Article pubs.acs.org/est
Changes in Food Web Structure Alter Trends of Mercury Uptake at Two Seabird Colonies in the Canadian Arctic Birgit M. Braune,*,† Anthony J. Gaston,†,⊥ Keith A. Hobson,‡ H. Grant Gilchrist,† and Mark L. Mallory§ †
Environment Canada, National Wildlife Research Centre, Carleton University, Raven Road, Ottawa, Ontario Canada K1A 0H3 Environment Canada, National Hydrology Research Centre, 11 Innovation Boulevard, Saskatoon, Saskatchewan Canada S7N 3H5 § Biology Department, Acadia University, Wolfville, Nova Scotia Canada B4P 2R6 ‡
S Supporting Information *
ABSTRACT: Arctic ecosystems are changing in response to climate change and some Arctic food web structures are being affected in ways which may have potential consequences for the biomagnification of environmental contaminants. Here, we examined how a shift in diet of an Arctic seabird resulted in a change of trophic position and how that change affected exposure to mercury over time. The thick-billed murre (Uria lomvia), which breeds in the eastern Canadian Arctic, has been monitored for diet and environmental contaminants at two colonies, one in northern Hudson Bay and one in the high Arctic. As a result of a change in diet, murres breeding in Hudson Bay lowered their trophic position which, in turn, should affect their mercury exposure over time. After adjusting mercury concentrations in murre eggs for trophic position, the temporal trend of mercury in Hudson Bay murre eggs changed from nonsignificant to a significantly increasing trend. Valid trends can be deduced only when factors, such as diet, have been taken into account.
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INTRODUCTION Mercury (Hg) is a naturally occurring element but an increase in global anthropogenic emissions has enhanced the amount of Hg cycling through the environment in recent decades.1 Due to its highly volatile nature, elemental Hg partitions readily into air where it can undergo long-range atmospheric transport to remote regions such as the Arctic. There is already some evidence that climate change is affecting the biogeochemical cycles of many environmental contaminants entering the Arctic including Hg.2,3 The Arctic region is currently undergoing a dramatic change in climate with a 2-fold increase in average annual temperature since 1980 compared with the rest of the world.4 As a result of increasing surface temperatures, the average extent of sea ice cover in the Arctic in summer has declined by 15−20% over the past 30 years.4 However, these changes are not uniform. In the Canadian Arctic, there has been no trend in summer ice cover reported in Lancaster Sound in the high Arctic,5 whereas warming ocean conditions and longer ice-free periods have been documented for Hudson Bay.6,7 There is also strong evidence that the food web structure in the Hudson Bay ecosystem is changing.8 Complex shifts in species distributions, consumer diets, and the timing of ice breakup and freeze-up have potential consequences for the biomagnification of environmental contaminants. Historically, Arctic cod (Boreogadus saida), a cold-water fish associated with ice cover, dominated the diet of thick-billed murres (Uria lomvia) breeding in the Canadian high Arctic9 © 2014 American Chemical Society
and, until the mid-1990s, was the most common prey item found in the diet of nestling murres throughout the Canadian Arctic.10,11 However, during the 1990s, as a result of changing ice conditions, there was a shift in the diet of thick-billed murres breeding in northern Hudson Bay from Arctic cod to primarily capelin (Mallotus villosus).12−14 Capelin brought back to the colony by thick-billed murres in northern Hudson Bay have been shown to occupy a lower trophic position and have lower Hg concentrations than Arctic cod.15 Given that Hg biomagnifies through the food chain,16−18 variation in diet over trophic levels through time may change the exposure of these murre populations to Hg. Other studies have shown how changes in diet have changed patterns of contaminant exposure in biota.19−29 In particular, dietary changes associated with a longer ice-free season in Hudson Bay have altered the dietary exposure of beluga (Delphinapterus leucas) to Hg28 and polar bears (Ursus maritimus) to halogenated contaminants.29 However, few studies have attempted to adjust contaminant temporal trends to account for these dietary changes. Eggs of thick-billed murres have been monitored for environmental contaminants at Prince Leopold Island in the Canadian high Arctic since 197530 and at Coats Island in Received: Revised: Accepted: Published: 13246
July 25, 2014 October 22, 2014 October 24, 2014 November 4, 2014 dx.doi.org/10.1021/es5036249 | Environ. Sci. Technol. 2014, 48, 13246−13252
Environmental Science & Technology
Article
Figure 1. Thick-billed murre colonies sampled at Coats Island in northern Hudson Bay and Prince Leopold Island in Lancaster Sound.
We assumed that a change in δ15N values in the eggs reflected a change in diet of the murres in their respective breeding areas rather than a baseline change in the isotopic composition of primary production. Previous studies in Lancaster Sound have provided evidence for little baseline change in δ15N over the last three decades.38 Trends in Hg concentrations were compared with an indicator of past diet of the laying female (δ15N in egg homogenates), and for Coats Island, δ15N values in eggs were compared with annual diet indices (proportions of different prey species delivered to offspring). Annual indices of diet were not available for Prince Leopold Island. Given the difference in trophic positions and Hg concentrations in Arctic cod and capelin, we expected a reduction in the exposure of Coats Island murres to Hg due to their switch in diet which occurred in the mid-1990s.
northern Hudson Bay since 1993.31 Contaminant trends may be influenced by differences in exposure at breeding and overwintering areas. Thick-billed murres breeding at Coats Island spend seven months of the year in northern Hudson Bay, whereas those breeding at Prince Leopold Island spend only half that time in the high Arctic.32 Murres from both colonies, however, overlap on their wintering grounds in the southern Davis Strait−Labrador Sea area.32,33 Therefore, it is assumed that any differences in contaminant exposure of murres breeding at these two colonies are related to contaminant exposure at the breeding areas. Given the change in diet documented for thick-billed murres breeding at Coats Island, the objective of this paper was to determine if those changes in diet affected temporal trends of Hg measured in eggs of thick-billed murres. Determination of trophic position, as a reflection of dietary change, is possible through the measurement of naturally occurring stable isotopes of nitrogen (15N/14N, expressed as δ15N).34−36 This is also true of seabird eggs as stable isotope ratios in eggs are expected to reflect the diet of the female prior to or during egg-laying.34,37
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MATERIALS AND METHODS Sample Collection and Preparation. Eggs of thick-billed murres were collected by hand from the Prince Leopold Island
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dx.doi.org/10.1021/es5036249 | Environ. Sci. Technol. 2014, 48, 13246−13252
Environmental Science & Technology
Article
assays were performed on 1 mg subsamples of homogenized material loaded into tin cups. The 1975−2011 samples were analyzed on a Europa 20:20 continuous-flow isotope ratio mass spectrometer (CFIRMS) interfaced with a Robo-Prep elemental analyzer. Within each analytical run, five unknowns were separated by two albumen laboratory standards. The 2012−2013 samples were analyzed using an isotope cube elemental analyzer (Elementar, Germany) interfaced with a Delta Advantage continuous-flow isotope ratio mass spectrometer (Thermo, Germany) coupled with a ConFlo III (Thermo, Germany). A glutamic acid laboratory standard was included for every 10 unknown samples. Quality control was maintained by running sample duplicates. All measurements are reported in standard δ-notation in parts per thousand (‰) relative to the AIR international standard. Replicate measurements of internal laboratory standards [1975−2011 samples: albumen, 2012− 2013 samples: C-55 (glutamic acid)] indicated measurement errors of ±0.3‰ and ±0.2‰, respectively. Interlaboratory comparisons of duplicate samples (n = 45) were consistent within measurement error; that is, mean values for δ15N between the two laboratories differed by 0.05). Data Treatment. Since the dietary information for thickbilled murres at the breeding colony was based on nestling diet, we needed to establish that the nestling diet was representative of the diet of the prelaying female. Therefore, δ15N values for Coats Island eggs were compared with indices of nestling diet obtained from observations of individual fish delivered to chicks at the colony in late July through early August of the same year as described elsewhere.12,13 We modeled egg δ15N values in relation to year and the proportions of the two dominant prey items in the nestling diet, Arctic cod and capelin,13 using the forward stepwise multiple regression module of Statistica 7.0, with model suitability determined from comparison of AICc values (Akaike Information Criterion for small samples) following the recommendations of Burnham and Anderson42 and Anderson.43 Models containing more variables than the top ranked model were not considered. The diet variables, being proportions, were arcsin-transformed for analysis. As eggs collected from 2006 to 2013 were individually analyzed for Hg and δ15N, those data were averaged for groups of three eggs per colony per year to facilitate statistical comparison with results for the three-egg pooled (composite) samples analyzed prior to 2006. In order to examine temporal trends of Hg without the potentially confounding effect of dietary change, the Hg concentration data were adjusted to account for departures in δ15N from the mean value for each colony over all years [(δ15N)average − (δ15N)measured] according to the following equation:
Migratory Bird Sanctuary (74°02′N, 90°05′W) in Lancaster Sound, Nunavut, Canada, from 1975 to 2013 (1975, 1976, 1977, 1987, 1988, 1993, 1998, 2003, annually 2005−2013), and from Coats Island (62°98′N, 82°00′W) in northern Hudson Bay from 1993 to 2013 (1993, 1998, 2003, annually 2005− 2011, 2013) (Figure 1) by Environment Canada. Eggs were kept cool in the field and shipped to the National Wildlife Research Centre (NWRC) for processing and chemical analyses. Egg contents were homogenized and stored frozen (−40 °C) in acid-rinsed polyethylene vials for Hg analysis. The validity of this storage method has been previously discussed.30 Archived samples collected prior to 1993 were retrieved from the National Wildlife Specimen Bank at NWRC and analyzed retrospectively, whereas samples collected from 1993 to 2013 were analyzed within six months of collection. Egg homogenates from 1975 to 2005 were analyzed for total Hg and for δ15N as pooled (composite) samples with each pool consisting of three individual egg samples (n = 9 eggs per colony per year from 1975 to 1988 analyzed as three pools of three eggs each; n = 15 eggs per colony per year from 1993 to 2005 analyzed as five pools of three eggs each). Eggs from 2006 to 2013 (n = 15 eggs per colony per year) were individually analyzed. Mercury Analysis. Mercury analyses were carried out at NWRC, Ottawa, Ontario. Samples collected during 1975 to 1998 were thawed, freeze-dried and digested in mineral acids prior to analysis. Those samples were then analyzed for total Hg using cold vapor atomic absorption spectrophotometry (CVAAS) with the 3030b-AAS (PerkinElmer) equipped with VGA (Varian) vapor generation system and PSC-55 (Varian) autosampler as described elsewhere.39 Samples collected during 2003−2013 were homogenized, freeze-dried, homogenized again and weighed into nickel combustion boats. Total Hg was analyzed using an Advanced Mercury Analyzer (AMA-254) equipped with an ASS-254 autosampler for solid samples as described elsewhere.40,41 The method employs direct combustion of the sample in an oxygen-rich atmosphere. Analytical accuracy for total Hg was determined by analyzing one or two blank samples with each sample set, as well as analysis of two standard reference materials (DOLT-2 and DORM-2 obtained from the Canadian National Research Council (CNRC)) for the 1975−1998 samples, and three standard reference materials (DOLT-2 and TORT-2 from CNRC and Oyster Tissue 1566b from the National Institute of Standards and Technology (NIST)) for the 2003−2013 samples. Recoveries of reference materials were within the certified range of values for both methodologies. Total Hg concentrations for sample duplicates (n = 24) using the two methodologies were also not significantly different (p > 0.05). Analytical precision was checked by analyzing replicate samples, averaging one replicate sample for every seven samples analyzed. Standard deviation for replicate readings was
