Article pubs.acs.org/est
Selenium Reduces the Retention of Methyl Mercury in the Brown Shrimp Crangon crangon Poul Bjerregaard* and Alan Christensen Institute of Biology, University of Southern Denmark, Campusvej 55, DK-5230 Odense M, Denmark ABSTRACT: Methyl mercury accumulated at the top of aquatic food chains constitutes a toxicological risk to humans and other top predators. Because the methyl mercury enters the aquatic food chains at the lower trophic levels, uptake and elimination processes at these levels affect the methyl mercury content at the higher levels. Selenium modulates the biokinetics of mercury in aquatic organisms in fairly complex ways, increasing mercury retention in some aquatic mammals, but decreasing methyl mercury retention in fish. However, it is not known if selenium modulates methyl mercury accumulation at lower trophic levels in aquatic food chains. Here, we show that selenium administered via the food augments the elimination of methyl mercury from marine shrimp and that the effect is dosedependent, demonstrable down to natural selenium concentrations in aquatic food items. Selenite, seleno-cystine, and seleno-methionine exert this effect but selenate does not. Our results suggest that the selenium naturally present at the lower trophic levels in marine food chains may play an essential role as a modifier of methyl mercury accumulation at these levels, thereby potentially also affecting biomagnification of methyl mercury toward the higher trophic levels in the aquatic food chains.
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INTRODUCTION At the higher trophic levels of aquatic food chains, methyl mercury may cause toxic effects in top predators among wildlife1 and neurological symptoms in children prenatally exposed via their mother’s marine diet.2 Although the direct discharge of mercury from point sources in the western world and the mercury concentrations in the atmosphere have been reduced considerably during the latest decades,3 anthropogenic mobilization of the metal via burning of fossil fuels still maintains the flux of mercury through the global atmosphere.4 The deposition from the atmosphere leads to elevated concentrations of methyl mercury in aquatic ecosystems − also in remote areas far from direct discharges of mercury.5,6 Methyl mercury is taken up from both food and water in most aquatic organisms and once assimilated, methyl mercury is retained very efficiently, with biological half-lives in various aquatic organisms typically ranging from several weeks in daphnia7 to years in larger crustaceans8,9 and some fish species.9,10 Because the assimilation efficiency from food is so high − in many cases approaching 100%11 − the retention time for the assimilated methyl mercury tends to be the more important parameter in determining the mercury level in an organism and most of the methyl mercury present in an aquatic food chain or food web has entered the biota at the lower trophic levels.12 Hence, the ability of the various species at the different levels of the food chain to eliminate methyl mercury determines the levels of methyl mercury attained at the upper end of the food chain. © 2012 American Chemical Society
Selenium interacts with the accumulation and toxicity of mercury in fairly complex ways (reviewed by ref 13) and fish in selenium contaminated areas have been shown to contain reduced amounts of mercury14,15 and fish16,17 and crayfish16 in experimental lakes treated with selenium decreased their mercury contents. Most previous laboratory investigations on the effects of selenium on mercury kinetics in fish and aquatic invertebrates have mainly dealt with interaction between the two elements in the uptake phase and most often with exposure to waterborne selenium forms (reviewed by ref 18); the results of these investigations show no consistent effects of selenium on the kinetics of mercury (organic and inorganic) and, hence, they fail to explain the observations from the field.14−17,19 Recently, it has been shown that exposure to dietary selenium strongly reduces the retention of methyl mercury in freshwater fish,20 but although this was very clearly established it may not be a universal phenomenon across all animal groups; for example, in mice, oral administration of selenium has little or no effect on the retention of methyl mercury.21−23 Therefore, we need to know if the effect of orally administered selenium on the retention of methylmercury may also be seen in organisms at lower levels in aquatic food chains. The present investigation was initiated to increase the understanding of selenium’s role in the retention of methyl mercury in organisms at the lower trophic level in aquatic food Received: Revised: Accepted: Published: 6324
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chains with the brown shrimp Crangon crangon as a model organism.
Table 1. Effect of Selenium on Retention of Methyl Mercury in the Brown Shrimp Crangon crangon; the Shrimp Were Exposed to Various Concentrations and Forms of Selenium in Food or Water and the Whole Body Retention of Assimilated Methyl Mercury Was Determined; r2 Is the Correlation Coefficient of the 1.Order Retention Curve; Within Each Experiment, Half Lives with No Common Letter Are Significantly Different
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EXPERIMENTAL SECTION We contaminated the shrimp with CH3203HgCl administered in food pellets. We then fed the shrimp uncontaminated food for approximately a week to allow unabsorbed mercury to be voided and assimilated mercury to distribute within the organism. Thereafter, we fed shrimp selenium enriched food or exposed them to waterborne selenium. We monitored retention of methyl mercury by regular determination of the radioactivity of the live shrimp in a gamma counter. The activity of each shrimp was set to 100%, the day the selenium exposure began. The retention of mercury was fitted to 1. order kinetics (Ct = C0*e−k*t) and the half-life calculated from the elimination coefficient as: T1/2 = ln 2/k. We made the food pellets from soft parts of blue mussels Mytilus edulis that were homogenized and solidified with gelatin. In one experiment, we used chicken breast muscle to obtain food with an artificially low selenium concentration. We determined the actual concentrations of selenium in the food by means of atomic absorption spectrometry. The effect of the form, concentration, and exposure route of selenium was investigated in 5 experiments. Experimental Animals. Shrimp Crangon crangon (L.) were caught at Kerteminde, Funen, Denmark, a site with no known contamination with mercury or selenium. After collection the shrimp were allowed to acclimate in aquaria for 2−6 days (natural seawater, 15 °C, light-dark cycle: 12:12 h). The salinities varied between 12 and 25‰. Experimental Setup. During experiments, the shrimp were held individually in beakers containing approximately 1 L of aerated, natural seawater. Every day the shrimp were offered food corresponding to 1.5 to 2% of their body weight. Any uneaten food was removed. The water was changed daily, approximately 1/2 h after feeding. Faeces and other materials were sucked up from the bottom of the beakers. Exposure Regimes. Groups of 10 to 20 shrimp were fed food pellets containing CH3203HgCl; each animal receiving two pellets on two consecutive days 7 to 9 days before the selenium treatment was initiated. The shrimp were then fed uncontaminated food for 5 to 7 days to allow unabsorbed mercury to be voided and assimilated mercury to distribute within the tissues. The 203Hg activity of the shrimp was determined regularly during the periods shown in Table 1. Preparation of Food. Soft parts from freshly caught mussels (Mytilus edulis) were homogenized in a food processor and mixed with gelatin and ultrapure water (containing the amounts of mercury and selenium wanted) in the ratio 0.65:0.25:0.1 The mixture was heated to 40−50 °C, stirred for 5−10 min, and poured into molds (80 × 80 × 1 mm) and frozen (−20 °C). In frozen condition, pellets weighing 6−9 mg wet weight were cut out as food for the shrimp. Chemicals. 203HgCl2 was obtained from the RISØ Research Centre, Denmark. Methyl mercury (CH3203HgCl) was prepared from 203HgCl2 according to Toribara.24 Selenite was from Fluka (>98% pure). Selenate, Se-methionine and Secystine were from Sigma-Aldrich (>98% pure). Gelatin was from Fluka. Experiments. In Experiment a, it was investigated if dietary selenite augments the elimination of methylmercury from C. crangon and if methyl mercury is eliminated via the faeces (further details given in Table 1). The water was filtered (1 μm filter) and the 203Hg activities in the water and faeces were
expt a
b
c
d
e
[Se] (μg Se g−1 wet weight)
form of Se added to food
0.34 13.5 28.8 0.34 19.0 23.4 18.5
none selenite selenite none selenite selenate Semethionine Se-cystine none selenite selenite selenite selenite none none selenite none selenite‡ selenite‡
18.8 0.34 0.79 1.84 5.0 12.7 0.06† 0.34 0.72 0.34 0.34 + 0.6‡ 0.34 + 4.7‡
n
duration of Setreatment (days)
r2
half-life for methyl mercury (days)
12 12 12 13 13 8 13
17 17 17 19 19 19 19
0.51 0.96 0.99 0.50 0.96 0.47 0.94
770a 157b 84c 770a 198b,c 462a,b 182b,c
13 10 10 10 10 10 20 20 20 17 17 17
19 11 11 11 11 11 24 24 24 16 16 16
0.97 0.38 0.81 0.91 0.87 0.90 0.22 0.46 0.72 0.47 0.64 0.94
151c 693a 239a 198a 210b 141b 1386a,b 630b 533b,c 770a 693a 165b
† Food made from homogenized chicken muscle. waterborne Se (mg L−1), also fed control food.
‡
Exposure to
measured in the 3 groups every day. The effect of various chemical forms (selenite, selenate, seleno-cystine and selenomethionine) on the retention of methyl mercury was investigated in experiment b (Table 1). Experiments c and d were carried out to investigate the effect of low selenium concentrations (shown in Table 1) on the retention of methyl mercury. In experiment d, a diet with an artificially low selenium concentration (made from homogenized chicken muscle, Table 1) was used. In experiment e, the effect of selenite in the water was tested. Dissection. After each experiment, shrimp were dissected into muscle, gills, exoskeleton, midgut gland and rest tissues. Each shrimp was dissected on a piece of paper towel and the activity of the paper was used as a measure for the methyl mercury activity in the hemolymph. Analysis of 203 MeHg Activity. The 203Hg activity in the live shrimp and tissues was determined by means of a Wizard 1480 3” automatic gamma counter. Values were corrected for radioactive decay. Selenium Measurements. Selenium concentrations were measured on a PerkinElmer MHS-20 Mercury/hydride system coupled to a PerkinElmer 2380 AAS as described by.25 Standard reference material (DORM-2 and TORT-2) was analyzed with each set of analyses. In every experiment, the selenium concentrations in both the selenium-dosed food and the control food were analyzed. The selenium concentrations were measured in the muscle, midgut gland, and gills. Because 6325
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addition of selenate to the diet did not (expt b of Table 1). Exposure to 5.0 and 12.7 μg Se-SeO32‑ g−1 in the diet increased the elimination of methyl mercury, whereas exposure to 0.79 and 1.84 only showed trends of this increase (expt c of Table 1). Shrimp on a diet with an artificially low selenium concentration retained methyl mercury with a half-life of 1386 days (Figure 2 and expt of d of Table 1). Exposure to 600
of the small amount of tissue in the gills and some of the midgut glands, these samples were pooled. Data Treatment. The statistical analyses were carried out in SYSTAT 7.0 (1997, SPSS Inc. 3/97) or in SPSS student version (SPSS Inc., 1989−1997). The data were checked graphically for normality and homogeneity. In all the experiments, ANOVA was used followed by Tukeýs multiple comparisons test. Repeated measures ANOVA analysis was used to check for difference in the retention of mercury between the groups. A significance level of α = 0.05 was used.
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RESULTS We showed that addition of selenium to the food of the marine shrimp Crangon crangon reduced the whole body retention of methyl mercury in the organism. Addition of 13.5 and 28.8 μg Se-SeO32‑ g−1 to the diet augmented the elimination of methyl mercury from C. crangon (part A of Figure 1 and expt a in Table
Figure 2. Half lives for methyl mercury in shrimp fed diets with various selenium concentrations. Artificially low selenium concentration (■), background selenium concentrations of mussels (○: mean ± SEM for 5 experiments), food amended with selenite (●), selenocystine (▼), or seleno-methionine (▲). Regressions shown for [Se]≤0.79 and [Se] > 0.79 μg Se g−1 wet weight.
μg Se-SeO32‑ L−1 in the water phase did not affect the whole body retention of methyl mercury, but retention decreased upon exposure to 4.7 mg Se-SeO32‑ L−1 (expt e of Table 1). Shrimp fed the natural background concentrations of selenium in the mussel diet retained methyl mercury with half-lives between 630 and 770 days (727 ± 28; SEM) in the 5 experiments. Administration of selenium − in the form of selenite, Se-cystine, or Se-methionine − in the food clearly augments the elimination of methylmercury from brown shrimp C. crangon. At low selenium concentrations (≤0.79 μg Se g−1), half-lives for methyl mercury are significantly correlated with the selenium concentration in the food (Figure 2); a correlation also exists for selenium concentrations between 0.79 and 29 μg Se g−1 in the food, but dependency of the half-life on the selenium concentration is less marked (Figure 2). After the elimination period, the major body burden of methyl mercury was present in the muscle tissue (50−55%) in the control shrimp, with 10 to 15% in the exoskeleton, approximately 2% in the midgut gland, 1 to 2% in the hemolymph, less than 1/2% in the gills and 20 to 30% in the rest (Figure 3). Exposure to selenium in the food did not cause major rearrangements of the body burden of methyl mercury. In the experiments where significant differences were found, methyl mercury burdens in muscle and midgut gland and in one case gills increased slightly, whereas the content in exoskeleton and rest tended to decrease. However, the effects of selenium exposure on the distribution of methyl mercury were so small and inconsistent that it was not possible to pinpoint specific tissues from which methyl mercury was lost upon selenium exposure (Figure 3).
Figure 1. Effect of selenite on whole body retention and faecal excretion of methyl mercury. Methyl mercury retained in shrimp receiving food containing 0.34 μg Se (○), 13.5 μg Se-SeO32‑ (▲), and 28.8 (■) μg Se-SeO32‑ g−1 wet weight. Mean ± SEM for 12 animals (A). Percentage of the total body burden (at day 0) retrieved in the faeces during the experiment (pooled samples from all animals in each group) (B).
1). In this experiment, faecal pellets were collected for examination of mercury elimination, and a dose-dependent increase in mercury elimination was observed with increasing selenium exposure (part B of Figure 1). The cumulated amount of mercury retrieved in the faecal pellets over the experimental period accounted for 75%, 57%, and 44% respectively of the mercury lost from the shrimp exposed to 0.34, 13.5, and 28.8 μg Se g−1 food. Of the chemical forms of selenium tested at 18 to 24 μg Se g−1, selenite, seleno-cystine, and seleno-methionine reduced the whole body retention of methyl mercury whereas 6326
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Figure 4. Selenium concentrations in the tissues of brown shrimp at the end of the experiments. Symbols as in Figure 4.
Figure 3. Tissue distribution of the methyl mercury in the shrimp at the end of the experiments. Shrimp exposed to selenate, selenocystine, seleno-methionine, and selenite at 18−23 μg Se g−1 food (A). Shrimp exposed to 0.79, 1.86, 5.0, or 12.7 μg Se-selenite g−1 food (B). Shrimp exposed to 0.6 or 4.7 mg Se-selenite L−1 in the seawater (concomitantly fed control food) (C). Shrimp exposed to an artificially low selenium concentration in the food (chicken muscle) or 0.72 μg Se-selenite g−1 (D). Control food in all experiments contained 0.34 μg Se g−1. Groups with no letter in common (within each experiment and tissue) are significantly different. Mean ± SEM; n and duration of the experiments are given in Table 1.
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DISCUSSION Retention of accumulated methyl mercury in aquatic organisms has been reported to show fairly large variations with half-lives from 17 d in daphnia7 to years in some fish species, e.g. pike Esox lucius9 (140−600 d) and rainbow trout Oncorhynchus mykiss10(202−516 d). Half lives for methyl mercury ingested via the food in Crangon crangon consistently ranged between 630 and 770 days in the present study and this does deviate substantially from the half-lives reported for other decapod crustaceans such as the shrimp Lysmata seticaudata8 (529 d), the shore crab Carcinus maenas26,27 (400−700 d) and the freshwater crayfish Astacus astacus9 (144−297 d). The results of the present experiments help explain why crustaceans living in environments experimentally enriched with selenium show decreased concentration of mercury, although previous laboratory experiments have failed to identify any effect of waterborne selenium on the uptake and assimilation of methyl mercury.28 It appears to be crucial for the diminishing effect of the selenium on the retention of the methyl mercury that the selenium is administered in the food rather than in the water. Natural background concentrations of dissolved selenium forms in both freshwater and marine environments are in the low nanogram per liter range29,30 and it takes extraordinary high selenite concentrations in the water phase (mg L−1 range) to affect the retention of methyl mercury (and adsorption of the dissolved selenite to the food items cannot be excluded). In aquatic ecosystems, however, the selenium concentrations in the organisms along the food chain increase with increases in the concentrations of dissolved
C. crangon contained approximately 1 μg Se g−1 dry weight in muscle and gills and 2−3 μg Se g−1 in the midgut gland (Figure 4). Selenium concentrations in the muscle increased significantly after 11 days’ exposure to 5 and 12.7 μg Se g−1 in the food (part B of Figure 4) and midgut gland and gill concentrations also appeared to increase after exposure to 1.8 μg Se g−1 (part B of Figure 4) although no statistical treatment could be carried out due to the pooling of the tissue samples. Twenty-three days’ exposure to 0.72 μg Se g−1 caused a statistically significant increase in the selenium concentration in muscle (part D of Figure 4). Exposure to selenite, Se-cystine, and Se-methionine in the food resulted in augmented selenium concentrations in the tissues (part A of Figure 4), whereas exposure to selenate did not. Exposure to 600 and 4700 μg Se L−1 in the water augmented selenium concentrations in muscle and apparently gills, but only exposure to 4700 μg Se L−1 showed a statistically significant effect in the midgut gland (part C of Figure 4). 6327
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selenium30 and, in long-term in situ experiments or in selenium-contaminated areas, the general levels of selenium in organisms − and thereby food items − are elevated.16,30 In organisms, selenium tends to be present in organic forms13,31 rather than as the selenite used in the majority of the present experiments. However, the fact that selenite, selenocystine and seleno-methionine had similar effects on the whole body retention of methyl mercury when added to the food (albeit at fairly high concentrations) indicates that the chemical form of the selenium may not be important for the effects on mercury retention, provided the form is not selenate. Similar conclusions were made in an investigation on the effect of selenium on retention of methyl mercury in goldfish Carassius auratus.20 Marine organisms generally have higher selenium concentrations than terrestrial organisms and chicken breast −although somewhat unnatural − was chosen as the basis for the low selenium diet. Sixty-seven and 20% of the selenium in chicken breast muscle were shown to consist of selenomethionine and seleno-cystein respectively,32 and thus the selenium forms in the chicken muscle are not fundamentally different form the forms found in marine bivalves.33 However, it cannot be excluded that other constituents than the low selenium content in the chicken muscle may be responsible for the higher half-life for methyl mercury in this particular experiment. The selenium concentrations found in the tissues of the control shrimp were in the same ranges as selenium concentrations earlier reported for marine, decapod crustaceans.28,34,35 The exposure to elevated concentrations of selenite and seleno-cystine and seleno-methionine in the food generally increased the selenium concentrations in all tissues whereas exposure to selenate had little or no effect. It is consistent with results from investigations on other marine invertebrates that uptake of selenite is much more efficient than uptake of selenate.36 In C. crangon selenium, exposure leads to a reduction of the whole body burden of methyl mercury caused by increased elimination. In another decapod, the shore crab Carcinus maenas, selenium exposure does not result in a decreased body burden of methyl mercury,26 but to a major redistribution of the accumulated methyl mercury among the tissues;37 in selenium exposed crabs the concentration in the muscles increases, whereas the concentration in the midgut gland decreases. This difference in the effects of selenium on the methyl mercury kinetics between the two decapod species merits further investigation. Although the majority of the methyl mercury ending up in the top predators of the aquatic ecosystems actually enters the food chain at the lower trophic levels,12 the presence, behavior, and transport of methyl mercury at these lower levels are less understood than at the higher levels. Nevertheless, modifications of assimilation and retention of methyl mercury at the lower levels of the food chains are bound to affect the levels of mercury in the top predators. In the brown shrimp, very small changes in the selenium content in the food appear to have a strong modulating effect on methyl mercury retention at natural background concentrations of selenium. In a recent investigation19 on the mercury and selenium concentrations in streams of the western USA, it was concluded that ‘high Hg concentrations in fish tissue.... were found only when Se concentrations in the same tissue were low’. The results of the present investigation underlines the need to consider the effect
of selenium on methyl mercury biokinetics as well as the interactions at the biochemical level in the tissues if the full mechanisms underlying selenium’s influence on mercury biomagnifications and toxicity are to be elucidated. The chemical/biochemical mechanism underlying the effect of selenium on the retention of methyl mercury in C. crangon is not known. Selenium may interact with mercury in a multitude of ways,13,38 but these biochemical interactions have been investigated in vertebrates only. The facts that a substantial amount of the methyl mercury excreted from C. crangon is lost via the faeces and that dietary selenium seems more efficient than waterborne selenium might suggest that the important interaction takes place in the gut. It might be speculated that selenium may interrupt an internal recirculation of methyl mercury similar to the entero-hepatic recirculation known to be present in fish.39 Fish exposed to selenium in the diet lose mercury from the general body rather than from any particular organ20,40 and the fact that the effect in the shrimp is similar might support this suggestion. However, further research is needed if the underlying mechanism is to be elucidated.
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AUTHOR INFORMATION
Corresponding Author
*Phone: +45 6550 2456, fax: +45 6550 2786, e-mail: poul@ biology.sdu.dk. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS This investigation was supported by grants from the Danish Natural Science Research Council.
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REFERENCES
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dx.doi.org/10.1021/es300549y | Environ. Sci. Technol. 2012, 46, 6324−6329
