Environ. Sci. Technol. 1997, 31, 2712-2720
Arsenic Biogeochemistry Affected by Eutrophication in Lake Biwa, Japan YOSHIKI SOHRIN* AND MASAKAZU MATSUI Institute for Chemical Research, Kyoto University, Uji, Kyoto 611, Japan MUNETSUGU KAWASHIMA Faculty of Liberal Arts and Education, Shiga University, Otsu, Shiga 520, Japan MASASHI HOJO AND HIROSHI HASEGAWA Department of Chemistry, Faculty of Science, Kochi University, Akebono-cho, Kochi 780, Japan
The seasonal variations of arsenic species in lake water were studied in the mesotrophic northern and eutrophic southern basins of Lake Biwa in Japan. Within the euphotic zone, arsenite [As(III)] increased in spring and fall, and dimethylarsinic acid [DMAA(V)] became the dominant form in summer. Measurable concentrations of monomethylarsonic acid [MMAA(V)] and trivalent methylarsenic species [monomethylarsonous acid, MMAA(III), and dimethylarsinous acid, DMAA(III)] also appeared, although they were always minor fractions. The total arsenic concentration in the euphotic zones remained constant in the northern basin throughout the year. However, it was increased by 2-4 times in the southern basin in summer. The enhancement was caused by the increase of As(V), which was accompanied by the increase of iron, manganese, and phosphorus. The concentration of methylarsenicals per chlorophyll a was lower in the southern basin. These results indicate that the variations of arsenic species in lake water largely depend on biological processes, such as the metabolism of phytoplankton, decomposition of organic matter by bacteria, and microbial reduction of iron and manganese oxides in sediments. Moreover, they show that eutrophication affects the concentration and speciation of arsenic in the lake water.
Introduction Aquatic organisms metabolize arsenic, forming organoarsenic compounds such as non-toxic arsenic-containing ribofuranosides and arsenobetaine (1-4). The metabolism results in the occurrence of thermodynamically unstable arsenite and methylarsenic compounds in natural waters. So far, mainly four arsenic species have been determined in natural waters. Arsenate [AsO(OH)3; As(V)] is the thermodynamically stable form under oxic conditions, of which one or two protons are dissociated at natural pH values. As(V) is a chemical analogue of phosphate and may interfere with oxidative phosphorylation (1). Monomethylarsonic acid [CH3AsO(OH)2; MMAA(V)] and dimethylarsinic acid [(CH3)2AsO(OH); DMAA(V)] also form anions in natural water but are much less toxic than * Corresponding author present address: Faculty of Technology, Kanazawa University, 2-40-20 Kodatsuno, Kanazawa 920, Japan; telephone: 76-234-4792; fax: 76-234-4800; e-mail address: sohrin@ kenroku.ipc.kanazawa-u.ac.jp.
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As(V). Arsenite [As(OH)3; As(III)] is a neutral species at natural pH values and inhibits the activity of enzymes by binding to thiol groups. Since there are large differences in chemical behavior and toxicity among the arsenic species, the determination of speciation is very important in the study of the biogeochemistry of arsenic. Methylated arsenic species in natural waters were first determined by Braman and Foreback (5). Andreae (6, 7) found a positive correlation between the concentrations of As(III) and methylated arsenicals and indicators of primary productivity, e.g., the chlorophyll a (Chl a) concentration and 14C-uptake rate. Froelich et al. (8) attributed the high levels of methylated arsenicals in estuarine water to high productivity under phosphorus-limited and nitrogen-enriched conditions. Howard et al. (9) observed that As(III) and methylated arsenicals appeared in an estuary when the water temperature increased. While the relationships between phytoplankton species composition and the concentrations of As(III) and methylated arsenicals have been studied in estuaries, a clear and general trend has not been observed (10-12). A few studies have been reported on methylated arsenicals in freshwater bodies. In the epilimnion of eutrophic Lake Greifen, Switzerland, As(III) increased beyond As(V) during summer stratification, while DMAA(V) and MMAA(V) were minor components (13). Anderson and Bruland (14) studied a number of lakes in California and found that neither depleted phosphate concentrations nor high dissolved salts correlated with the appearance of methylated arsenicals. They also found that DMAA(V) became the dominant form of dissolved arsenic within the surface photic zone of Davis Creek Reservoir during late summer and fall. Aurilio et al. (15) showed that the arsenic speciation in three lakes of the Aberjona Watershed was far from thermodynamic equilibrium and that DMAA(V) increased in summer and fall. In all these studies, the speciation of arsenic was determined with hydride generation followed by atomic spectrophotometry (16, 17). However, it has been suggested that there are significant amounts of hidden arsenic species in natural waters that are not detected by the normal hydride technique (18). In spite of the substantial accumulation of knowledge on the arsenic speciation in natural waters, the detailed mechanism of appearance of As(III) and methylated arsenicals is still uncertain. Lake Biwa (Figure 1) is the largest lake in Japan. The northern basin is located in a rural area and has a surface area of 616 km2 and an average depth of 44 m (19). The southern basin is located in an urban area and has a surface area of 58 km2 and an average depth of 3.5 m. The waters in the northern basin flow into the southern basin and flow out through the Seta River. The residence time of water is estimated to be 5.5 yr for the northern basin and 0.04 yr for the southern basin. Thermal stratification occurs in the northern basin from May to December, and convection of the lake water occurs from January to April. The dissolved oxygen (DO) concentration in the bottom layer reaches a minimum in late fall but has never been observed to be totally depleted owing to vertical mixing in winter and the inflow of snow-thaw water in early spring. The waters in the shallow southern basin are mixed by wind-driven circulation and are saturated with oxygen throughout the year except special areas. At present, the northern and southern basins are thought to be mesotrophic and eutrophic, respectively. The biomass in the southern basin is much larger than that in the northern basin. It was reported that the mean density of phytoplankton in 1993 was 950 and 2500 cells/mL, respectively, at the centers of the northern and southern basins (20). The southern basin contained more kinds of plankton species in addition to almost all dominant species observed
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1997 American Chemical Society
FIGURE 1. Sampling stations in Lake Biwa. in the northern basin. The lake is an intriguing environment, since one can observe a difference in the progression of eutrophication in the adjoining two basins. We have studied the seasonal variations of arsenic speciation in the two basins of Lake Biwa in order to elucidate the effect of eutrophication on the biogeochemistry of arsenic. In addition, the new analytical technique used in this study (21) allowed us to determine trivalent methyl arsenicals, that is, monomethylarsonous acid, [CH3As (OH)2; MMAA(III)] and dimethylarsinous acid [(CH3)2AsOH; DMAA(III)]. This is the first report of the distribution of trivalent methyl arsenicals in lake water (our preliminary results have appeared in refs 21 and 22).
Experimental Section Sampling. Field investigations were carried out from June 1992 to February 1995. The sampling was usually carried out between 9:00 and 14:00 at approximately 1-month intervals. Water samples were collected at intervals of 5-20 m using a Van Dorn sampler or at 1-2 m intervals using a pump system. The sampling stations are marked on the map (Figure 1). Vertical samples were collected from stations N1 (35°13′ N, 135°59′ E; depth 74 m) off Ohmimaiko in the northern basin. Samples taken from N1 seem to be representative for offshore waters of the northern basin. Surface water samples were collected at stations N2, S1, and S2. Vertical samples were also collected from S3 in the southern basin. Station S3 was located at a dredged area (35°00′ N, 135°54′ E; depth 13 m), which was developed to obtain earth and sand in 19781980 and extended over 500 m2. This area is usually stratified from June to September, and sulfate reduction occurs in the hypolimnion (23). There was an unusually cool and rainy summer in 1993 and an unusually hot and dry summer in 1994. At Hikone, on the east shore of the northern basin, the mean atmospheric temperature in August was 24.3 °C for 1993 and 28.8 °C for
1994, while it is 26.6 °C for normal years (24). The precipitation at Otsu, on the southwest shore of the southern basin, was 527 mm from June to August in 1992, which seems to be a representative value for a typical summer. During the period in 1993, the amount of precipitation (1110 mm) was more than twice that in 1992, and that (231 mm) in 1994, conversely, was less than half that in 1992. Reagents. Standard solutions of 10-3 M MMAA(III) and DMAA(III) were made by dissolving the corresponding bromides (Alfa) in 0.1 M sodium hydroxide under a nitrogen atmosphere. MMAA(III) and DMAA(III) were dissolved as hydroxides by alkaline hydrolysis. The standard solutions were stored in sealed glass tubes to avoid oxidation. For other arsenic stock solutions (10-2 M), the sodium salts [Na2CH3AsO3 prepared by Quick’s method (25) and NaAsO2, Na2HAsO4 and Na(CH3)2AsO2 obtained from Nacalai Tesque] were dissolved in distilled water. They were diluted to the required concentrations daily before use. The organoarsenical solutions were standardized by the hydride generation followed by atomic absorption spectrometry (HG-AAS) after decomposition to As(V). The standards were stable for at least 6 months. Safety Note. The arsenic compounds described in this paper can be severe toxins and should be handled with extreme care. Avoid inhaling arsenic bromides and arsines. Analytical Methods. A detailed description of the analytical method for arsenic is given elsewhere (21). In our method, arsenic(III) and arsenic(V + III) species were determined in separate aliquots. Arsenic(III) species in sample water (500 mL) were extracted with diethylammonium diethyldithiocarbamate into carbon tetrachloride immediately after the sampling. For analysis of arsenic(V + III) and nutrients, samples were filtered with 0.45-µm Millipore filters immediately upon collection and acidified to pH 2 by the addition of 1 M hydrochloric acid. These samples were stored in a refrigerator until analysis. We analyzed arsenic species using the refrigerated samples within 1-2 days of collection, during which period neither losses nor changes of the arsenic species were observed. Arsenic(III) species were back-extracted into an aqueous phase and analyzed using HG-AAS. The concentrations of arsenic(V + III) were measured directly using HG-AAS, and the concentrations of arsenic(V) species were obtained as the difference between those for arsenic(V + III) and arsenic(III). We determined the concentrations of As(V), MMAA(V), DMAA(V), As(III), MMAA(III), and DMAA(III). For each pentavalent species, the detection limit was 0.11-0.14 nM (3 times the standard deviation of the blank), and the precision for five replicate determinations was 1-4% (a relative standard deviation) at 10 nM. For As(III), the detection limit was 15 pM, and the precision was 3% at 2 nM. For each trivalent methylated species, the detection limit was 13-17 pM, and the precision was 5-7% at 0.1 nM. Analyses of other chemical species are described elsewhere (23).
Results and Discussion Total Arsenic. For some samples, ∑As, which was the sum of concentrations for As(V + III), MMAA(V + III), and DMAA(V + III), was compared with total dissolved arsenic (T-As; Supporting Information Table 7). T-As was determined after organoarsenicals and As(III) were converted into As(V) by alkaline persulfate oxidation in a Teflon digestion bomb (21). Howard and Comber (18) broke down the hidden arsenic species to HG-AAS detectable forms with UV irradiation. Such arsenic species also should be included in T-As by our method. ∑As agreed with T-As fairly well considering the analytical precision. Thus, it is assumed that the six arsenic species determined in this study usually constitute a majority of T-As in the waters of Lake Biwa. The T-As is on the same order of magnitude as that reported for unpolluted lakes (5, 6, 13, 14).
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FIGURE 2. Vertical profiles of arsenic species, temperature, DO, Chl a, and DRP at station N1 in 1993: 0, Feb 6; O, May 7; 4, Aug 12; 3, Oct 22. The hatching shows the bottom of the euphotic zone on August 12, which is estimated as 2-3 times the transparency (8.5 m).
FIGURE 3. Vertical profiles of arsenic species, temperature, DO, Chl a, and DRP at station N1 in 1994: 0, Apr 25; 4, Aug 4; ), Oct 3; 3, Nov 19. The hatching shows the bottom of the euphotic zone on August 4, which is estimated as 2-3 times the transparency (10.2 m).
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FIGURE 4. Vertical profiles of arsenic species, temperature, DO, Chl a, and DRP at station S3 in 1993: 0, May 7; 4, Jul 19; ), Aug 12; 3, Sep 11. The hatching shows the bottom of the euphotic zone on August 12, which is estimated as 2-3 times of transparency (2.4 m). For better resolution of the points, logarithmic scales are used for ∑As, As(V), As(III), and DRP. Distributions of Arsenic Species. All data are listed in tables in Supporting Information. Some vertical profiles of arsenic species, water temperature, DO, Chl a, and dissolved reactive phosphorus (DRP) at station N1 and S3 in 1993 and 1994 are shown in Figures 2-5. In the northern basin, ∑As was uniformly distributed through the water column throughout 1993. ∑As and As(V) increased near the bottom during the summer and fall in 1994. In the hypolimnion (>40 m), As(V) was the dominant form of arsenic throughout the observation. In the surface photic zone, arsenic speciation changed seasonally. While As(V) was dominant in the winter mixing period, its concentration decreased in the summer stagnation period. As(III) increased in spring and fall, and DMAA(V) increased and became the dominant species in summer. The concentration of As(III) and DMAA(V) in the epilimnion (11 m in 1993, >7 m in 1994) in summer with the depletion of DO in both years. The species of arsenic most contributing to the increase were As(V) and As(III). In the epilimnion (
