Hepatic trace element concentrations of breeding female common eiders across a latitudinal gradient in the eastern Canadian Arctic
Introduction
A variety of trace elements, many of toxicological interest (e.g., cadmium - Cd, mercury - Hg, selenium - Se) are elevated in Arctic wildlife species (Muir et al., 1999, AMAP, 2009). This is attributable in part to long-range transport to Arctic ecosystems from anthropogenic sources (e.g., emissions from industrial activity) in tropic and temperate regions to the south (Bidleman et al., 2003), and in part to natural variation in environmental levels (Braune et al. 1991). For many years, researchers around the circumpolar north have monitored levels of contaminants in Arctic wildlife, and in the case of trace elements, particular focus has been on Hg (Rigét et al., 2011), while much less attention has been given to other elements (but see Rigét et al., 2004, Campbell et al., 2005, Øverjordet et al., 2015). In general, contamination of species that are harvested for food is of great concern to northern indigenous communities because many northern people still rely heavily on wild food to fulfill cultural and dietary needs (Kinloch et al., 1992, Priest and Usher, 2004, AMAP, 2009, Ford, 2009).
The common eider (Somateria mollissima) is a useful species to monitor trace elements in the north because they are harvested around most of the circumpolar Arctic for sport and subsistence, they accumulate trace elements, often in high concentrations (e.g., Norheim, 1987, Wenzel and Gabrielsen, 1995, Franson et al., 2000, Wayland et al., 2001, Wayland et al., 2002, Lovvorn et al., 2013, Mallory et al., 2014, Fenstad et al., 2017), and some literature reports concentrations that suggest there are local and broad regional patterns in trace elements concentrations within the species. In one review, Mallory et al. (2004) found evidence of significant regional differences in trace element concentrations in tissues, with Se and Hg higher in liver and muscle tissue of eiders breeding around Hudson Bay, Nunavut, Canada than elsewhere. More recently, Pratte et al. (2015) showed that eiders nesting farther north in Canada had higher Hg in their eggs, and for colonies located > 55°N, egg Se declined with increasing latitude. Marked differences in arsenic (As) and Cd in eggs among colonies were also detected (Pratte et al. 2015). Given these findings, the work presented here builds on existing data, and further explores how trace element concentrations in eiders may be related to latitude and other spatial patterns in the region.
In this study, we examined concentrations of essential and non-essential trace elements in livers of breeding female common eiders from three sites separated by approximately 20° in latitude across northeastern Canada. Previously we reported on increasing trends over time of hepatic Cd and zinc (Zn) in these samples (Mallory et al. 2014). Here, our objectives primarily focused on examining spatial patterns using a suite of nine elements. First, we assessed whether hepatic trace concentrations differed among eiders at these widely separated colonies, and particularly if they followed the pattern established by recent sampling of eggs (Pratte et al. 2015). We predicted that hepatic Hg would increase with increasing latitude, while Se and As would decrease. Second, we examined interactions between elements. In particular, studies have shown that high Se can prevent toxic effects of Hg (Ralston et al., 2007, Sørmo et al., 2011), but in marine birds this typically happens around molar Hg:Se ratios near 1 (Kim et al., 1996). Eiders rarely reach this ratio (Braune and Scheuhammer, 2008, Fenstad et al., 2017), so we did not expect high ratios for these sites. Importantly, although any single element may affect a species, increasingly there is evidence that many interactions may occur within the body between trace elements. Some elements have negative impacts on biota (e.g., Hg), but there are also combinations of elements that may reduce the toxicity of single elements (Shore et al., 2011). Additionally, some mixtures of elements can have a stronger negative effect than those that occur independently (Sarigiannis and Hansen, 2012), which can lead to cumulative effects in biota (Provencher et al. 2016). Lastly, we used multivariate analysis of hepatic trace element concentrations to explore whether the suite of trace elements varied in some related pattern across our sampling colonies, as a basis for future work using trace elements as geotracers of breeding origin.
Section snippets
Methods
We collected breeding female common eiders from three colonies in eastern Canada: Table Bay, Newfoundland and Labrador (53.7°N, 56.6°W; 8 June 2008), East Bay (64.1°N, 81.7°W; 28 July 2008) and Tern (Nasaruvaalik) Island, Nunavut (75.8°N, 96.3°W; 14 July 2008; Fig. 1). At each site, 10 females were either caught on their nest about one week into incubation (hence sitting on their full clutch) and euthanized by cervical dislocation, or were shot with a shotgun using #2 steel shot. Timing of egg
Results
Female eiders nesting at the three colonies where individuals were collected had significantly different concentrations of hepatic As, Hg, Mn, Rb and Se, while concentrations of Cd, Cu, and Zn were similar across sites (Table 1). As, Se and Hg were lowest in eiders from the northernmost colony, Tern Island (Tukey Honest Significant Difference, p < 0.05). However, molar Hg:Se ratios were similar across all locations, and across sites eiders with high molar Hg did not have significantly higher
Discussion
Across our samples, the majority of common eiders had hepatic concentrations of trace elements that were below toxicological thresholds (Puls, 1994, Beyer and Meador, 2011) where adverse effects (e.g., tissue or organ damage, reduced physiological performance or reproductive output) have been noted (converted to dw: Se > 33 μg/g, Heinz, 1996; Hg 100 μg/g, Thompson, 1996; Pb 7–168 μg/g, Franson, 1996). The exceptions were for Cd and Zn, which we reported previously had increased by 300% over two
Acknowledgements
Financial and logistic support were provided by Environment Canada, Natural Resources Canada (Polar Continental Shelf Program), Natural Sciences and Engineering Research Council of Canada (Grants 418551-2012, 424234-2012), and a Nasivvik Centre Undergraduate Student Award to CDM. All collections were made under appropriate territorial, provincial or federal wildlife permits. We thank the many field assistants who helped collect the samples, notably R. Kelly, I. Buttler, K. Allard and J.
References (72)
- et al.
Inter- and intraclutch variation in egg mercury levels in marine bird species from the Canadian Arctic
Sci. Total Environ.
(2010) - et al.
Geographical distribution of metals in livers of polar bears from the Northwest Territories
Canada. Sci. Total Environ.
(1991) - et al.
Contaminant residues in seabird eggs from the Canadian Arctic II. Spatial trends and evidence from stable isotopes for intercolony differences
Environ. Pollut.
(2002) - et al.
Persistent halogenated organic contaminants and mercury in northern fulmars (Fulmarus glacialis) from the Canadian Arctic
Environ. Pollut.
(2010) - et al.
Temporal trends of mercury in eggs of five sympatrically breeding seabird species in the Canadian Arctic
Environ. Pollut.
(2016) - et al.
Otolith elemental fingerprints as biological tracers of fish stocks
Fish. Res.
(2000) - et al.
Mercury and other trace elements in a pelagic arctic marine food web (Northwater Polynya, Baffin Bay)
Sci. Total Environ.
(2005) - et al.
Metal bioaccumulation by estuarine food webs in New England
USA. J. Marine Sci. Engineer.
(2016) - et al.
Mercury bioaccumulation and biomagnification in a small Arctic polynya ecosystem
Sci. Total Environ.
(2015) - et al.
Blood and feather concentrations of toxic elements in a Baltic and an Arctic seabird population
Marine Pollut. Bull.
(2017)
Trace elements in Antarctic fish species and the influence of foraging habitats and dietary habits on mercury levels
Sci. Total Environ.
Specific accumulation of mercury and selenium in seabirds
Environ. Pollut.
Inuit foods and diet: a preliminary assessment of benefits and risks
Sci. Total Environ.
Tracking contaminants in seabirds of Arctic Canada: temporal and spatial insights
Marine Pollut. Bull.
Increasing cadmium and zinc levels in wild common eiders breeding along Canada's remote northern coastline
Sci. Total Environ.
Elevated mercury levels in a wintering population of common eiders (Somateria mollissima) in the northeastern United States
Marine Pollut. Bull.
Spatial and temporal trends and effects of contaminants in the Canadian Arctic marine ecosystem: a review
Sci. Total Environ.
Levels and interactions of heavy metals in sea birds from Svalbard and the Antarctic
Environ. Pollut.
Trace elements in eggs of common eiders (Somateria mollissima) breeding in Nova Scotia, Canada
Marine Pollut. Bull.
Effect of diet, location and sampling year on bioaccumulation of mercury, selenium and cadmium in pelagic feeding seabirds in Svalbard
Chemosphere
Trace element concentrations and gastrointestinal parasites of Arctic terns breeding in the Canadian high Arctic
Sci. Total Environ.
Implications of mercury and lead concentrations on breeding physiology and phenology in an Arctic breeding sea duck
Environ. Pollut.
Levels and spatial and temporal trends of contaminants in Greenland biota: an updated review
Sci. Total Environ.
Temporal trends of Hg in Arctic biota, an update
Sci. Total Environ.
Overview and regional and temporal differences of heavy metals in arctic whales and ringed seals in the Canadian arctic
Sci. Total Environ.
Immune function, stress response and body condition in arctic-breeding common eiders in relation to cadmium, mercury and selenium concentrations
Environ. Res.
Concentrations of cadmium, mercury, and selenium in common eider ducks in the eastern Canadian arctic: influence of reproductive stage
Sci. Total Environ.
Environmental contaminants in biota
Sources, Occurrence, Trends and Pathways in the Physical Environment — Canadian Arctic Contaminants Assessment Report II
Incubation constancy and mass loss in the common eider Somateria mollissima
Ibis
Regional and species specific bioaccumulation of major and trace elements in Arctic seabirds
Environ. Toxicol. Chem.
Trace element and metallothionein concentrations in seabirds from the Canadian Arctic
Environ. Toxicol. Chem.
One problem, many solutions: simple statistical approaches help unravel the complexity of the immune system in an ecological context
PLoS One
Comparison of arsenic, cadmium, chromium, lead, manganese, mercury and selenium in feathers in bald eagle (Haliaeetus leucocephalus), and comparison with common eider (Somateria mollissima), glaucous-winged gull (Larus glaucescens), pigeon guillemot (Cepphus columba), and tufted puffin (Fratercula cirrhata) from the Aleutian Chain of Alaska
Environ. Monit. Assess.
Evidence for biomagnification of rubidium in freshwater and marine food webs
Can. J. Fish. Aquat. Sci.
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