Biomagnification and bioaccumulation of mercury in an arctic marine

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assess mercury biomagnification within this extensive arctic marine food web. Résumé ..... support. Financial support to K.A.H. was provided by the Sci-.


Biomagnification and bioaccumulation of mercury in an arctic marine food web: insights from stable nitrogen isotope analysis Lisa Atwell, Keith A. Hobson, and Harold E. Welch

Abstract: Several recent studies have shown that the use of δ15N analysis to characterize trophic relationships can be useful for tracing biocontaminants in food webs. In this study, concentration of total mercury was measured in tissues from 112 individuals representing 27 species from the arctic marine food web of Lancaster Sound, Northwest Territories. Samples ranged from particulate organic matter through polar bears (Ursus maritimus). Using δ15N values to identify trophic position, we found that total mercury in muscle tissue biomagnified in this food web. Polar bears were a notable exception, having a lower mean mercury concentration than their main prey, ringed seals (Phoca hispida). Most vertebrates showed greater variance in mercury concentration than invertebrates, and there was a trend in seabirds toward increased variability in mercury concentration with trophic position. Within species, we found no evidence of bioaccumulation of mercury with age in the muscle tissue of clams (Mya truncata) or ringed seals. Because stable nitrogen isotopes illustrated the relationship in this biome between trophic position and mercury level on a continuous, quantitative scale, we were able to determine that log10[Hg] (µg/g dry weight) = 0.2(δ15N) – 3.3. The measurement of δ15N values and mercury concentration allowed us to quantitatively assess mercury biomagnification within this extensive arctic marine food web. Résumé : Plusieurs études récentes ont montré que l’utilisation d’une analyse du δ15N pour caractériser les relations trophiques peut être utile pour suivre les biocontaminants dans les réseaux trophiques. Dans la présente étude, nous avons mesuré la concentration totale du mercure dans les tissus de 112 individus représentant 27 espèces appartenant au réseau trophique marin arctique du détroit de Lancaster, dans les Territoires du Nord-Ouest. Les échantillons allaient de particules de matière organique à des tissus prélevés sur des ours blancs (Ursus maritimus). En nous servant des valeurs de δ15N pour déterminer la position trophique, nous avons mis en évidence une bioamplification de la teneur en mercure total dans les tissus musculaires dans ce réseau trophique. Les ours blancs constituaient une exception notable, car leurs tissus avaient une concentration moyenne en mercure plus faible que ceux de leur principale proie : le phoque annelé (Phoca hispida). Les concentrations de mercure notées chez la plupart des vertébrés ont montré une variance supérieure à celles obtenues pour les invertébrés; et on a observé chez les oiseaux marins une tendance à une variabilité accrue de la concentration de mercure en fonction de la position trophique. Au sein d’une espèce, nous n’avons trouvé aucune preuve de bioamplification du mercure en fonction de l’âge dans les tissus musculaires de la mye tronquée (Mya truncata) ou du phoque annelé. Puisque les isotopes stables de l’azote illustraient dans ce biome la relation entre la position trophique et la teneur en mercure selon une échelle quantitative continue, nous avons pu déterminer que log10[Hg] (µg/g de poids sec) = 0,2(δ15N) – 3,3. La mesure des valeurs de δ15N et de la teneur en mercure nous a permis d’évaluer quantitativement la bioamplification du mercure dans ce vaste réseau trophique marin arctique. [Traduit par la Rédaction]

Introduction Previous studies investigating the potential for mercury to biomagnify progressively through higher trophic levels of food webs have produced varied results. While several researchers have found evidence for biomagnification of mercury with trophic level (e.g., Riisgard and Hansen 1990; Futter 1994; Jarman et al. 1996), others have found no such relationship

(Williams and Weiss 1973; Wagemann and Muir 1984). Disagreement in findings may be due, in part, to the difficulty of accurately characterizing trophic structure in complex food webs. Traditional methods of assessing trophic position have depended largely on inferred feeding behaviour or stomach content analysis (Rowan and Rasmussen 1992; Futter 1994). These methods can be limited, since they usually provide only a “snapshot” of feeding habits for a particular season, life

Received April 8, 1997. Accepted December 23, 1997. J13956 L. Atwell. Department of Biology, University of Saskatchewan, Saskatoon, SK S7N 0W0, Canada. K.A. Hobson.1 Department of Biology, University of Saskatchewan, Saskatoon, SK S7N 0W0, Canada, and Canadian Wildlife Service, Prairie and Northern Wildlife Research Centre, 115 Perimeter Rd., Saskatoon, SK S7N 0X4, Canada. H.E. Welch. Department of Fisheries and Oceans, Freshwater Institute, 501 University Crescent, Winnipeg, MB R3T 2N2, Canada. 1

Author for correspondence at Canadian Wildlife Service, Prairie and Northern Wildlife Research Centre, 115 Perimeter Rd., Saskatoon, SK S7N 0X4, Canada. e-mail: [email protected]

Can. J. Fish. Aquat. Sci. 55: 1114–1121 (1998).

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history stage, or location. These snapshots may not necessarily reflect an organism’s long-term feeding habits, which can ultimately influence its contaminant load. Changes in diets and varying degrees of omnivory in consumers can also confound the process of accurately assessing trophic position (e.g., Rowan and Rasmussen 1992; Futter 1994). The measurement of stable isotopes of nitrogen (15N/14N) has recently become useful as an alternative method to characterize trophic level (reviewed by Michener and Schell 1994). Enrichment (i.e., an increase in relative abundance of 15 N) on the order of 3–5‰ generally occurs at each trophic transfer (DeNiro and Epstein 1981; Minagawa and Wada 1984; Hobson and Welch 1992). Measurement of the relative abundance of 15N in organisms provides a continuous variable, then, by which trophic position can be quantitatively assessed. This method offers a useful alternative for characterizing food web structure because it is a time-integrated measure of dietary components and therefore not subject to the same temporal bias as stomach content analysis (DeNiro and Epstein 1981; Tieszen et al. 1983; Hobson and Clark 1992) . Moreover, trophic positioning of organisms by stable nitrogen isotope analysis is based on assimilated (not just ingested) food, and trophic estimates can reflect dietary integrations over many meals, depending on the tissue analyzed (e.g., Tieszen et al. 1983). The time frame over which the δ15N value of a tissue represents the trophic position of an organism depends on the tissue’s specific rate of turnover (e.g., Hobson and Clark 1992). However, caution should be exercised when comparing δ15N values between food webs, since baseline δ15N values may vary from system to system (Cabana and Rasmussen 1996). Often, δ15N values can only be interpreted relative to other organisms in the same food web, or by comparison with a species common to all food webs under observation. Several recent studies have used stable nitrogen isotope measurements to describe the biomagnification of lipophilic contaminants in freshwater and marine ecosystems (Cabana and Rasmussen 1994; Kiriluk et al. 1995). Kidd et al. (1995b) concluded that the regression slope of the logarithmic concentration of total dichlorodiphenyltrichloroethane (ΣDDT), total hexachlorocyclohexane (ΣHCH), and total chlorinated bronanes (ΣCHB) versus δ15N represented the degree of biomagnification in a subarctic lake. Broman et al. (1992) and Rolff et al. (1993) developed biomagnification models of polychlorinated dibenzo-p-dioxins (PCDD) and dibenzofurans (PCDF) for two Baltic marine food webs using δ15N as a numerical representative of trophic position. Recently, Jarman et al. (1996) used δ15N analysis to investigate the behaviour of both lipophilic and metal contaminants in the marine food web of the Californian Gulf of the Farallones. Their study illustrated that mercury was strongly associated with δ15N and hence trophic level, indicating that mercury biomagnified in that food web. Kidd et al. (1995a) found a similar association between mercury and δ15N in fish from several freshwater lakes in Canada. Previous investigations in the Canadian Arctic have revealed mercury levels in biota to be higher than might be expected in pristine environments (Smith and Armstrong 1975; Wagemann et al. 1983). Some researchers have found mercury contamination in the Arctic to be highest in upper trophic level biota from northwestern regions (Norstrom et al.


1986; Braune et al. 1991). As there are practically no sources of industrial mercury in the arctic environment, geologic sources and atmospheric transport from developed regions appear to be the most likely origins of mercury in arctic marine food webs (e.g., Braune et al. 1991). Recently, Hobson and Welch (1992) used stable isotopes of nitrogen to examine trophic relationships among organisms from the marine food web of Lancaster Sound, Northwest Territories. Here, we extend their findings by examining the relationship between δ15N, as an indicator of trophic position, and mercury levels in the tissues of a subsample of those organisms. The demonstration that δ15N characterized the structure of this complex food web was used to explore the magnitude of mercury biomagnification in 112 individuals representing 27 different species ranging from particulate organic matter (POM) and algae through polar bears (Ursus maritimus). As well, mercury concentration in two long-lived species, clams (Mya truncata) and ringed seals (Phoca hispida), was examined for evidence of bioaccumulation with age. To our knowledge, this is the most extensive food web for which mercury biomagnification has been assessed quantitatively.

Materials and methods Sample collection From the previous collections of Hobson and Welch (1992), we obtained tissues from 11 species of invertebrates, two species of fish, eight species of marine birds, two species of toothed whales, walrus (Odobenus rosmarus), and polar bear (summarized in Table 1) for which δ15N had been determined. All samples were from the region of Lancaster Sound and collected between 1988 and 1990 (see Hobson and Welch 1992 for a description of sampling methods). Additionally, clams and ringed seals were collected from the region of Barrow Strait in 1990 to examine whether mercury accumulated with age. Seal tissue and teeth were provided by local Inuit hunters from unsexed animals. Clams and seals were aged at the Freshwater Institute, Winnipeg, Manitoba, by counting annular growth rings on shells and teeth. Both δ15N and mercury analyses were performed on muscle tissue, except for small ( 0 indicates that the transfer efficiency of a contaminant is greater than the biomass transfer efficiency (biomagnification), and B < 0 indicates a contaminant transfer efficiency less than that of the biomass transfer efficiency (Rolff et al. 1993). The biomagnification power (0.20) of mercury observed in © 1998 NRC Canada


this arctic marine food web is of similar magnitude to that observed in freshwater fishes (i.e., 0.2–0.3) from several lakes by Kidd et al. (1995a), who also determined trophic position using δ15N values in muscle tissue. Kidd et al. (1995a) described mercury biomagnification in a subset of the food web (i.e., fishes) whereas the biomagnification power of 0.20 found in our study is the overall biomagnification of mercury through many groups (i.e., invertebrates, fish, birds, mammals). Our description of biomagnification does not reflect the potential of mercury to biomagnify in specific subsets of this food web. For example, invertebrates in our study, taken as a subset, showed no biomagnification with trophic position (log10[Hg] (µg/g) = –0.04(δ15N) – 0.73). Similarly, as reveiwed by Boudou and Ribeyre (1995), benthic invertebrate food webs in Swedish forest lakes did not biomagnify mercury, since detrivores had higher mercury levels than predatory invertebrates. This strongly suggests that there may be different transfer mechanisms occurring at different levels of the food web. Jarman et al. (1996) found the overall biomagnification power of mercury in the Gulf of the Farallones food web to be 0.32 (values in Jarman et al.’s (1996) table 2 converted from ln[Hg] to log 10[Hg] for comparison with the results presented here). In Jarman et al.’s (1996) study, the Gulf of the Farallones food web was represented largely by marine birds which may assimilate mercury differently rate than metabolically less active organisms such as many invertebrates. It should be noted that Jarman et al. (1996) analyzed mercury concentration in a variety of tissues, including egg albumen, and their results may not be directly comparable with our findings based on muscle tissue. Boudou and Ribeyre (1995) suggested that omnivory or differences in metabolic rate or feeding ecology may influence the trophic transfer of mercury. Mean mercury levels and δ15N values of species showed a trend of increasing variability in mercury levels with increasing trophic position. In general, vertebrates had wider ranges of mercury concentrations in their tissues than did invertebrates (Fig. 1). Higher trophic level organisms are more likely to be migratory and to have larger foraging ranges than low trophic level organisms. Thus, among high trophic levels, individuals of the same species may encounter quite different levels of dietary mercury during certain seasons, or even during individual foraging excursions. Mercury concentration among eight arctic seabird species showed notably more variation in upper trophic position birds. Although differences in mean mercury levels among species were not statistically significant, the dovekie and eiders at the lowest trophic levels had mercury levels almost an order of magnitude lower than the highest trophic level birds (gulls, murres, and black-legged kittiwakes). Birds incorporate mercury into feathers (e.g., Thompson et al. 1992), and Furness et al. (1986) suggested that feather moult reduces mercury body burdens through the loss of mercury bound to feather keratin (see also Thompson et al. 1991). Mercury sequestered in plumage may account for up to 93% of the total body burden (Braune and Gaskin 1987), and regular elimination of mercury during moult may reduce interspecific differences in accumulated mercury. Alternatively, mercury levels in seabirds may be more influenced by age than by trophic position. For example, Särkkä et al. (1978) found differences in total mercury content between muscle

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tissue of juvenile and adult aquatic bird species from a large lake in Finland. As well, Dietz et al. (1990) found a wide range of mercury concentrations in arctic marine birds in Greenland. However, both Hutton (1981) and Thompson et al. (1991) found no evidence of mercury accumulation with age in several seabird species and suggested that individual diet was the important factor affecting variability of mercury levels in soft tissues. Polar bears had a mean δ15N value 3.2‰ higher than their main prey, ringed seals. Mercury levels in polar bears, however, were generally lower than in ringed seals. Polar bears preferentially consume seal skin and fat (Norstrom et al. 1986) which, in many marine mammals, are low in mercury content relative to other tissues (Sergeant and Armstrong 1973; Muir et al. 1988). Polar bears are therefore exposed to less dietary mercury than other animals that consume whole bodies, or mostly muscle, of their prey. Muscle tissue contains more of the body burden of mercury than other tissues, including liver which has a higher concentration, because muscle is relatively more abundant (see Pentreath 1976a). As well, Dietz et al. (1990) noted the unusually high capacity of polar bear kidneys for storing mercury and suggested that this caused their blood mercury levels, and therefore muscle mercury levels, to be lower than in other marine mammals. While previous studies suggest that mercury levels tend to be greater in tissues of higher trophic level organisms (e.g., Riisgard and Hansen 1990; Futter 1994), it is unclear to what extent this is a result of biomagnification through the food web or bioaccumulation within organisms over time. This can be difficult to discern, as higher trophic level organisms tend to be longer lived and therefore have more potential for accumulating mercury in their tissues. Some authors have suggested that mercury accumulates with age (e.g., Dietz et al. 1990; Wagemann et al. 1990) and that the food chain accounts for very little magnification of mercury (Williams and Weiss 1973), but we find no such evidence in either clams (age ranging over 42 years) or ringed seals (age ranging over 24 years). This discrepancy is possibly due to the type of tissue chosen for analysis. In marine mammals, mercury concentration in liver tissue is up to two orders of magnitude higher than in muscle (e.g., Sergeant and Armstrong 1973). Mercury also accumulates over time more readily in liver than in muscle, but experiments with rainbow trout (Oncorhynchus mykiss) indicate that muscle appears to retain the mercury burden for a much longer period during depuration (Boudou and Ribeyre 1995). Thus, liver may provide information only on short-term exposure to mercury or may accumulate mercury only when an organism is exposed to constant or increasing levels of dietary mercury. Smith and Armstrong (1975) found a weak, but inconsistent correlation of total mercury with age in muscle of ringed seals, and Wagemann et al. (1990) found no correlation between muscle mercury levels and age in beluga whales from the Canadian Arctic. However, Honda et al. (1983) observed that levels of total mercury in muscle tissue of striped dolphins (Stenella coeruleoalba) reached a plateau around 15 years of age. There does not appear to be strong evidence that mercury accumulates in muscle tissue with age; however, for seals, this may be confounded by the fact that reproductive females reduce their toxicant loads during pregnancy and nursing (Wagemann et al. 1988; André et al. 1990). Small amounts of © 1998 NRC Canada

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mercury may be passed through milk while the pup is nursing during the first 5–7 weeks. However, the amount of mercury ingested with milk is not enough to account for the levels of mercury found in pup tissues (Wagemann et al. 1988). Milk is extremely high in fat, and mercury is found in relatively low levels in lipids (Sergeant and Armstrong 1973; Wagemann et al. 1983), so this is not likely to be a major pathway for mercury transfer. Alternatively, mercury transfer can occur during gestation between mother and fetus as methyl mercury (i.e., organic mercury) readily passes across the placental barrier (Jernelov 1986). This may result in increased pup mercury levels, with concurrent decreases in body burden of the mother. Honda et al. (1983) attributed a relatively wide variation of mercury levels in female striped dolphins of reproductive age to parturition and lactation. Young-of-the-year seals displayed greater variability in δ15N values (mean 15.9 6 1.3‰) and lower mean mercury levels (0.57 6 0.27 µg/g) than seals older than 1 year (16.4 6 0.9‰ and 1.31 6 0.45 µg/g, respectively). A decrease in δ15N may occur upon weaning when the diet shifts from milk (i.e., same trophic level as adult seals) to fish, amphipods, euphausiids, and crustaceans, all at lower trophic positions (e.g., Hobson and Welch 1992). Mercury concentrations in muscle tissue of young seals may decrease after birth as the proportion of maternally derived fetal tissue decreases relative to diet-derived tissue. As well, ringed seals reach about 70% of adult length by age 1 (Frost and Lowry 1981), and this rapid rate of growth with no concomitant increase in dietary exposure to mercury may physically “dilute” mercury taken up through the diet (Boudou and Ribeyre 1995). Clams did not show a significant accumulation of mercury with age or with size. However, an unexpected finding was the marginally significant correlation between age and δ15N of clams. This suggests perhaps some physiological shift in food assimilation with age, or a change in the size and relative trophic position of particles filtered by larger clams. Conversely, Minagawa and Wada (1984) found δ15N to be independent of age in two species of marine mussels up to about 8 years old. Again, further analysis of this relationship would be useful. In this study, total concentrations of mercury were measured, but it should be noted that organic and inorganic species of mercury have very different dynamics within a food web. Most mercury present in seawater is in the inorganic form (Pentreath 1976b); however, benthic invertebrates take up organic mercury much more readily than inorganic mercury (Riisgard and Hansen 1990). Fish take up mercury directly from seawater (Pentreath 1976b) as well as diet (Riisgard and Hansen 1990) and show high concentrations of organic mercury in muscle tissue relative to both diet and seawater (Riisgard and Hansen 1990). Aquatic birds have also been found to have very high ratios of organic to inorganic mercury in muscle tissue (up to 100%, Särkkä et al. 1978; Thompson et al. 1991), and most mercury in marine mammal muscle is organic (Dietz et al. 1990). However, the ratio of organic to inorganic mercury in liver of fish (Pentreath 1976a), birds (Thompson et al. 1991; but see Thompson and Furness 1989), and marine mammals (e.g., Dietz et al. 1990) is low, relative to muscle tissue, and to overall body burdens in prey. Demethylation occurs in the liver, and so, it is the less toxic inorganic form that is sequestered in this organ;


however, no mechanism has been found (Smith and Armstrong 1975 (seals); Thompson and Furness 1989 (birds); Dietz et al. 1990 (polar bears)). Our δ15N values in tissues from a broad range of arctic marine animals described their trophic position quantitatively on a continuous scale. Such an illustration of trophic positioning allowed for a more detailed account of the relationship between mercury and trophic position for this extensive food web. Mercury increased with trophic position at an overall biomagnification power of 0.20, and we did not find evidence that mercury accumulation in muscle tissue was linked with age. These findings indicate that total mercury burdens in muscle tissue are a result of biomagnification through the food web rather than bioaccumulation. Further studies on the dynamics of both organic and inorganic mercury would improve our understanding of mercury behaviour in food webs, and future work should concentrate on using the stable-isotope method to further explore the behaviour of both species of mercury.

Acknowledgements We thank the Polar Continental Shelf Program for logistical support. Financial support to K.A.H. was provided by the Science Institute of the Northwest Territories, the Northern Studies Training Program, a Natural Sciences and Engineering Research Council of Canada (NSERC) Postgraduate Scholarship, and a University of Saskatchewan Graduate Fellowship. Stable-isotope analyses were conducted at the laboratory of Chris van Kessel, Department of Soil Sciences, University of Saskatchewan, Saskatoon, Sask., and mercury analyses were performed at the laboratory of Robert Hunt at the Freshwater Institute, Winnipeg, Man. We also thank Carolyn Ranson for assistance with mercury sample preparation and two anonymous reviewers for valuable comments on an earlier draft of this manuscript.

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