in a DO-rich situation. Future studies are needed to clarify this process. Anomalous release of Mn and As by any kind of geothermal anomalies/eruptions may also be possible to be considered apart from hypoxia, although historical data of the lake suggest that contribution by this process is low. Toxicity Assessment. According to the ECOTOX database of the United States Environmental Protection Agency (U.S. EPA), the LC50 value of Mn in freshwater fish is usually >10 000 μg/L.31 Rainbow trout shows the highest sensitivity to Mn among common experimental fish, and the LC50 value for this species is reduced to 2910 μg/L.31 Although data for the LBW were taken at a depth of only 15 cm above the lake sediment, the level of Mn at Station E in December was above this value. Data on the LC50 value for Mn in isaza are not available yet, but a toxicity evaluation of Mn will be an important matter for future studies. Arsenic is well-known as a toxic element, but the toxicity of arsenate and arsenite is not high relative to Mn. For example, the 96-h LC50 value of arsenate in bluegill, rainbow trout, and

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ASSOCIATED CONTENT

S Supporting Information *

Detailed sampling and analytical methods, results of tissue distribution/speciation and geochemical data, brief discussion on geochemical part. This information is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]; tel/fax: +81-89-927-8196; present address: Center for Marine Environmental Studies, Ehime University, Bunkyo-cho 2-5, Matsuyama, Ehime 7908577, Japan. Notes

The authors declare no competing financial interest. 5795

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[As(III) + As(V)] in seafood products by acid digestion, solvent extraction and hydride generation atomic absorption spectrometry. Analyst 1999, 124 (4), 601−607. (19) Larsen, E. H.; Engman, J.; Sloth, J. J.; Hansen, M.; Jorhem, L. Determination of inorganic arsenic in white fish using microwaveassisted alkaline alcoholic sample dissolution and HPLC-ICP-MS. Anal. Bioanal. Chem. 2005, 381 (2), 339−346. (20) Allen, T.; Rana, S. V. S. Effect of arsenic (AsIII) on glutathionedependent enzymes in liver and kidney of the freshwater fish Channa punctatus. Biol. Trace Element Res. 2004, 100 (1), 39−48. (21) Stumm, W., Morgan, J. J. Aquatic Chemistry; Wiley: New York, 1996. (22) Mito, S.; Sohrin, Y.; Norisuye, K.; Matsui, M.; Hasegawa, H.; Maruo, M.; Tsuchiya, M.; Kawashima, M. The budget of dissolved trace metals in Lake Biwa, Japan. Limnology 2004, 5 (1), 7−16. (23) Dixit, S.; Hering, J. G. Comparison of arsenic(V) and Arsenic(III) sorption onto iron oxide minerals: Implications for arsenic mobility. Environ. Sci. Technol. 2003, 37 (18), 4182−4189. (24) Takamatsu, T. Limnological and Environmental Studies of Elements in the Sediment of Lake Biwa; Research Report 75; National Institute for Environmental Studies: Japan, 1985. (25) Balzer, W. On the distribution of iron and manganese at the sediment/water interface: Thermodynamic versus kinetic control. Geochim. Cosmochim. Acta 1982, 46 (7), 1153−1161. (26) Balistrieri, L. S.; Murray, J. W.; Paul, B. The biogeochemical cycling of trace metals in the water column of Lake Sammamish, Washington: Response to seasonally anoxic conditions. Limnol. Oceanogr. 1992, 37 (3), 529−548. (27) Sugiyama, M.; Hori, T.; Kihara, S.; Matsui, M. Geochemical behavior of trace elements in Lake Biwa. Limnology 2005, 6 (2), 117− 130. (28) Zielhuis, R. L.; Wibowo, A. A. E. Standard setting and metal speciation: Arsenic. In Changing Metal Cycles and Human Health; Nriagu, J. O., Ed.; Dahlem Konferenzen, Springer: Berlin, 1984; pp 323−344. (29) Scott, N.; Hatlelid, K. M.; MacKenzie, N. E.; Carter, D. E. Reactions of arsenic(III) and arsenic(V) species with glutathione. Chem. Res. Toxicol. 1993, 6 (1), 102−106. (30) Kitchin, K. T.; Wallace, K. The role of protein binding of trivalent arsenicals in arsenic carcinogenesis and toxicity. J. Inorg. Biochem. 2008, 102 (3), 532−539. (31) U.S. Environmental Protection Agency. ECOTOX database system; accessed April 20, 2012; http://cfpub.epa.gov/ecotox/ advanced_query.htm. (32) Miller, T. G.; Mackay, W. C. Relationship of secreted mucus to copper and acid toxicity in rainbow trout. Bull. Environ. Contam. Toxicol. 1982, 28 (1), 68−74. (33) Gorski, J.; Nugegoda, D. Toxicity of trace metals to Juvenile abalone, Haliotis rubra following short-term exposure. Environ. Contam. Toxicol. 2006, 77 (5), 732−740. (34) Bhattacharya, S.; Bhattacharya, A.; Roy, S. Arsenic-induced responses in freshwater teleosts. Fish Physiol. Biochem. 2007, 33 (4), 463−473. (35) Alazemi, B. M.; Lewis, J. W.; Andrews, E. B. Gill damage in the freshwater fish Gnathonemus petersii (Family: Mormyridae) exposed to selected pollutants: An ultrastructural study. Environ. Technol. 1996, 17 (3), 225−238. (36) Aposhian, H. V.; Aposhian, M. M. Arsenic toxicology: Five questions. Chem. Res. Toxicol. 2006, 19 (1), 1−15. (37) Taylor, S. R.; McLennan, S. M. The geochemical evolution of the continental crust. Rev. Geophys. 1995, 33 (2), 241−265. (38) Endoh, S.; Yamashita, S.; Kawakami, M.; Okumura, Y. Recent warming of Lake Biwa water. Jpn. J. Limnol. 1999, 60 (2), 223−228 (in Japanese).. (39) Coats, R.; Perez-Losada, J.; Schladow, G.; Richards, R.; Goldman, C. The warming of Lake Tahoe. Climate Change 2006, 76 (1−2), 121−148. (40) Jankowski, T.; Livingstone, D. M. Consequences of the 2003 European heat wave for lake temperature profiles, thermal stability,

ACKNOWLEDGMENTS This work was supported by a Grant-in-Aid for Scientific Research for Young Scientists provided by the Ministry of Education, Culture, Sports, Science, and Technology, Japan (MEXT). This work was also supported by a Research Grant for Young Scientists in the Global Center of Excellence Program of Ehime University, “Center of Excellence for Interdisciplinary Studies on Environmental Chemistry” from MEXT, and the Japan Society for the Promotion of Science (JSPS). The X-ray absorption experiments were performed with the approval of KEK (Proposals 2009G632 and 2011G152).

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REFERENCES

(1) Diaz, R. J. Overview of hypoxia around the world. J. Environ. Qual. 2001, 30 (20), 275−281. (2) Diaz, R. J.; Rosenberg, R. Spreading dead zones and consequences for marine ecosystems. Science 2008, 321 (5891), 926−929. (3) Rabalais, N. N.; Diaz, R. J.; Levin, L. A.; Turner, R. E.; Gilbert, D.; Zhang, J. Dynamics and distribution of natural and human-caused hypoxia. Biogeosci. 2010, 7, 585−619. (4) Straile, D.; Jöhnk, K.; Rossknecht, H. Complex effects of winter warming on the physicochemical characteristics of a deep lake. Limnol. Oceanogr. 2003, 48 (4), 1432−1438. (5) Livingstone, D. M. A change of climate provokes a change of paradigm: Taking leave of two tacit assumptions about physical lake forcing. Int. Rev. Hydrobiol. 2008, 93 (4−5), 404−414. (6) Yoshimizu, C.; Yoshiyama, K.; Tayasu, I.; Koitabashi, T.; Nagata, T. Vulnerability of a large monomictic lake (Lake Biwa) to warm winter event. Limnol. 2010, 11 (3), 233−239. (7) Vaquer-Sunyer, R.; Duarte, C. M. Thresholds of hypoxia for marine biodiversity. Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (40), 15452−15457. (8) Vaquer-Sunyer, R.; Duarte, C. M. Sulfide exposure accelerates hypoxia-driven mortality. Limnol. Oceanogr. 2010, 55 (3), 1075−1082. (9) Vaquer-Sunyer, R.; Duarte, C. M. Temperature effects on oxygen thresholds for hypoxia in marine benthic organisms. Global Change Biol. 2011, 17 (5), 1788−1797. (10) Aurilio, A. C.; Mason, R. P.; Hemond, H. F. Speciation and fate of arsenic in three lakes of the Aberjona watershed. Environ. Sci. Technol. 1994, 28 (4), 577−585. (11) Kneebone, P. E.; Hering, J. G. Behavior of arsenic and other redox-sensitive elements in Crowley Lake, CA: A reservoir in the Los Angeles aqueduct system. Environ. Sci. Technol. 2000, 34 (20), 4307− 4312. (12) Martin, A. J.; Pedersen, T. F. Seasonal and interannual mobility of arsenic in a lake impacted by metal mining. Environ. Sci. Technol. 2002, 36 (7), 1516−1523. (13) Hirata, S. H.; Hayase, D.; Eguchi, A.; Itai, T.; Nomiyama, K.; Isobe, T.; Agusa, T.; Ishikawa, T.; Kumagai, M.; Tanabe, S. Arsenic and Mn levels in Isaza (Gymnogobius isaza) during the mass mortality event in Lake Biwa, Japan. Environ. Pollut. 2011, 159 (10), 2789−2796. (14) Gault, A. G.; Jana, J.; Chakraborty, S.; Mukherjee, P.; Sarkar, M.; Nath, B.; Polya, D. A.; Chatterjee, D. Preservation strategies for inorganic arsenic species in high iron, low-Eh groundwater from West Bengal, India. Anal. Biochem. 2005, 38 (2), 347−353. (15) Allison, J. D.; Brown, D. S.; Novo-Gradac, J. MINTEQ2/ PRODEFA2, A Geochemical Assessment Database and Test Cases for Environmental Systems: Vers. 3.0 User’s Manual; Report EPA/600/391/-21; U.S. Environmental Protection Agency: Athens, GA, 1991. (16) Perez-Vilar, J.; Hill, R. L. The structure and assembly of secreted mucins. J. Biol. Chem. 1999, 274 (45), 31751−31754. (17) Shephard, K. Function for fish mucus. Rev. Fish Biol. Fisher. 1994, 4 (4), 401−429. (18) Muñoz, O.; Vélez, D.; Montoro, R. Optimization of the solubilization, extraction and determination of inorganic arsenic 5796

dx.doi.org/10.1021/es300376y | Environ. Sci. Technol. 2012, 46, 5789−5797

Environmental Science & Technology

Article

and hypolimnetic oxygen depletion: Implications for a warmer world. Limnol. Oceanogr. 2006, 51 (2), 815−819. (41) Hirae, T. Water Quality and Lake Environmental Conditions in Lake Ikeda; Research Report 53; National Institute for Environmental Studies: Japan, 2000 (in Japanese).

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