Relationships between total mercury in sediments and methyl mercury

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Relationships between total mercury in sediments and methyl mercury in the freshwater gastropod prosobranch Bithynia tentaculata in the St. Lawrence River, Quebec J.C. Désy, J.-F. Archambault, B. Pinel-Alloul, J. Hubert, and P.G.C. Campbell

Abstract: Total Hg concentrations in sediment and methyl mercury (MeHg) levels in the gastropod species Bithynia tentaculata were evaluated at 21 stations in the fluvial corridor of the St. Lawrence River (Quebec, Canada). In the sediments (n = 21), total Hg concentrations ranged from 34 to 2790 ng·g dry weight–1. In the gastropods, MeHg concentrations varied from 15 to 290 ng·g dry weight–1 in undepurated gastropods (n = 20) and from 41 to 420 ng·g dry weight–1 in depurated gastropods (n = 13; without gut contents). The southern sector of Lake St. Louis, located near the Îles-de-la-Paix, had significantly higher Hg concentrations than any other sectors under study, both for total Hg in the sediments and MeHg in the gastropods. We established linear models to describe the relationships between Hg contamination in sediments and molluscs for the fluvial corridor of the St. Lawrence River and for the Lake St. Louis sector. Total Hg in sediments and MeHg in gastropods were highly correlated for all pooled stations (r = 0.83), and the relationship was even stronger for the Lake St. Louis stations (r = 0.92). Our study suggests that the gastropod B. tentaculata is a promising biomonitor species for assessing Hg contamination in the fluvial corridor and lakes of the St. Lawrence River. Résumé : Les concentrations de Hg total dans les sédiments et de méthylmercure (MeHg) dans le mollusque gastéropode Bithynia tentaculata ont été évaluées à 21 stations dans le corridor fluvial du fleuve Saint-Laurent (Québec, Canada). Dans les sédiments (n = 21), les concentrations de Hg total s’étendaient de 34 à 2 790 ng·g poids sec–1. Dans les gastéropodes, les concentrations variaient de 15 à 290 ng·g poids sec–1 pour les individus non-dépurés (n = 20) et de 41 à 420 ng·g poids sec–1 pour les individus dépurés (sans contenu digestif) (n = 13). Le secteur sud du lac SaintLouis, près des Îles-de-la-Paix, avait des concentrations en mercure significativement supérieures à celles des autres secteurs, à la fois pour le Hg total dans les sédiments et le méthylmercure dans les gastéropodes. Nous avons établi des modèles linéaires pour décrire les relations entre la contamination en mercure dans les sédiments et dans les mollusques pour l’ensemble du corridor fluvial, et pour le secteur du lac Saint-Louis. Les concentrations de Hg total dans les sédiments et de méthylmercure dans les gastéropodes étaient corrélées significativement pour l’ensemble des stations (r = 0,83), et encore plus fortement pour les stations du lac Saint-Louis (r = 0,92). Notre étude suggère que le gastéropode B. tentaculata pourrait être un bon organisme sentinelle pour évaluer la contamination par le mercure dans le couloir et les lacs fluviaux du Saint-Laurent. Désy et al.

Introduction In rivers and lakes, many pollutants are accumulated in bottom sediments, where they are potentially available to Received September 30, 1998. Accepted September 1, 1999. J14807 J.C. Désy and B. Pinel-Alloul.1 GRIL, Département des Sciences biologiques, Université de Montréal, C.P. 6128, succursale Centre-ville, Montréal, QC H3C 3J7, Canada. J.-F. Archambault and J. Hubert. Département de Chimie, Université de Montréal, C.P. 6128, succursale Centre-ville, Montréal, QC H3C 3J7, Canada. P.G.C. Campbell. Institut national de la Recherche scientifique, INRS-Eau, Université du Québec, C.P. 7500, Sainte-Foy, QC G1V 4C7, Canada. 1

Author to whom all correspondence should be addressed. e-mail: [email protected]

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benthic macroinvertebrates and their consumers (Luoma 1983). Among the pollutants associated with aquatic sediments, Hg is one of the most threatening for aquatic life, especially in its methylated forms. Indeed, methyl mercury (MeHg) is efficiently transferred and biomagnified along aquatic food webs (Boudou and Ribeyre 1981; Watras and Bloom 1992; Becker and Bigham 1995). Molluscs have been widely studied as biomonitors for metal contamination in aquatic ecosystems (Cossa 1995), even though clear relationships between contamination in sediment and molluscs are not always found (MetcalfeSmith et al. 1992). In the St. Lawrence River, several recent studies were conducted on the bioaccumulation, kinetics, and uptake of Hg by unionid bivalves (Metcalfe-Smith et al. 1996). In contrast, little work has been done on Hg bioaccumulation by gastropods, which are more abundant and widespread than large bivalves in the St. Lawrence River (Pinel-Alloul et al. 1996). Bithynia tentaculata (Proso© 2000 NRC Canada


Désy et al.

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Fig. 1. Study sites with locations of sampling stations.

branchia, Gastropoda) is a major component of the macroinvertebrate community in the St. Lawrence River (Magnin 1970) and an important part of the diet of fish (Mongeau et al. 1992) and ducks (Reinecke and Owen 1980). Although this species could be a potential vector of metal contamination for wildlife and humans, Hg contamination in this gastropod has never been evaluated. Recent studies on bioaccumulation of Cd, Zn, and Pb by B. tentaculata indicated that this gastropod has strong capacities to accumulate trace metals and that good relationships exist between metal bioaccumulation and bioavailable Cd and Zn in water, filamentous algae, or macrophytes (Flessas et al. 2000). This study is a first attempt to describe MeHg accumulation by B. tentaculata in the St. Lawrence River, relative to total Hg contamination in sediments. First, we evaluated whether MeHg concentrations in gastropods and total Hg concentrations in sediments varied among sectors of the fluvial corridor and lakes of the St. Lawrence River and followed similar spatial patterns. Second, we investigated the relationships between total Hg contamination in the sediments and MeHg concentrations in the soft tissues of the gastropods in order to evaluate the suitability of the gastropod B. tentaculata as a biomonitor of Hg contamination in the St. Lawrence River.

Materials and methods Survey sites and biomonitor species The study was carried out in three sectors of the fluvial corridor of the St. Lawrence River: Lake St. François, Lake St. Louis and the Contrecoeur Islands (Fig. 1A). These fluvial lakes are natural enlargements of the St. Lawrence River. They represent sinks for temporary or permanent deposition of small particles (Carignan et al. 1994). Lake St. François (Fig. 1B), the first natural enlargement of the St. Lawrence River downstream from Lake Ontario, receives its water mainly from the Great Lakes and small tributaries. Although no major industry is located on its shore or in the tributary basins, this lake is contaminated by both metals and organic contaminants (Sloterdijk 1991; Carignan et al. 1994). Toxic substances are thought to originate mainly from contaminated waters of the Great Lakes and from the international section of the St. Lawrence River (St. Lawrence Centre 1996). Local inputs come from industries located at the entrance of the lake, in the region of Cornwall– Massena. Lake St. Louis (Fig. 1C), the second natural enlargement of the St. Lawrence River, receives its water from Lake St. François and the Ottawa River. Its main tributaries contributing to pollutant discharges (organic and inorganic) are the St. Louis and Châteauguay rivers on the south shore and, on the north shore, the Ottawa River and the Denis and Bouchard streams. The St. Louis River is known to be an important source of contaminants, especially of Hg (Jarry et al. 1985). Industrial discharges and municipal © 2000 NRC Canada



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Can. J. Fish. Aquat. Sci. Vol. 57(Suppl. 1), 2000 Table 1. MeHg concentrations (ng·g dry weight–1) in undepurated and depurated B. tentaculata and total Hg concentrations (ng·g dry weight–1) in sediments at each station. B. tentaculata Undepurated Station

N

Lake St. François

LSF-1 LSF-2 LSF-3 LSF-4

3 3 3 3

47 (15) 62 (10) 35.2 (6) 62 (19)

1 1 1 2

Lake St. Louis

LSL-1 LSL-2 LSL-3 LSL-4 LSL-5 LSL-6 LSL-7 LSL-8 LSL-9 LSL-10 LSL-11 LSL-12 LSL-13

3 3

1 1

3 1 2 1 3 3 2 2 3 2

223 (18) 30.0 na 38.9 (5) 31.3 45.8 (5) 27.5 122 (9) 163 (95) 291 (15) 231 (9) 184 (5) 88.5 (2)

CTC-1 CTC-2 CTC-3 CTC-4

1 3 1 3

38.3 38.5 (5) 67.2 14.7 (4)

Contrecoeur region

Mean

Depurated N

1 2 2 1 2 2

1

Mean 71.3 57.0 57.0 40.5 (0.6) 196 47.4 na na na 42.1 na 113 (18) 134 (10) 416 220 (9.8) 182 (4.5) na na na na 63.3

Sediment N 1 1 1 1 1 1 1 1 1 1 1 2 2 2 2 2 2 1 1 1 1

Mean 61.0 73.0 305 85.0 934 184 184 34.0 122 220 78.0 456 (75) 1883 (516) 2787 (326) 2234 (1013) 1030 (104) 469 (61.5) 52.0 231 160 142

Note: N = number of samples per station. Standard deviation is indicated in parentheses (if available). na, not available.

waste effluents also contribute to toxic inputs in Lake St. Louis. The Contrecoeur Islands (Fig. 1D) are located 40 km downstream from the Island of Montreal. The Contrecoeur region has been identified as a potential contaminant deposition and accumulation zone. This region receives, in part, pollutants from Montreal urban effluents, where trace metal concentrations have been increasing since the 1960s. Four important industries also discharge toxic effluents into this reach of the St. Lawrence River (St. Lawrence Centre 1996). During summer 1992, we sampled 14 sites located in three sectors of the fluvial corridor of the St. Lawrence River: four stations in Lake St. François, six stations in Lake St. Louis, and four stations in the Contrecoeur Islands (Fig. 1). These sites were chosen according to their previously known concentrations of Hg in sediments (Jarry et al. 1985; Pinel-Alloul et al. 1991). In 1992, we found extremely high Hg concentrations in both sediments and gastropods in the southern part of Lake St. Louis, in the Îles-de-laPaix region (LSL-1; see Table 1 and Fig. 1C); these data produced a wide gap in our Hg contamination gradient. To improve the coverage of the Hg gradient in the southern part of Lake St. Louis, we sampled seven new stations (LSL-7 to LSL-13, Fig. 1C) in this region in August 1996. We chose the most abundant gastropod, B. tentaculata, as the biomonitor species. This prosobranch species, originating from Europe, was probably introduced into North America circa 1870. It is now widely distributed in calcareous rivers and lakes in northeastern North America. This gastropod is the most abundant species among benthic macroinvertebrates of the St. Lawrence River. It has been found in high density in Lake St. François (Pinel-Alloul et al. 1991), Lake St. Louis (Magnin 1970; Pinel-Alloul et Magnin 1971), Lake St. Pierre (Lamarche et al. 1982), and the freshwater tidal portion of the upper estuary (Vincent 1979). In Lake St. Louis, B. tentaculata has a vital cycle lasting 6 months to 1 year

(Pinel-Alloul and Magnin 1971). Its main feeding mode is by grazing, with its radula, the periphytic algae–detritus–bacteria complex on macrophytes and rock surfaces (Kornijów 1996). However, filterfeeding can be a supplemental mode of feeding depending on the abundance and nature of suspended particles (Tashiro and Colman 1982). Recent studies on the bioaccumulation of metals (Cd, Zn, Pb) by B. tentaculata have indicated that this gastropod has a good potential for biomonitoring trace metal contamination in the St. Lawrence River (Flessas et al. 2000).

Sampling procedures At each site, sediments were collected by scuba divers using polypropylene core samplers; care was taken not to disturb the water–sediment interface. Each sediment sample was a composite of five to six core samples (7 cm in diameter) collected over an area of about 100 m2 to reduce the intrasite spatial variability. Only the uppermost oxic layer of sediments (0.5 cm) was collected from each core. The grey–greenish color of the oxic layer enabled us to distinguish it from the lower anoxic dark layer. The bulk sediment samples were stored at –20°C until the extraction procedure. At six stations (LSL-8 to LSL-13), sufficient core samples were collected to allow the preparation of two composite samples rather than the usual single composite sample, allowing us to estimate within-site variation in total Hg concentrations in the sediments. Benthic invertebrates (mainly molluscs, amphipods, and insect larvae) were collected by scuba divers using a rectangular net with scraping movements in submerged macrophyte stands near the sediments. Benthic macroinvertebrates were immediately pooled in ice-cold containers and transferred to the laboratory. There, the organisms were sorted by species, and only adult specimens of the gastropod B. tentaculata (over maturity size 6 mm, Pinel-Alloul and Magnin 1971) were selected for analysis. For each site, one to © 2000 NRC Canada



Désy et al. three composite samples were prepared, depending on the abundance of the organisms; about 25 individuals were needed to obtain approximately 100 mg of soft tissues (dry weight), a sufficient weight for suitable analytical procedures. Bithynia tentaculata was found and collected at 20 of the 21 sampling stations. Because metal contents in the gut can contribute significantly to total metal burdens in benthic macroinvertebrates (Saouter et al. 1993; Amyot et al. 1996), we assessed the effect of gut contents on MeHg concentrations in B. tentaculata using depuration experiments (gut clearance). For 13 sampling stations, we took about 25 adult individuals of B. tentaculata and placed them on a sieve immersed in a bucket of filtered water (450 ng·g–1) were all located near the Îles-de-la-Paix in the southern part of Lake St. Louis (Table 1; Fig. 1C). The minimum value was observed in Lake St. Louis at station LSL-4. In Lake St. François (LSF-1 to LSF-4) and the region of Contrecoeur (CTC-1 to CTC-4), total Hg concentrations in sediments were lower and similar to concentrations observed in the northern and western sectors of Lake St. Louis (LSL-2 to LSL-6) (Table 1; Fig. 1C). For all sectors of the St. Lawrence River, total Hg contamination in sediments averaged 558 ng·g–1 but was highly variable, as reflected by standard deviations of magnitude similar or greater than the averages and coefficients of variation (CV) varying from 54 to 143% (Table 2). Although mean total Hg concentrations in the sediments of Lake St. Louis appeared to be higher than in the Lake St. François and Contrecoeur regions (Fig. 2A), no spatial differences were found in total Hg concentrations in sediments among the three studied sectors of the St. Lawrence River (Mann– Whitney U tests, P = 0.021–0.886) due to the small numbers of sampling stations in two of the three sectors and the high variability within each sector. To account for the large variation between the northern and southern stations in the Lake St. Louis sector, we compared the different sampling regions using four sectors instead of three: Lake St. Louis divided into sectors located north and south (LSL-north, LSL-south) of the Îles-de-la-Paix, Lake St. François (LSF), and the Contrecoeur region (CTC) (Fig. 2B). In this second analysis, a highly significant difference was found among sectors. Total Hg concentrations in sediments in the southern stations in Lake St. Louis were significantly higher than those observed in all three other sectors (Mann–Whitney U tests, P = 0.002– 0.005). MeHg in gastropods MeHg ranged from 15 (CTC-4) to 290 ng·g–1 (LSL-10) in undepurated gastropods and from 41 (LSF-4) to 420 ng·g–1 (LSL-10) in depurated gastropods (Table 1). As was the case for the sediments, the most contaminated Bithynia, either depurated or not, were collected at stations located south of the Îles-de-la-Paix in Lake St. Louis (LSL-1, LSL-8 to LSL-12). For the 13 stations where both depurated and undepurated gastropods were available, we did not find significant differences in MeHg concentrations between depurated and undepurated individuals (Wilcoxon matched-pairs test, Z = –0.175, P = 0.861). Mean MeHg concentrations in depurated gastropods (126 ng·g–1) (Table 2) were similar to those in the undepurated gastropods (92 ng·g–1). The CV of mean

Fig. 2. Mean concentrations of total Hg in sediments in (A) three sectors (CTC, Contrecoeur region; LSF, Lake St. François; LSL, Lake St. Louis) and (B) four sectors, with subdivision of Lake St. Louis (LSL-north, northern part of Lake St. Louis; LSL-south, southern part of Lake St. Louis). Error bars represent the sample standard deviation.

MeHg concentrations in gastropods was similar in the two groups within each sector and over all sectors in the St. Lawrence River (89.6% for the undepurated group and 87% for the depurated group) (Table 2). Based on pooled data from depurated and undepurated samples, MeHg concentrations in the gastropod soft tissues were higher in Lake St. Louis than in Lake St. François or the Contrecoeur region (Table 2; Fig. 3A) (Mann–Whitney © 2000 NRC Canada



Désy et al. Fig. 3. Mean concentrations of MeHg in gastropods (depurated and undepurated) in (A) three sectors (CTC, Contrecoeur region; LSF, Lake St. François; LSL, Lake St. Louis) and (B) four sectors, with subdivision of Lake St. Louis (LSL-north, northern part of Lake St. Louis; LSL-south, southern part of Lake St. Louis). Error bars represent the sample standard deviation.

U tests, P = 0.0002–0.002). When we divided Lake St. Louis into two subsectors (north and south), we found highly significant differences among sectors. MeHg concentrations in the gastropods from the south of Lake St. Louis were higher than those in the gastropods from the stations of all other sectors (Mann–Whitney U tests, P < 0.00001). Moreover, MeHg concentrations in gastropods from the northern sector of Lake St. Louis were significantly lower than those observed in Lake St. François (Mann–Whitney U test, P = 0.002). Relationships between sediment and Bithynia Hg contamination First, we established the relationships between total Hg in sediments and MeHg in gastropods including all data from undepurated and depurated gastropods from stations of all sectors (Fig. 4A). MeHg concentrations in gastropods were highly correlated with total Hg concentrations in the sediments (r = 0.83, P = 0.00001). Analysis of the residuals according to the three sectors (Lake St. François, Lake St. Louis, and Contrecoeur) indicated that there was no regional

169 Fig. 4. Relationships between concentrations of total Hg in sediments and MeHg in the gastropod B. tentaculata (depurated and undepurated) (A) with all sectors under study and (B) with data from Lake St. Louis only. Circles, Contrecoeur region; diamonds, Lake St. François; triangles, northern part of Lake St. Louis; squares, southern part of Lake St. Louis.

influence on the relationships between Hg contamination in sediments and gastropods (Kruskal–Wallis test, P = 0.22). The same conclusion was obtained when testing regional effects with four sectors by dividing Lake St. Louis into northern and southern parts (Kruskal–Wallis test, P = 0.18). Similarly, analyses performed to test the influence of gut contents on the relationships showed no significant effect (Kruskal–Wallis test, P = 0.41). Thus, the general equation log[MeHg]gastropods = 0.56(0.43–0.71) ´ log[total Hg]sediments + 0.50(0.13–0.82) is valid for predicting MeHg contamination in gastropods from total Hg contamination in sediments in all studied sectors along the fluvial corridor of the St. Lawrence River and for undepurated as well as depurated organisms. Confidence intervals (95%) for the slope and intercept are indicated in © 2000 NRC Canada



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parentheses. However, this general relationship is greatly influenced by stations in Lake St. Louis located south of Îles-de-la-Paix (Fig. 4A). Because the stations in Lake St. Louis encompassed the full gradient observed in Hg contamination in all sectors (Fig. 4A), we constructed another model considering only the data from Lake St. Louis (Fig. 4B). In this lake, total Hg in sediments and MeHg in gastropods were also highly correlated (r = 0.92, P = 0.00001) and the relationship was described by the following equation (confidence intervals at 95% for the slope and intercept are indicated in parentheses): log[MeHg]gastropods = 0.64(0.52–0.79) ´ log[total Hg]sediments + 0.25(–0.14–0.60). Residue analysis indicated that there were no differences in the deviations between predicted and observed MeHg concentrations in gastropods from the northern or southern sectors of Lake St. Louis (Kruskal–Wallis test, P = 0.14). Similar analyses performed to test the influence of gut contents on the relationships showed no significant effect (Kruskal–Wallis test, P = 0.31). A comparison between the St. Lawrence model and the Lake St. Louis model clearly showed that the slope and intercept of the Lake St. Louis equation were similar to those of the general equation.

Discussion Total Hg in sediments In our study, 12 of the 21 stations had sediment total Hg contents over 170 ng·g–1, the provisional Canadian environmental quality guideline in sediments for protection of aquatic life (Environment Canada 1997). In Lake St. Louis, all but three stations (LSL-4, LSL-5, LSL-7) had sediment Hg contamination over 170 ng·g–1. In the other sectors, only station LSF-3 located near Lancaster on the north shore of Lake St. François and station CTC-2 located downstream from the Sidbec-Dosco metallurgic plant in the Contrecoeur region showed total Hg concentrations in sediments above the proposed guideline. The small number of stations surveyed and the large variation in total Hg concentrations in sediments within and among sectors make it difficult to compare our results with previous studies conducted on Hg contamination in sediments of the St. Lawrence River. In Lake St. François, previous studies have reported a wide range in total Hg concentrations in sediments; most of the reported values fall in the range from