Higher Mass-Independent Isotope Fractionation of Methylmercury in

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Higher Mass-Independent Isotope Fractionation of Methylmercury in the Pelagic Food Web of Lake Baikal (Russia) Vincent Perrot,*,† Mikhail V. Pastukhov,‡ Vladimir N. Epov,† Søren Husted,§ Olivier F. X. Donard,† and David Amouroux*,† †

Laboratoire de Chimie Analytique Bio-Inorganique et Environnement, Institut Pluridisciplinaire de Recherche sur l’Environnement et les Matériaux, CNRS-UPPA-UMR-5254, Hélioparc, 2 Avenue du Président Pierre Angot, Pau, 64053, France ‡ Laboratory of Geochemical Mapping and Monitoring, Institute of Geochemistry SB RAS, 1A Favorskogo Street, PB-304, Irkutsk, 664033, Russia § Department of Agriculture and Ecology, Plant and Soil Science, University of Copenhagen, Thorvaldsensvej, 401871 Frederiksberg, Copenhagen, Denmark S Supporting Information *

ABSTRACT: Mercury undergoes several transformations that influence its stable isotope composition during a number of environmental and biological processes. Measurements of Hg isotopic mass-dependent (MDF) and mass-independent fractionation (MIF) in food webs may therefore help to identify major sources and processes leading to significant bioaccumulation of methylmercury (MeHg). In this work, δ13C, δ15N, concentration of Hg species (MeHg, inorganic Hg), and stable isotopic composition of Hg were determined at different trophic levels of the remote and pristine Lake Baikal ecosystem. Muscle of seals and different fish as well as amphipods, zooplankton, and phytoplankton were specifically investigated. MDF during trophic transfer of MeHg leading to enrichment of heavier isotopes in the predators was clearly established by δ202Hg measurements in the pelagic prey−predator system (carnivorous sculpins and top-predator seals). Despite the low concentrations of Hg in the ecosystem, the pelagic food web reveals very high MIF Δ199Hg (3.15−6.65‰) in comparison to coastal fish (0.26−1.65‰) and most previous studies in aquatic organisms. Trophic transfer does not influence MIF signature since similar Δ199Hg was observed in sculpins (4.59 ± 0.55‰) and seal muscles (4.62 ± 0.60‰). The MIF is suggested to be mainly controlled by specific physical and biogeochemical characteristics of the water column. The higher level of MIF in pelagic fish of Lake Baikal is mainly due to the bioaccumulation of residual MeHg that is efficiently turned over and photodemethylated in deep oligotrophic and stationary (i.e., long residence time) freshwater columns.

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INTRODUCTION Study of mercury (Hg) is a great concern because this nonessential element can cause serious toxicological effects. Methylmercury (MeHg) remains the principal Hg molecular species easily able to bioaccumulate and biomagnify within aquatic food webs. In aquatic ecosystems, MeHg is predominantly produced from inorganic Hg (IHg) by anaerobic micro-organisms,1 followed by uptake and bioaccumulation within food webs.2−4 Consequently top predators can accumulate high levels of Hg, mostly composed of MeHg (>95%).2,5 Stable isotope analysis of metals is useful for environmental and biomedical research.6 Because Hg has seven stable isotopes able to fractionate during several biotic or abiotic chemical reactions,7−16 several publications have focused on the Hg isotopic signatures of different matrices in nature (soils, sediments, air, biological samples, rocks, hydrothermal ores); these are reviewed elsewhere.17−19 In particular, Hg isotopic © 2012 American Chemical Society

composition in environmental samples is used to track Hg behavior and sources within aquatic ecosystems.17,20−26 Mercury isotopic composition measured in environmental samples is a result of several transformations before and after Hg has entered an ecosystem. Both Hg mass-dependent (MDF) and mass-independent fractionation (MIF) signatures were observed in many samples, which have provided better information on the fate of Hg in aquatic environments. Whereas MDF is known to occur for all Hg isotopes during transformation or exchange reactions, significant MIF is associated mainly with the two odd isotopes (199 and 201) and was identified in few reactions.7,9,14 For example, the extent of MIF exhibited significant variations depending on ecosystem Received: Revised: Accepted: Published: 5902

December 20, 2011 April 2, 2012 April 30, 2012 April 30, 2012 dx.doi.org/10.1021/es204572g | Environ. Sci. Technol. 2012, 46, 5902−5911

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and samples. It was previously shown that stable isotopes of nitrogen and carbon provide powerful tools to estimate the trophic level (TL) and the carbon sources in aquatic food webs.27−29 Hence, combining measurements of stable isotopic ratios of Hg, C, and N in biological samples from marine or freshwater aquatic ecosystems can be useful to study bioaccumulation and trophic transfer of Hg.20,24,26 In a recent study,25 we identified a relation between isotopic ratios and bioaccumulation of Hg in fish from a shallow coastal area of Lake Baikal, which exhibit a distinct isotopic signature from a large downstream reservoir (Bratsk Water-Reservoir), contaminated by former chlor-alkali plants. This work focuses on Hg bioaccumulation in the Lake Baikal (LB) pelagic food web. LB is the oldest, deepest lake in the world and contains approximately 20% of the world’s surface liquid freshwater. Additionally, LB represents a good opportunity to study the fate of heavy metals within the food web, as human impact is minimal and the relationship among biological species, which are mainly endemic, is relatively simple.28 As a result, the pelagic food web of LB is well characterized:28,30 levels of Hg and other trace elements in water and biota are low31−35 in comparison with most other freshwater ecosystems. The aim of this study was to measure Hg stable isotopic composition and Hg species concentrations (i.e., IHg and MeHg) in several biological samples of the LB pelagic food chain (plankton, amphipods, fish and seal muscle), and characterize their diet and TL using δ13C and δ15N signatures, in order to better constrain the sources and accumulation pathways of MeHg in this pristine pelagic environment. Speciation and isotopic ratios of Hg in seals are of special interest as seals are the ultimate top predator in the LB food chain and accumulate relatively high levels of Hg in their organs.32 Moreover, only total Hg concentration has been previously reported in Baikalian seal (Phoca sibirica) tissue.32,33,35 To differentiate pelagic and coastal Hg cycles in this large freshwater lake, previously published results on coastal Hg isotopic ratios and concentration in LB sediments, fish, and plankton 25 have also been compared to the new results presented in this work.

Figure 1. Lake Baikal map and sampling sites of the different biological organisms. Black circles (1, 2, and 3) represent sampling sites of different fish, plankton, and amphipods; gray ellipses (4 and 5) represent sampling sites of different seals. Dashed lines separate the three basins of the Lake. Sampling sites 1, 2, and 3 are called “Listvyanka”, “Selenga river”, and “Maloye More”, respectively. Sampling sites 4 and 5 where seals were collected are called “Southern B” and “Central B”, respectively.

standard for carbon, versus atmospheric nitrogen gas for nitrogen. If not specified in the text, uncertainty of the results is expressed as 1 SD. More details of sample collection and biometry are available in Supporting Information (SI) and in previous publications.25,32,34 2. Instrumentation and Sample Preparation for Total Hg, MeHg, and IHg Concentration Analysis. Concentration of total Hg ([THg]) in samples was measured using a Milestone Direct Mercury Analyzer 80. To measure the Hg speciation, an amount of dried sample (200 mg) was digested in 5 mL of 25% tetramethyl ammonium hydroxyde with microwave-assisted extraction. Then [MeHg] and [IHg] were determined by ID-GC-ICP-MS after aqueous phase derivatization; details of sample preparation and analysis are described in previous works.36,37 The sums of IHg and MeHg concentrations were compared to [THg] analysis to verify the recovery of the extraction. Reference materials certified for MeHg and THg concentration (IRMM BCR-CRM 464 tuna fish from Adriatic Sea and DOLT-4 NRC-CNRC dogfish liver), and CRM BOk-2 9055-2008 (Laboratory of Optic Spectrometry and Standards, Institute of Geochemistry SB RAS, Perca f luviatilis, recommended for [THg]) were also analyzed for total concentration and speciation of Hg (Table S-1). 3. Hg Isotopic Ratio Measurements. Total mineralization of samples was carried out with Digi-Prep MS (SCP Science, Quebec, Canada) or in a closed-valve microwave system (Multiwave ANTON PAAR). Total Hg isotopic compositions of samples were measured for the six most abundant stable Hg-isotopes (198Hg, 199Hg, 200Hg, 201Hg, 202Hg, and 204Hg) relative to the bracketing standard NIST SRM-3133 reference material using cold-vapor-MC-ICP-MS (Nu Instru-

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MATERIALS AND METHODS 1. Sample Collection. Samples of plankton, amphipods, fish, and seal were collected at different LB sampling sites (Figure 1). Macro-zoobenthos amphipods (living at the depth between 210 and 230 m) Ommatogammarus albinus, Ommatogammarus f lavus, and Acanthogammarus godlewskii were sampled at sites 1 and 2. Phyto- and zooplankton were collected at sample sites 1, 2, and 3. Pelagic sculpins from family Comephoridae (Comephorus dybowski and Comephorus baicalensis) and from family Cottidae (Cottocomephorus inermis and Cottocomephorus grewingkii) were sampled at sites 1 and 2. Pelagic fish Coregonus autumnalis migratorius and coastal fish Thymallus arcticus were sampled at site 1, whereas coastal Rutilus rutilus and Perca f luviatilis were collected at sample site 3. Seven seals (Phoca sibirica) were collected at sampling site 4 (Ph. 8, 14, 15, 17) and at sampling site 5 (Ph. 10, 12, 16); these samples were provided by Vinogradov Institute of Geochemistry SB RAS from previous studies.32 Mass, length, and sex of each fish were determined followed by separation of muscle-tissue, which was preserved at −18 °C until analysis. The age of adult seals was determined by analysis of dental and cement growth layers in the teeth. Isotopic δ13C and δ15N were expressed as the deviation (‰) from the Pee Dee Belemnite 5903

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Figure 2. (a) δ15N(‰) versus δ13C(‰) measured in different biological species of Lake Baikal. Other fish as mentioned in the figure are C. aut. migratorius and T. arcticus. Correlations are used to differentiate the different food webs. (b) δ202Hg(‰) versus δ15N(‰) for both pelagic and coastal food webs.

migratorius and Thymallus arcticus) are not on the same regression line which indicates a different trophic chain. The coastal fish roach and perch sampled at Maloye More, which belong to a more complex and diverse ecosystem28 do not seem to have any trophic relationship with the pelagic ecosystem. Average [THg], [IHg], and [MeHg] in fish and seals are expressed on a dry weight basis (reported in Table 1), and other samples are detailed in Tables S-4 and S-5. Pelagic sculpins (Comephoridae, Cottidae), C. aut. migratorius and T. arcticus have significantly lower [THg] than coastal fish from Maloye More (perch and roach), with [THg] equal to 99 ± 85 ng·g−1 (n = 33) and 522 ± 291 ng·g−1 (n = 24), respectively. Among sculpins, a higher concentration of total Hg was found in C. baicalensis (190 ± 122 ng·g−1, n = 7), followed by C. dybowski (86 ± 45 ng·g−1, n = 6). For C. grewinkii and C. inermis fish, Ciesielski et al.32 reported Hg concentrations below the detection limit of their analytical method, in which we measured the lowest [THg] of the Comephoridae with an average of 51 ± 22 ng·g−1, n = 11). These trends of [THg] between Comephoridae fish seem to be consistent with our δ15N results and with previous studies28,30 which reported differences in feeding habits and TL between these sculpins. C. aut. migratorius and T. arcticus also displayed relatively low Hg concentrations (73 ± 14 ng·g−1, n = 8). Phyto- and zooplankton (n = 4) exhibited very low [THg] concentrations, ranging from 2 to 26 ng·g−1. On the contrary, benthic amphipods had relatively high [THg] concentrations (375 ± 212 ng·g−1, n = 4) in comparison with pelagic fish and sculpins which are at least one TL higher than amphipods.28 However, these amphipods can be either necrophagous (they mainly eat dead sculpins), carnivorous, or phytophagous,28,32 thus accumulating Hg from various feeding sources. Similarly, a study in southeast Georgia lakes reported that amphipods had a higher Hg content than fish with higher TL in the food chain, suggesting a complex bioaccumulation pathway in invertebrates.41 We observed significant differences of [THg] between young and adult seal muscle, i.e., young seals (1−1.5 months) had [THg] of 175 ± 31 ng·g−1 (n = 4) whereas adult seals (>1 year) had [THg] of 920 ± 164 ng·g−1 (n = 3). These results are in agreement with those reported by previous studies33,35 for

ments, Wrexham, UK). A desolvating nebulizer system from Nu Instruments (Wrexham, UK) was used to introduce NIST SRM-997 thallium for the instrumental mass-bias correction using the exponential law. Reference materials UM-Almadén (University of Michigan, USA) and BCR-CRM 464 were used as secondary standards with the previously published isotopic composition.7,25,38−40 Mercury isotopic composition of samples was reported using delta notation according to the procedure described in the SI. Reproducibility, precision, and accuracy of the results are reported as δ202Hg ± 2 SD (‰) on the longterm measurements of UM-Almadén during 2 weeks of analysis (−0.59 ± 0.17, n = 21). Details of sample preparation, analytical methods, and reproducibility of standards (Table S-2) are available in the SI.

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RESULTS AND DISCUSSION 1. Trophic Level, Total [Hg], and Hg Species Concentration of Biological Samples. Significant differences of δ15N and/or δ13C were observed among seals, pelagic fish, sculpins, and coastal fish, and also among different sampling sites (Figure 2, Figure S-2). Differences in terms of weight and length among fish are presented in the SI (Figure S3, Figure S-4, and Table S-3). In the Listvyanka site, pelagic sculpins Comephorus and Cottocomephorus display δ15N from 11.6 to 14.2 and δ13C from −30.8 to −25.7, whereas other pelagic fish display δ15N from 11.0 to 12.3 and δ13C from −25.4 to −21.4. In the shallow sampling site of Maloye More, piscivorous fish (Perca fluviatilis) exhibit δ15N from 11.9 to 13.2 and δ13C from −16.5 to −12.5, whereas herbivorous fish (Rutilus rutilus) exhibit δ15N from 8.0 to 9.8 and δ13C from −20.6 to −16.5.25 Seals show the highest values of δ15N ranging from 13.6 to 15.4, and display δ13C from −26.3 to −23.0. These results indicate both different TLs and trophic chains depending on geographical situation and diet. Previous studies have reported sculpins as the main food of Baikalian seals,28,32 which is in agreement with our results of carbon and nitrogen stable isotopes (Figure 2). It should be noted that, similar to the observation of Yoshii et al.,28 we observed a slight decrease of δ15N with age of the seals. Other fish (Coregonus autumnalis 5904


5905

31 7 152 48 38 20 12 10

mean SD mean SD

16 9 12 2

mean SD mean SD

mean SD mean SD

16 7 48 21 52 12

6 1 5 1 13 8

728 184 266 85

144 25 768 124

58 8 57 1

165 111 67 43 9

25 14 19 9 15

[MeHg]

mean SD mean SD mean SD mean SD mean SD mean SD

[IHg]

766 194 278 94

175 31 920 164

75 16 69 3

22 6 53 22 65 12

190 122 86 45 21

[THg]

5 2 4 2

18 2 16 3

21 7 17 2

29 13 10 2 20 11

16 6 25 11 63

%IHg

95 2 96 2

82 2 84 3

79 7 83 2

71 13 90 2 80 11

84 6 75 11 37

%MeHg

1.88 0.20 1.76 0.42 −0.48 0.07 −0.61 0.07

−0.74 0.14 −0.90 0.13

0.88 0.21 0.54 0.07

0.64 0.26 1.30 0.07 0.80 0.05

0.91 0.14 0.83 0.11 −0.02

δ202Hg

2.66 0.26 2.47 0.63

1.13 0.24 0.75 0.19

0.82 0.40 1.89 0.13 1.06 0.02

1.24 0.20 1.15 0.16 −0.34

δ204Hg

0.53 0.15 −0.02 0.09

5.34 0.27 4.55 0.61

5.08 0.68 2.60 0.10

3.75 0.55 5.53 0.12 4.12 0.21

4.36 0.14 4.25 0.18 1.92

δ201Hg

−0.21 0.06 −0.27 0.05

1.04 0.12 0.96 0.21

0.51 0.15 0.36 0.06

0.46 0.21 0.80 0.02 0.45 0.05

0.54 0.09 0.47 0.06 0.09

δ200Hg

1.02 0.22 0.43 0.14

5.47 0.22 4.57 0.66

5.86 0.75 3.05 0.03

4.31 0.63 6.06 0.27 4.73 0.28

4.94 0.21 4.88 0.19 3.26

δ199Hg

0.89 0.017 0.44 0.11

3.93 0.14 3.23 0.47

4.42 0.56 2.20 0.05

3.27 0.46 4.54 0.07 3.51 0.21

3.67 0.15 3.62 0.14 1.93

Δ201Hg

0.03 0.04 0.04 0.05

0.10 0.02 0.08 0.01

0.04 0.05 0.09 0.02

0.11 0.06 0.05 0.02

0.08 0.03 0.05 0.02 0.09

Δ200Hg

1.14 0.23 0.58 0.15

4.99 0.18 4.12 0.62

5.64 0.72 2.91 0.01

4.15 0.60 5.73 0.25 4.53 0.28

4.71 0.22 4.67 0.18 3.26

Δ199Hg

12.7 0.3 9.1 0.6

15.0 0.3 14.0 0.4

11.2 0.2 11.4 1.3

12.3 0.5 13.3 0.1 13.3 0.7

13.5 0.2 13.2 0.4 11.7

δ15N

−14.0 1.2 −18.7 1.4

−24.5 1.5 −24.4 1.1

−25.1 0.3 −18.4 4.2

−29.3 1.0 −26.7 0.6 −27.9 0.9

−26.7 0.9 −26.8 0.5 −28.4

δ13C

a Means are given for the same biological species at the same sampling site, except for seals (results are separated between young and adult seals because of significant differences in [THg]). bResults of Perca f luviatilis and Rutilus rutilus were previously published.25

sculpins Comephorus baicalensis (n = 7) Lystvyanka Comephorus dybowski (n = 6) Lystvyanka Comephorus dybowski (embryon) (n = l) Lystvyanka Cottocomephorus grewingki (n = 5) Lystvyanka Cottocomephorus inermis (n = 2) Selenga River Cottocomephorus inermis (n = 4) Lystvyanka others Coregonus autumnalis migratorius (n = 6) Lystvyanka Thymallus arcticus (n = 2) Lystvyanka seals Phoca Sibirica (young) (n = 4) Phoca Sibirica (old) (n = 3) coastal food webb Perca fluviatilis (n = 12) Maloye More Rutilus rutilus (n = 12) Maloye More

sample/location

Table 1. Means of THg, MeHg, and IHg (ng·g−1, dw), C, N, and Hg isotopic ratios (As Delta Values, ‰) Measured in Muscle of Fish and Seal Samplesa

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[THg] in Baikalian adult seal muscle. Because adult seals are known to feed almost exclusively on sculpins, we have estimated a biomagnification factor (BMF = mean [THg]adults seals/mean [THg]sculpins) of 4.8, which is close to the BMF of 4.4 of Baikalian seals calculated by Ciesielski et al.32 Zoo- and phytoplankton exhibit a high percentage of IHg (from 83 to 97%), whereas other organisms contain a high MeHg fraction. Pelagic fish and sculpins contain 61−92% of MeHg (except for embryon of Comephorus dybowski which has very low [THg] and only 37% of MeHg); coastal fish display a high percentage of MeHg (from 90 to 98%); amphipods have %MeHg from 88 to 95%; and seal muscle contains 80−87% of MeHg. A power law relationship is observed between the total content of Hg and percentage of IHg (Figure S-5), showing that %IHg is decreasing (or %MeHg is increasing (Figure S-6) with [THg]. Also there are positive correlations among δ13C, δ15N, and [THg] (Figures S-7 and S-8). Therefore, we confirm that MeHg is predominantly bioaccumulated within the food webs, and that Hg content in biota depends on their feeding habits and location. Adult seals do not show correlation among δ13C, %IHg, and [THg]. This specificity may be due to the fact that adult seals have complex metabolism and developed mechanisms for detoxification/elimination of heavy metals (such as selenium and metallothionein binding capacity), which lead to different Hg species distribution and content among their organs (i.e., muscle, hair, kidney, brain, liver).33−35,42,43 Similarly to other publications,33,34 adult seals of LB exhibited lower total Hg content than in other reported freshwater or marine ecosystems, due to the pristine characteristics of LB. 2. Hg Stable Isotopic ratios within the Food Web. 2.1. Mass Dependent Fractionation. Means of the Hg isotopic composition in fish and seal samples are given in Table 1. All the results are summarized in Tables S-4 and S-5. Overall Hg stable isotopic ratios displayed a wide range of values among samples (δ202Hg from −1.45 to 2.24 ‰, n = 74), which represents a δ202Hg variation higher than 3.5‰ within the aquatic ecosystem of LB. Pelagic food web (pelagic sculpins and fish, amphipods, and seals) exhibits positive δ202Hg (−0.02 to 2.24‰, n = 46), whereas plankton and coastal fish exhibit negative δ202Hg (−1.45 to −0.33‰, n = 28). The only embryonic Comephoridae that have been analyzed for Hg isotopic ratios display a unique isotopic composition (δ202Hg = −0.02‰). Excluding this atypical result, pelagic sculpins show relatively homogeneous isotopic signatures with δ202Hg of 0.85 ± 0.22‰ (n = 26). C. aut. migratorius and T. arcticus had similar isotopic ratios (δ202Hg = 0.80 ± 0.24‰, n = 8), as well as amphipods Ommatogammarus (δ202Hg = 0.75 ± 0.11‰ (n = 2)) whereas amphipods A. godlewskii displayed slightly lower δ202Hg of 0.44 ± 0.11‰ (n = 2). On the other hand, seals (Phoca sibirica) show the highest δ202Hg values (1.83 ± 0.29‰, n = 7), whereas plankton samples exhibited the lowest δ202Hg values (−1.09 ± 0.31‰, n = 4). To compare with pelagic fish, previously published data of Baikalian coastal fish showed enrichment by lighter isotopes, such as δ202Hg of −0.61 ± 0.07‰ (n = 12) and −0.48 ± 0.07‰ (n = 12) which were observed for roach and perch, respectively.25 2.2. Mass Independent Fractionation. All biota samples showed mass independent fractionation of 199Hg and 201Hg odd isotopes (Figure 3 and Figure S-9). However, we observed significant differences among samples. An average Δ199Hg of 5.64 ± 0.72‰ (n = 6) was measured for C. aut. migratorius, including a maximum value of 6.65‰ for one individual. Sculpins showed slightly lower but still high values of Δ199Hg

Figure 3. Δ199Hg versus Δ201Hg in biological samples of Lake Baikal, with dashed line showing strong correlation for all samples. Value of the slope suggests mass-independent fractionation of Hg in such samples coming from accumulation of photodemethylated MeHg.

(4.59 ± 0.55‰, n = 27), similar to seal muscle (Δ199Hg = 4.62 ± 0.60‰, n = 7). Fish T. arcticus displayed significantly lower MIF for Δ199Hg equal to 2.91 ± 0.01‰ (n = 2), which was similar to the Δ199Hg of amphipods A. godlewskii (2.95 ± 0.02‰, n = 2). Close to the trend of δ202Hg for amphipods, Δ199Hg for Ommatogammarus was higher (3.50 ± 0.11‰, n = 2) than for A. godlewskii. In comparison with the pelagic biota (and T. arcticus) from the open water, coastal fish roach and perch from Maloye More (similar to δ202Hg signatures), had lower values of MIF (Δ199Hg = 1.14 ± 0.23‰ (n = 12) and 0.58 ± 0.15‰ (n = 12) for perch and roach, respectively).25 We also observed significant differences of MIF between phytoand zooplankton, exhibiting Δ199Hg equal to 0.32 ± 0.22‰ (n = 2) and 1.34 ± 0.27‰ (n = 2), respectively. 3. Isotopic Ratios (Hg, N, C) Tracing Hg in Lake Baikal Food Webs. 3.1. Coastal and Pelagic Food Webs of Lake Baikal. Results in terms of concentration (THg), speciation (MeHg and IHg), carbon and nitrogen stable isotopes, and Hg isotopic ratios (MDF and MIF) showed strong differences among the organisms of LB (Tables S-4 and S-5). According to the literature27,28 and the δ15N and δ13C results we identified at least two trophic food webs (Figure 2 and Figure S-10) in agreement with Yoshii et al.28 which described the pelagic food web of LB as less complex and isotopically distinct than the coastal food web. Therefore pelagic sculpins and seals were identified to belong to the same pelagic food web, whereas Perca f luviatilis and Rutilus rutilus belong to the more complex coastal food web. Other fish (C. aut. migratorius and T. arcticus) displayed intermediate δ13C values, also in confirmation of a previous work.28 The latter paper argued that such fish have a weak relationship with pelagic sculpins because they only feed on sculpin larvae and are not a component of the seals’ diet. δ15N and δ13C of amphipods are not available, but according to the literature, amphipods Acanthogammarus and Ommatogammarus seem to be part of the benthic food chain and are not the main diet of the pelagic sculpins.28,30,32,44 However, pelagic sculpins are planktonic foragers and migrate vertically30 allowing the interaction between these species. Also phytoplankton (BK-7 and BK-1) and one sample of zooplankton (BK-9) were assumed to be pelagic due to their sampling site (no data available). Zooplankton Pl-Ba (collected at Maloye 5906



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can represent 3−15% of the total Hg. Hence, according to the Δ199Hg/Δ201Hg ratios of 1.27 in the LB organisms (R2 = 0.996, n = 81, Figure 3), we can reasonably assume that high MIF measured in fish and seals is related to the accumulation of the residual MeHg after significant photodemethylation yield. The relatively lower MIF observed in plankton for all sampling sites (Δ199Hg from 0.17 to 1.53‰, n = 4) in comparison with pelagic fish can be mainly explained by the very low proportion of MeHg compared to IHg in these samples (see above). This leads to a much lower global MIF level since the fractionation factor during IHg photoreduction is suggested to be lower than during MeHg photodemethylation.7 A slightly lower MIF was measured in amphipods than in pelagic fish (Δ199Hg from 2.93 to 3.58‰, n = 4). It is thus suggested that less photodemethylated MeHg is incorporated in amphipods than in pelagic fish because the former live in deeper waters (below 200 m)44 where light penetration is limited, and that they eat dead sculpins, which have high MIF, but also have other food sources. The calculated mass-balance (see details in SI) between isotope anomalies (i.e., Δ199Hg and Δ201Hg) and the fractions of Hg species (i.e., %IHg and % MeHg) in the different biological organisms revealed that differences of MIF among these samples cannot be simply attributed to their respective MeHg and IHg fraction. We can conclude that high variation of MIF between the different food webs (pelagic and coastal) of LB is dependent on the feeding location and thus water column characteristics. Additionally, there is no relationship between Δ199Hg and %MeHg or [THg] (Figure S-13), and seals have Δ199Hg value similar to the 4 pelagic sculpins which represent mainly seals’ diet (4.62 ± 0.60‰ (n = 7) and 4.59 ± 0.55‰ (n = 27), respectively). Therefore, MIF is unlikely to be produced in vivo. In a previous study,25 we measured higher MIF levels in carnivorous fish (perch) than in herbivorous fish (roach). Nevertheless, a trophic relationship has not been clearly established between these species,44 and we measured a higher MIF level in coastal plankton, which is at the bottom of the food chain, than in perch. This also suggests that MIF level in biological samples is directly constrained by the Hg isotopic composition before its assimilation, rather than in vivo mass-independent isotope fractionation. 3.3.2. Hg Sources and Cycling Provide Different MIF Levels in the Different Food Webs. In the open water of LB (i.e., the pelagic zone), horizontal transport of organic matter from coastal areas is limited.46 Additionally, transport of organic matter from the sediment is negligible due to the great depth of the water column (>1000 m).46,47 Therefore MeHg in the pelagic food web is likely to derive mainly from the IHg methylation in the water column and to a lesser extent from MeHg atmospheric deposition and coastal advective inputs. MeHg is also unlikely to come from the sediment−water interface. Near the bottom (≈700−1000 m) and intermediate depth (≈500−700 m) waters have a long renewal time of 8 and 15 years, respectively, while the residence time of LB water (and major ions) is as high as 330 years.47,48 Because the surface layer, above 400 m, is well mixed between May and October, Hg residence time and recycling in pelagic waters is supposed to be very long if compared to other freshwater ecosystems.48 The longer residence time of Hg may allow specific MeHg recycling through biotic methylation, providing only MDF, and light-induced demethylation, involving both MDF and MIF. MeHg turnover pathways in the water column are therefore suggested to largely affect its isotopic composition

More, sampling site 3, mix of 85% zoo- and 15% phytoplankton) with available δ15N and δ13C data showed a predominant coastal signature.25 3.2. MDF during Hg Trophic Transfer. We observed significant trends of δ202Hg increasing with δ15N (Figure 2) within each food web (pelagic and coastal). A student t test showed significant differences (P < 0.0003 in any case) of δ202Hg and δ15N between each group of populations (roaches/ perches, sculpins/seals). This observation suggests that within the same food web, the bioaccumulation of mercury leads to an enrichment by heavier isotopes, corroborating results of previous studies.7,20,25 The prey−predator system (sculpins− seals) of the pelagic food web showed an enrichment in heavier isotopes during trophic transfer close to +1‰ (δ202Hg = 0.85 ± 0.22‰ and 1.83 ± 0.29‰, respectively), whereas this trend is less pronounced in the coastal food web where trophic relationships between roaches and perches are less characterized. The absolute value of δ202Hg would not represent the quantity of Hg accumulated in biological species; coastal fish, which contain higher [MeHg] than pelagic sculpins, display lower δ202Hg. In the pelagic food web, seals also have a higher δ202Hg than the pelagic sculpins they feed on, but no dependence of δ202Hg with Hg concentration can be observed, since young seals (n = 4) with lower [THg] than adults (n = 3) (175 ± 31 and 920 ± 164 ng·g−1, respectively) had similar δ202Hg values (1.88 ± 0.20‰ and 1.76 ± 0.42‰, respectively). Among pelagic fish and seals we observed only a weak dependence of δ202Hg on [THg] (Figure S-11) as well as between %IHg and δ202Hg (Figure S-12) suggesting that even if IHg and MeHg exhibit different δ202Hg, such difference cannot explain the variations of δ202Hg among samples . Phyto- and zooplankton, which are at the beginning of the food web and have lower TL than pelagic sculpins,28 exhibited a low percentage of MeHg and a highly negative δ202Hg (from −1.45 to −0.78 ‰). We also observed that embryonic Comephorus dybowski had a significantly lower δ202Hg (and lower %MeHg) than adult ones (the only negative value of the pelagic food web), which can be explained by different Hg sources for embryos in comparison to adults. As trophic transfer of Hg is carried out through MeHg rather than IHg species uptake, we can conclude that Hg MDF variations in the pelagic food web of LB are probably due to trophic transfer rather than in vivo processes due to bioaccumulation. Thus, trophic transfer process is likely to enrich Hg in heavier isotopes, with a δ202Hg absolute value depending both on the studied ecosystems and biological species TL. 3.3. MIF Origin between Coastal and Pelagic Area of Lake Baikal. 3.3.1. Extent of MIF in Relation to Aquatic Photodemethylation of Bioaccumulated MeHg in the Food Webs. Pelagic fish (Comephoridae and Cottidae families and C. aut. migratorius) and seals exhibited high MIF (Δ199Hg up to 6.65‰), which is higher than MIF observed in biological species from other freshwater7,20,23,26 or marine24,45 ecosystems. Previous publications8,11,12 showed that biotic processes such as biotic methylation/demethylation and reduction in the water column and surface sediment are unlikely to produce MIF. MIF is mainly recognized to be produced in the water column by the photoreduction of IHg and/or MeHg. These pathways lead to the enrichment of odd isotopes in the residual Hg reactant compound,7,9,14,15 with a ratio Δ199Hg/Δ201Hg close to 1.3 for photodemethylation of MeHg and close to 1.0 for photoreduction of IHg.7 MeHg has been determined in the water column of the southern and central basins of LB31 and 5907



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Figure 4. Δ199Hg versus δ202Hg as indicator of source and bioaccumulation of Hg within the pelagic and coastal food webs of Lake Baikal. The red arrow illustrates the MDF (a 1‰ increase of δ202Hg between sculpins and seals) during trophic transfer.

and MIF positive anomaly.7 The remaining MeHg exhibiting a high MIF is further accumulated in the food web. This hypothesis is supported by a higher [MeHg] in deep waters (0.022 ng·L−1) compared to surface waters (0.009 ng·L−1) of LB.31 This is consistent with a water column Hg methylation and higher MeHg demethylation within the euphotic zone, as already demonstrated for the marine water column.49 On the contrary, the water column of the Maloye More sampling site displays much a shallower depth (2−20 m), allowing the bioaccumulation of MeHg more efficiently produced and released from IHg methylation at the sediment−water interface. Moreover, the water column of this coastal area exhibits a longer duration of the ice-pack cover, as well as higher snow thickness than the southern pelagic area31,50 which limits light penetration and thus the yields of photodemethylation.45 The shallow depth may also promote rapid scavenging and sedimentation of MeHg thus allowing less MeHg photodemethylation. [MeHg] in Maloye More water was found to be significantly higher (0.026−0.038 ng·L−1) than in the open water column (0.009−0.022 ng·L−1).31 This result agrees with our results showing that coastal fish (roach and perch) sampled at this site displayed significantly higher MeHg content but lower MIF than the pelagic fish (Table 1 and previous study25). Differences in water circulation between the pelagic and the coastal areas definitely have a major influence on Hg residence time, leading to a different level of Hg species transformations, such as photodemethylation, within the respective water columns. Therefore, Hg MIF level is expected to be promoted in the pelagic water column. 3.3.3. Higher Rate and Extent of Demethylation in the Pelagic Water Column Causes Higher MIF. As previously suggested,7 photoinduced demethylation of MeHg is the most likely process responsible for MIF signatures observed in aquatic biological samples. However, it is still unclear why significantly different levels of MIF are observed in the Hg of fish among different freshwater lakes and between freshwater and marine waters.7,23,24,26 Rates of MeHg photodegradation have been demonstrated to be dependent on the type of MeHg-binding ligands.51 These rates are suggested to be

generally higher in freshwater than in seawater due to the respective prevalence of Hg−thiolate complexes associated with dissolved organic matter and Hg−chloride complexes. Concentrations of dissolved organic carbon (DOC) in LB ranged from 90 to 110 μM of DOC (about 1 mg/L of DOC), which is usually higher than those in oligotrophic oceanic environments,52 while the total salinity of the lake is only 0.1‰.53 Thus, the relatively lower MIF observed in biota of marine systems24 compared to the MIF observed in the pelagic area of LB and several other freshwater lake systems7,26 is likely to be the consequence of the accumulation of MeHg that undergoes less photodegradation because of higher salinity and maybe lower DOC. In a marine system, pelagic fishes had also higher MIF signatures compared to coastal fish, due to a disconnected food web and higher MeHg photodegradation in the pelagic area.24 Analogy with the latter study can be made between coastal and pelagic fish of LB. Assuming about 1 mg/L of DOC in LB and extrapolating the exponential slope between the fraction of demethylated MeHg and the Δ201Hg measured in fish7 (see Supporting Information), we estimated between 76 and 84% of MeHg demethylated before incorporation into pelagic fish (Δ201Hg between 3.5 and 4.5‰). In coastal fish from Maloye More (Δ201Hg between 0.5 and 1‰) the fraction of demethylated MeHg before incorporation into the fish was only around 19−34%, which is significantly lower than in the pelagic water column. In addition to the difference of water column depth and the duration of annual ice pack cover (see above), other characteristics of each ecosystems may explain the differences in photodemethylationand thus Hg MIF differences between the fishfrom the pelagic and the coastal area of LB. First, the pelagic area is characterized by a pristine and deep oligotrophic water column. In opposition, a study reported that the Maloye More site belongs to higher fishery and tourism activities resulting in significant toxic pollution.54 High phosphate and nitrate dissolution have been found in the bay of Maloye More, which coincided with the local occurrence of the diatom species Stephanodiscus meyerii, a genus which is typical for meso- to eutrophic lakes.50 Thus, lower transparency and higher DOM content in the water column of Maloye More should limit the photodemethylation process while higher 5908



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eutrophication may promote methylation.49,55 This hypothesis is also confirmed by the higher MeHg content observed in fish and in the water column of Maloye More compared to the pelagic zone. Physico-chemical characteristics of the pelagic water column of LB are thus likely to be responsible for the rapid demethylation of MeHg associated with higher MIF in the fish species compared to coastal zone. 3.4. Combining Hg Isotopic Signature (MDF and MIF) to Track MeHg Sources and Bioaccumulation Pathways in Lake Baikal. Plotting the results of MDF versus MIF signatures measured in our samples (Figure 4) shows strong differentiation between pelagic and coastal food webs of LB. Previous work24 demonstrates Hg isotopic contrast between coastal and oceanic marine fish, and suggests that the two food webs of LB have different MeHg processes and inputs leading to highly different Hg isotopic compositions. Significantly higher MIF in the pelagic food web than the coastal food web is the result of strong photodemethylation of MeHg in the open water column. Photodemethylation also produces MDF which enriches residual MeHg in heavier isotopes.7 Thus, the extent of MeHg photodemethylation can explain both the higher Δ199Hg and the higher δ202Hg measured in the pelagic food web when compared to the coastal food web. Figure S-14 shows that the MIF and MDF observed in the carnivorous pelagic fish of LB are comparable with isotopic signatures observed in carnivorous fish (burbot fish) from another deep, large and midlatitude lake, Lake Michigan, where high photodemethylation levels and dominant atmospheric Hg supply was suggested.7 Other piscivorous fishes (Arctic char) from a deep crater lake with a similar water residence time (330 yrs) as LB also supports the same conclusions from the authors.26 In the same study, lower MIF and MDF were detected in northern Arctic lakes where ice cover duration should limit the extent of photodemethylation.26 Photodemethylation plays an important role in the isotopic composition of Hg in fish of the coastal area but its yield is rather limited, while the shallow water column allows direct accumulation of Hg from sediment into coastal fish. Biotic methylation has been suggested to produce MeHg enriched in lighter isotopes compared to the residual IHg,8 and surface sediment in the coastal area displays a negative value of δ202Hg (close to −2‰).25 Hence, coastal fish could accumulate an initial Hg from sediment which has very negative δ202Hg, however the relatively less negative δ202Hg observed in fish is probably due to the trophic transfer. On the contrary, the pelagic fishes of the LB are likely accumulating Hg originating from the atmosphere (global slightly negative MIF signature, Δ199Hg = −0.25 ± 0.28‰ as recorded in moss, peat, and lichens,19 and slightly negative or positive MIF signature measured in coal deposits56) rather than directly from deep or coastal sediment. Precipitation and ambient air in North America Great Lakes also showed slighly negative or positive MIF.57 Anthropogenic influence is unlikely in LB since fish from a highly Hg contaminated water reservoir located downstream LB displayed very low MIF and very high Hg concentrations.25 Due to the complex equilibrium between MeHg and IHg species in relation to several transformation pathways in natural aquatic ecosystems, measuring species-specific isotopic fractionation should increase the knowledge of isotopic fractionation in identifying the processes involved in the Hg biogeochemical cycle.

Article

ASSOCIATED CONTENT

S Supporting Information *

Additional data tables, figures, method descriptions, and discussions. This material 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] (V.P.); david.amouroux@ univ-pau.fr (D.A.) phone: +33 (0) 559 407 756; fax: +33 (0) 559 407 781. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS V.P. acknowledges “Ministère de l’Enseignement Supérieur et de la Recherche” for his Doctoral Fellowship (Ecole Doctorale ED211). We thank Sylvain Berail (CNRS, LCABIE-IPREM) for the technical assistance during the MC-ICPMS analysis. We acknowledge the Institut National des Sciences de l’Univers (CNRS) for the financial support of the MerLaBa project in 2008, 2010, and 2011 within the Cytrix EC2CO programme. Also, we are grateful to J.D. Blum for providing UM-Almadén secondary standard for Hg isotopic ratios measurements.

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REFERENCES

(1) Compeau, G. C.; Bartha, R. Sulfate-Reducing Bacteria: Principal methylators of mercury in anoxic estuarine sediments. Appl. Environ. Microbiol. 1985, 50, 498−502. (2) Fitzgerald, W. F.; Lamborg, C. H. Geochemistry of mercury in the environment. In Treatise on Geochemistry; Elsevier/ University of Connecticut: CT, USA, 2003; Vol. 9. (3) Mason, R. P.; Reinfelder, J. R.; Morel, F. M. M. Uptake, toxicity, and trophic transfert of mercury in a coastal diatom. Environ. Sci. Technol. 1996, 30, 1835−1845. (4) Watras, C. J.; Back, R. C.; Halvorsen, S.; Hudson, R. J. M.; Morrison, K. A.; Wente, S. P. Bioaccumulation of mercury in pelagic freshwater food webs. Sci. Total Environ. 1998, 219, 183−208. (5) Morel, F. M. M.; Kraepiel, A. M. L.; Amyot, M. The chemical cycle and bioaccumulation of mercury. Ann. Rev. Ecol. Syst. 1998, 29, 543−566. (6) Bullen, T. D.; Walczyk, T. Environmental and Biomedical Applications of Natural Metal Stable Isotope Variations. Elements 2009, 5, 381−385. (7) Bergquist, B. A.; Blum, J. D. Mass-dependent and -independent fractionation of Hg isotopes by photoreduction in aquatic systems. Science 2007, 318, 417−420. (8) Rodriguez-Gonzales, P.; Epov, V. N.; Bridou, R.; Tessier, E.; Guyoneaud, R.; Monperrus, M.; Amouroux, D. Species-Specific Stable Isotope Fractionation of Mercury during Hg(II) Methylation by an Anaerobic Bacteria. Environ. Sci. Technol. 2009, 43, 9183−9188. (9) Zheng, W.; Hintelmann, H. Mercury Isotope Fractionation during photoreduction in natural water is controlled by its Hg/DOC ratio. Geochim. Cosmochim. Acta 2009, 73, 6704−6715. (10) Estrade, N.; Carignan, J.; Sonke, J. E.; Donard, O. F. X. Mercury isotope fractionation during liquid-vapor evaporation experiments. Geochim. Cosmochim. Acta 2009, 73, 2693−2711. (11) Kritee, K.; Barkay, T.; Blum, J. D. Mass dependant stable isotope fractionation of mercury during mer mediated microbial degradation of monomethylmercury. Geochim. Cosmochim. Acta 2009, 73, 1285−1296. (12) Kritee, K.; Blum, J. D.; Barkay, T. Mercury stable isotope fractionation during reduction of Hg(II) by different microbial pathways. Environ. Sci. Technol. 2008, 42, 9171−9177. 5909



Article

accumulation in Baikal seals (Pusa sibirica), Caspian seals (Pusa caspica) and northern fur seals (Callorhinus ursinus). Environ. Pollut. 2004, 127, 83−97. (34) Ciesielski, T.; Pastukhov, M. V.; Fodor, P.; Bertenyi, Z.; Namiesnik, J.; Szefer, P. Relationships and bioaccumulation of chemical elements in the Baikal seals. Environ. Pollut. 2006, 139, 372−384. (35) Watanabe, I.; Tanabe, S.; Amano, M.; Miyasaki, N.; Petrov, E. A.; Tatsukawa, R. Age-Dependent Accumulation of Heavy metals in Baikal Seal (Phoca sibirica) from the Lake Baikal. Arch. Environ. Contam. Toxicol. 1998, 35, 518−526. (36) Rodriguez Martin-Doimeadios, R. C.; Tessier, E.; Amouroux, D.; Guyoneaud, R.; Duran, R.; Caumette, P.; Donard, O. F. X. Mercury methylation/demethylation and volatilization pathways in estuarine sediment slurries using species-specific enriched stable isotopes. Mar. Chem. 2004, 90, 107−123. (37) Monperrus, M.; Rodriguez-Gonzalez, P.; Amouroux, D.; Garcia Alonso, J. I.; Donard, O. F. X. Evaluating the potential and limitations of double-spiking species-specific isotope dilution analysis for the accurate quantification of mercury species in different environmental matrices. Anal. Bioanal. Chem. 2008, 390, 655−666. (38) Estrade, N.; Carignan, J.; Sonke, J. E.; Donard, O. F. X. Measuring Hg Isotopes in Bio-Geo-Environmental Reference Materials. Geostand. Geoanal. Res. 2009, 34, 79−93. (39) Epov, V. N.; Rodriguez-Gonzalez, P.; Sonke, J. E.; Tessier, E.; Amouroux, D.; Maurice-Bourgoin, L.; Donard, O. F. X. Simultaneous Determination of Species-Specific Isotopic Composition of Hg by Gas Chromatography Coupled to Multicollector ICPM. Anal. Chem. 2008, 80, 3530−3538. (40) Epov, V. N.; Berail, S.; Jimenez-Moreno, M.; Perrot, V.; Pecheyran, C.; Amouroux, D.; Donard, O. F. X. Approach to measure Isotopic Ratios in Species Using Multicollector-ICPMS Coupled with Chromatography. Anal. Chem. 2010, 82, 5652−5662. (41) George, B. M.; Batzer, D. Spatial and temporal variations of mercury levels in Okefenokee invertebrates: Southeast Georgia. Environ. Pollut. 2008, 152, 484−490. (42) Wagemann, R.; Trebacz, E.; Boila, G.; Lockhart, W. L. Mercury species in the liver of ringed seals. Sci. Total Environ. 2000, 261, 21− 32. (43) Sonne, C.; Aspholm, O.; Dietz, R.; Andersen, S.; Berntssen, M. H. G.; Hylland, K. A study of metal concentrations and metallothionein binding capacity in liver, kidney and brain tissues of three Arctic seal species. Sci. Total Environ. 2009, 407, 6166−6172. (44) Yoshii, K. Stable isotope analyses of benthic organisms in Lake Baikal. Hydrobiologia 1999, 411, 145−159. (45) Point, D.; Sonke, J. E.; Day, R. D.; Roseneau, D. G.; Hobson, K. A.; Vander Pol, S. S.; Moors, A. J.; Pugh, R. S.; Donard, O. F. X.; Becker, P. R. Methylmercury photodegradation influenced by sea-ice cover in Arctic marine ecosystems. Nat. Geosci. 2011, 4, 188−194. (46) Shimaraev, M. N.; Granin, N. G.; Zhdanov, A. A. Deep Ventilation of Lake Baikal Waters Due to Spring Thermal Bars. Limnol. Oceanogr. 1993, 38, 1068−1072. (47) Weiss, R. F.; Carmack, E. C.; Koropalov, V. M. Deep-water renewal and biological production in Lake Baikal. Nature 1991, 349, 665−669. (48) Afanasyev, A. N. The water budget of Lake Baikal. Trans. Baikal Limnol. Station Akademic Nauc SSSR Vostok-Siberia 1960, 18, 155− 241. (49) Monperrus, M.; Tessier, E.; Amouroux, D.; Leynaert, A.; Huonnic, P.; Donard, O. F. X. Mercury methylation, demethylation and reduction rates in coastal and marine surface waters of the Mediterranean Sea. Mar. Chem. 2007, 107, 49−63. (50) Mackay, A. W.; Battarbee, R. W.; Flower, R. J.; Granin, N. G.; Jewson, D. H.; Ryves, D. B. Assessing the potential for developing internal diatom-based transfer functions for Lake Baikal. Limnol. Oceanogr. 2003, 48, 1183−1192. (51) Zhang, T.; Hsu-Kim, H. Photolytic degradation of methylmercury enhanced by binding to natural organic ligands. Nat. Geosci. 2010, 3, 473−476.

(13) Zheng, W.; Foucher, D.; Hintelmann, H. Mercury isotope fractionation during volatilization of Hg(0) from solution into the gas phase. J. Anal. At. Spectrom. 2007, 22, 1097−1104. (14) Zheng, W.; Hintelmann, H. Isotope Fractionation of Mercury during Its Photochemical Reduction by Low-Molecular-Weight Organic Compounds. J. Phys. Chem. A 2010, 114, 4246−4253. (15) Malinovsky, D.; Latruwe, K.; Moens, L.; Vanhaecke, F. Experimental study of mass-independence of Hg isotope fractionation during photodecomposition of dissolved methylmercury. J. Anal. At. Spectrom. 2010, 25, 950−956. (16) Malinovsky, D.; Vanhaecke, F. Mercury isotope fractionation during abiotic transmethylation reactions. Int. J. Mass Spectrom. 2011, No. 10.1016/j.ijms.2011.1001.1020. (17) Bergquist, B. A.; Blum, J. D. The Odds and Evens of Mercury isotopes: Applications of Mass-Dependent and Mass-Independent Isotope Fractionation. Elements 2009, 5, 353−357. (18) Yin, R.; Feng, X.; Shi, W. Application of the stable-isotope system to the study of sources and fate of Hg in the environment: A review. Appl. Geochem. 2010, 25, 1467−1477. (19) Sonke, J. E. A global model of mass independent mercury stable isotope fractionation. Geochim. Cosmochim. Acta 2011, 75, 4577−4590. (20) Jackson, T. A.; Whittle, D. M.; Evans, M. S.; Muir, D. C. G. Evidence for mass-independent and mass-dependent fractionation of the stable isotopes of mercury by natural processes in aquatic ecosystems. Appl. Geochem. 2008, 23, 547−571. (21) Foucher, D.; Ogrinc, N.; Hintelmann, H. Tracing Mercury Contamination from the Idrija Mining Region (Slovenia) to the Gulf of Trieste Using Hg Isotope Ratios Measurements. Environ. Sci. Technol. 2009, 43, 33−39. (22) Laffont, L.; Sonke, J. E.; Maurice, L.; Hintelmann, H.; Pouilly, M.; Bacarreza, Y. S.; Perez, T.; Behra, P. Anomalous Mercury Isotopic Compositions of Fish and Human Hair in the Bolivian Amazon. Environ. Sci. Technol. 2009, 43, 8985−8990. (23) Das, R.; Salters, V. J. M.; Odom, A. L. A case for in vivo massindependant fractionation of mercury isotopes in fish. Geochem. Geophys. Geosyst. 2009, 10. (24) Senn, D. B.; Chesney, E. J.; Blum, J. D.; Bank, M. S.; Maage, A.; Shine, J. P. Stable Isotope (N, C, Hg) Study of Methylmercury Sources and Trophic Transfer in the Northern Gulf of Mexico. Environ. Sci. Technol. 2010, 44, 1630−1637. (25) Perrot, V.; Epov, V. N.; Pastukhov, M. V.; Grebenshchikova, V. I.; Zouiten, C.; Sonke, J. E.; Husted, S.; Donard, O. F. X.; Amouroux, D. Tracing Sources and Bioaccumulation of Mercury in Fish of Lake Baikal-Angara River Using Hg Isotopic Composition. Environ. Sci. Technol. 2010, 44, 8030−8037. (26) Gantner, N.; Hintelmann, H.; Zheng, W.; Muir, D. C. G. Variations in Stable Isotope Fractionation of Hg in Food Webs of Artic Lakes. Environ. Sci. Technol. 2009, 43, 9148−9154. (27) Post, D. M. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 2002, 83, 703−718. (28) Yoshii, K.; Melnik, N. G.; Timoshkin, O. A.; Bondarenko, N. A.; Anoshko, P. N.; Yoshioka, T.; Wada, E. Stable isotope analyses of the pelagic food web in Lake Baikal. Limnol. Oceanogr. 1999, 44, 502−511. (29) Gustin, M. S.; Saito, L.; Peacock, M. Anthropogenic impacts on mercury concentrations and nitrogen and carbon isotope ratios in fish muscle tissue of the Truckee River watershed. Sci. Total Environ. 2005, 347, 282−294. (30) Miyasaka, H.; Dzyuba, Y. V.; Genkai-Kato, M.; Ito, S.; Kohzu, A.; Anoshko, P. N.; Khanayev, I. V.; Shubenkov, S. G.; Melnik, N. G.; Timoshkin, O. A.; Wada, E. Feeding ecology of two planktonic sculpins, Comephorus baicalensis and Comephorus dybowskii (Comephoridae), in Lake Baikal. Ichthyol. Res. 2006, 53, 419−422. (31) Meuleman, C.; Leermakers, M.; Baeyens, W. Mercury speciation in Lake Baikal. Water, Air Soil Pollut. 1995, 80, 539−551. (32) Ciesielski, T.; Pastukhov, M. V.; Szefer, P.; Jenssen, B. M. Bioaccumulation of mercury in the pelagic food chain of the Lake Baikal. Chemosphere 2010, 78, 1378−1384. (33) Ikemoto, T.; Kunito, T.; Watanabe, I.; Yasunaga, G.; Baba, N.; Miyasaki, N.; Petrov, E. A.; Tanabe, S. Comparison of trace element 5910



Article

(52) Yoshioka, T.; Ueda, S.; Khodzher, T.; Bashenkhaeva, N.; Korovyakova, I.; Sorokovikova, L.; Gorbunova, L. Distribution of dissolved organic carbon in Lake Baikal and its watershed. Limnology 2002, 3, 0159−0168. (53) Millero, F. J. The Equation of State of Lakes. Aquat. Geochem. 2000, 6, 1−17. (54) Kozhova, O. M.; Silow, E. A. The current problems of Lake Baikal ecosystem conservation. Lakes Reservoirs: Res. Manage. 1998, 3, 19−33. (55) Monperrus, M.; Tessier, E.; Point, D.; Vidimova, K.; Amouroux, D.; Guyoneaud, R.; Leynaert, A.; Grall, J.; Chauvaud, L.; Thouzeau, G.; Donard, O. F. X. The biogeochemistry of mercury at the sedimentwater interface in the Thau Lagoon. Estuarine, Coastal Shelf Sci. 2007, 72, 485−496. (56) Biswas, A.; Blum, J. D.; Bergquist, B. A.; Keeler, G.; Xie, Z. Natural Mercury Isotope Variation in Coal Deposits and Organic Soils. Environ. Sci. Technol. 2008, 42, 8303−8309. (57) Gratz, L. E.; Keeler, G. J.; Blum, J. D.; Sherman, L. S. Isotopic Composition and Fractionation of Mercury in Great Lakes Precipitation and Ambient Air. Environ. Sci. Technol. 2010, 44, 7764−7770.

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