Sea Ice-Associated Diet Change Increases the Levels of Chlorinated
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Environ. Sci. Technol. 2009, 43, 4334–4339 benthic-dominated Northern Bering Sea ecosystem to a more Sea Ice-associated Diet Change pelagic, Southern Bering Sea-type (subarctic) ecosystem (6). Increases the Levels of Chlorinated Environmental contamination by persistent organic pol- lutants (POPs) is also a major concern for northern ecosys- and Brominated Contaminants in tems, despite substantial distances from source regions further south (7, 8). Contamination of subarctic and arctic Polar Bears regions by POPs occurs mainly through long-range transport from lower latitudes (9). Polychlorinated biphenyls (PCB) as MELISSA A. MCKINNEY,* well as organochlorine pesticides (OCP) including dichlo- ELIZABETH PEACOCK, AND rodiphenyltrichloroethane (DDT), hexachlorocyclohexane ROBERT J. LETCHER* (HCH), and chlordane (CHL) have long been observed as contaminants in northern biota (10, 11). Lesser known, more Wildlife Toxicology and Disease Program, Science and Technology Branch, Environment Canada, Ottawa, Ontario recently monitored chemicals such as polybrominated K1A 0H3, Canada, Department of Chemistry, Carleton diphenyl ether (PBDE) flame retardants and perfluorinated University, Ottawa, Ontario K1S 5B6, Canada, and contaminants (PFCs) are now also a concern in the Arctic Department of Environment, Government of Nunavut, (12, 13). As upper trophic level consumers, polar bears, as Igloolik, Nunavut X0A 0L0 Canada well as humans consuming a local diet, accumulate high tissue concentrations of, e.g., PCB and CHL contaminants, - Received February 13, 2009. Revised manuscript received which have been related to biological effects (14 16). For April 17, 2009. Accepted April 22, 2009. instance, endocrine, immune, and reproductive biomarkers have been correlated with tissue levels of PCBs and certain OCPs in polar bears (15, 16 and references therein). Polar bears from the western Hudson Bay (WHB) sub- Two global environmental issues, climate change and population exist near the southern limit of the range of this contamination by persistent organic pollutants, represent species (Figure 1), and appear to be more impacted by recent major concerns for arctic ecosystems. Yet, it is unclear how climate warming than their more northerly located conspe- cifics (17). Hudson Bay polar bears (as well as those from the these two stressors interact in the Arctic. For instance, the European Arctic) also have generally elevated adipose influence of climate-associated changes in food web structure concentrations of organohalogen contaminants relative to on exposure to pollutants within arctic ecosystems is presently other circumpolar populations (18). For this subpopulation, unknown. Here, we report on recent changes in feeding movement, mating and feeding depends in part on the timing ecology (1991-2007) in polar bears (Ursus maritimus) from and conditions of seasonal sea ice in the bay (19). In this the western Hudson Bay subpopulation that have resulted in region, the mean annual air temperature is on average about increases in the tissue concentrations of several chlorinated and 1.5 °C warmer (as measured at Churchill, Manitoba, 58.3°N, brominated contaminants. Differences in timing of the annual 93.8°W) (20), and the summer sea ice breakup is around sea ice breakup explained a significant proportion of the diet three weeks earlier (20), than thirty years ago in the western variation among years. As expected from climate change part of the bay. Over the same period, there has been no significant trend in the timing of fall sea ice freeze-up in predictions, this diet change was consistent with an increase western Hudson Bay (20). There have been no significant in the consumed proportions of open water-associated seal trends in winter maximum land-fast ice thickness and timing species compared to ice-associated seal species in years of at Churchill from 1960 to 1987 (21). The increasingly earlier earlier sea ice breakup. Our results demonstrate that climate breakup of the summer sea ice has been linked to lower change is a modulating influence on contaminants in this polar body condition, birth, and survival rates in WHB bears over bear subpopulation and may pose an additional and previously the past two decades (19, 22). We hypothesized that this sea unidentified threat to northern ecosystems through altered exposures to contaminants. Introduction There is an established link between recent climate change and phenological, geographical, and compositional changes to ecosystems across many regions of the world (1, 2). The magnitude of warming is regionally variable, though, and is nearly twice the global average in the Arctic (3, 4). There are reports of recent and drastic climate-related shifts in the composition of arctic and subarctic marine ecosystems. In northern Hudson Bay, there has been an increase in subarctic fish relative to arctic fish (as measured by the diet of thick- billed murre (Uria lomvia)) with decreasing July ice cover from 1980 to 2002 (5). Reduced sea ice, along with warmer air and ocean temperatures, has shifted the previously * Address correspondence to either author. Phone: 613-998-6688 (M.A.M.); 613-998-6696 (R.J.L.). Fax: 613-998-0458 (M.A.M., R.J.L.); FIGURE 1. Map of study site. The western Hudson Bay polar bear E-mail: [email protected] (M.A.M.); robert.letcher@ subpopulation, indicated by the striped area, is bounded by ec.gc.ca (R.J.L.). 63.10°N, 88.30°W, and by the western Hudson Bay coastal region. 4334 9 ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 43, NO. 12, 2009 10.1021/es900471g CCC: $40.75 2009 American Chemical Society Published on Web 05/07/2009 ice change is also impacting WHB polar bear feeding ecology, (31). Thus, we used changes in polar bear FA patterns over as measured by stable isotope and fatty acid dietary tracers. time, in conjunction with this published prey FA data, to Since diet is the main route of exposure to contaminants, we infer alterations in the proportions of prey species consumed. also hypothesized that feeding changes would, in turn, impact Extraction and analysis of FAs from adipose tissue has been their tissue contaminant levels. described previously. In short, 10-20 mg of inner adipose tissue was used to avoid potentially oxidized outer tissue Experimental Methods (32). Lipids were extracted thrice using 2:1 CHCl3:MeOH (33) Study Site and Sample Details. We analyzed archived WHB containing 0.01% 2,6-di-t-butyl-4-methylphenol as antioxi- polar bear adipose tissues from seven available years over dant. 5-R-Cholestane was used as internal standard. The the 17 year period of 1991-2007: 1991 (n ) 14), 1992 (n ) extract was evaporated to dryness under N2, and lipid was 15), 1994 (n ) 15), 1995 (n ) 15), 2001 (n ) 9), 2003 (n ) 12), redissolved in toluene. FAs were methylated via the Hilditch and 2007 (n ) 12). Supporting Information (SI) Table S2 reagent (32). After addition of 2% KHCO3, the organic layer provides further sample details. The 1990s samples were was collected and fatty acid methyl esters (FAMEs) were adipose biopsies taken during polar bear tagging operations, completely collected by two further extractions with hexane. whereas the 2000s samples were mainly pieces of adipose FAMEs were analyzed by GC-FID equipped with a Supelco- tissue taken from bears harvested by Inuit hunters. It has 2560 bis-cyanopropyl column and quantified against a been shown that there are no differences POPs patterns and Supelco 37 component FAME external standard (25). Here, concentrations or fatty acid composition among major we report only on the “dietary” FAs (i.e., those that are adipose depots in polar bear (23, 24). All samples were initially incorporated relatively unchanged from prey to predator and during shipment kept frozen and stored at -40 °C over adipose tissues for a monogastric predator) (28, 32) that were the long term at Environment Canada’s Wildlife Specimen available for quantification based on the external standard. Bank. There appears to be no change in fatty acid concen- Each FAME was calculated as the % of total dietary FAME. trations and patterns between samples stored at -40 and Organohalogen Contaminant Analysis. We extracted -80 °C(25). To focus on the effect of diet on the contaminant brominated and chlorinated contaminants from polar bear concentrations over time, we selected and corrected (see adipose tissue as described previously (34) with modifications also the Data Analysis Section, SI Table S2) the data set to outlined here. We homogenized around 0.5 g of fat with minimize confounding factors that could contribute to sodium sulfate and spiked it with a mixture of 13C-PCBs, interindividual variation in contaminant levels. We selected 13C-p,p’-DDE and BDE30 internal standards. We then samples collected in fall/winter, which were at least 3 years extracted the contaminants with 1:1 DCM:hexane using an old and 80% of which were female to minimize seasonal, age accelerated solvent extractor at 100 °C and 1500 psi for one and gender related variability. cycle. A 10% portion of the extract was used for gravimetric Determination of Sea Ice Breakup Timing. We calculated determination of lipid content. From the remainder, lipids the timing of annual sea ice breakup with established and other bioorganics were removed by automated gel methods (19, 26). In brief, we determined the date when the permeation chromatography. The extract was further cleaned ice cover in WHB (Figure 1) was at 50% by interpolation of up on a preconditioned (6 mL of 10% MeOH in DCM, followed weekly sea ice data from the Canadian Ice Service (http:// by 8 mL of 5% DCM in hexane) silica (500 mg) solid phase ice-glaces.ec.gc.ca). extraction cartridge with 8 mL of 5% DCM in hexane (35). Diet Analysis. Traditional methods of studying feeding Analysis of PCBs and OCPs by GC-MS in electron impact behavior, such as observation of kills and analysis of gut ionization mode has been detailed elsewhere (36).