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The importance of open marine waters to the enrichment of total mercury and monomethylmercury in lichens in the Canadian High Arctic Kyra St. Pierre, Vincent L. St.Louis, Jane Kirk, Igor Lehnherr, Sunny Wang, and Catherine La Farge Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.5b00347 • Publication Date (Web): 16 Apr 2015 Downloaded from http://pubs.acs.org on April 19, 2015
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Environmental Science & Technology is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.
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The importance of open marine waters to the enrichment of total
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mercury and monomethylmercury in lichens in the Canadian High
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Arctic
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St. Pierre, K.A.1, *; St.Louis, V.L.1; Kirk, J.L.2; Lehnherr, I.3; Wang, S.1; La Farge, C.1
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Canada 2
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Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9,
Aquatic Ecosystem Protection Research Division, Environment Canada, Burlington, Ontario L7R 4A6, Canada
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Department of Geography, University of Toronto Mississauga, Mississauga, Ontario L5L 1C6, Canada
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* Corresponding author: Phone: 1-780-492-0900; fax: 1-780-492-9234; e-mail:
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[email protected] 18 19 20 21 22 23 24
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ABSTRACT
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Caribou, which rely on lichens as forage, are the most important dietary source of
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neurotoxic monomethylmercury (MMHg) to many of Canada’s Arctic Aboriginal people.
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However, little is understood about the sources of MMHg to lichens in the High Arctic.
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We quantified MMHg, total mercury (THg) and other chemical parameters (e.g., marine
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and crustal elements, δ13C, δ15N, organic carbon, calcium carbonate) in lichen and soil
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samples collected along transects extending from the coast on Bathurst and Devon
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islands, Nunavut, to determine factors driving lichen MMHg and THg concentrations in
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the High Arctic. Lichen MMHg and THg concentrations ranged from 1.41 to 17.1 ng g-1,
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and from 36.0 to 361 ng g-1, respectively. Both were highly enriched over concentrations
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in underlying soils, indicating a predominately atmospheric source of Hg in lichens.
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However, MMHg and THg enrichment at coastal sites on Bathurst Island was far greater
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than on Devon Island. We suggest that this variability can be explained by the proximity
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of the Bathurst transect to several polynyas, which promote enhanced Hg deposition to
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adjacent landscapes through various biogeochemical processes. This study is the first to
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clearly show a strong marine influence on MMHg inputs to coastal terrestrial food webs
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with implications for MMHg accumulation in caribou and the health of the people who
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depend on them as part of a traditional diet.
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INTRODUCTION
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In the Canadian High Arctic, Aboriginal peoples rely heavily on high trophic level
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organisms such as marine mammals, Arctic char (Salvelinus alpinus) and caribou
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(Rangifer tarandus) as part of their traditional country diet 1. While hunting and eating
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these foods provide many social and nutritional benefits 2, they are also sources of certain
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pollutants that undergo long-range transport to the Arctic, and then bioaccumulate in
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organisms and biomagnify through food chains 3. One of these pollutants is the
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neurotoxin monomethylmercury (MMHg). Though lower in MMHg concentrations than
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marine mammals, caribou represent the most important dietary source of MMHg to most
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Canadian Arctic Aboriginal people with the exception of the Baffin Inuit, based on
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estimates of the frequency with which caribou is consumed 4. Lichens are the most
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important forage for Arctic caribou in winter, when they can make up 77% of the caribou
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diet 5, 6.
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Lichens are unique terrestrial organisms that form a symbiotic relationship
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between fungi, algae and/or cyanobacteria 7. Lichens grow on diverse substrates and are
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often the dominant autotroph in polar ecosystems. They are typically slow growing and
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lack cuticle or stomata, which permit direct nutrient and pollutant ad- or absorption to the
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lichen thalli 8, 9. Unfortunately, lichens have the highest MMHg and total Hg (THg; all
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forms of Hg in a sample) concentrations of all caribou forage types 5. Potential sources of
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inorganic Hg to lichens include wet 9 deposition, dry deposition of aerosols and larger
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particulate matter 10, and direct gaseous elemental Hg (Hg0 ) uptake 11. Though never
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investigated, possible sources of MMHg to lichens include wet deposition and dry
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deposition of aerosols and larger particulate matter, but also methylation of inorganic Hg
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to MMHg on or within lichen, as well as adsorption of MMHg from soils. Another
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potential source of MMHg to lichens in coastal terrestrial environments is the
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atmospheric deposition of MMHg originating from the photodemethylation of DMHg 12.
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DMHg is often the dominant form of organic Hg in seawater 13, but is extremely volatile
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and readily evades to the atmosphere where it can be rapidly photodegraded to MMHg
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then deposited to nearby landscapes 14, 15. In Alaska, Norway and Hudson Bay 16-18,
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higher concentrations of total Hg (THg) in coastal lichens were attributed to higher
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gaseous oxidized Hg (GOM) and particulate bound Hg (PBM) deposition during
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springtime atmospheric Hg depletion events (AMDEs) 18. However, trends in MMHg
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were not examined in these studies.
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To assess the role of marine waters as the source of MMHg to terrestrial
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ecosystems, we collected lichens along transects starting at the coast and moving inland
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on Bathurst and Devon islands in the Canadian High Arctic, Nunavut. The eastern coast
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of Bathurst Island is located in proximity to several polynyas (Figure 1), unlike the
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western coast of Devon Island. It was hypothesized that concentrations of MMHg and
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THg would be highest in lichens on Bathurst Island near the coast due to the presence of
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polynyas and the unique biogeochemical processes associated with these perennially
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open water areas. Lichens and their underlying soils were analyzed for concentrations of
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lithogenic metals and elements associated with marine sources (Na, K, Ca, Sr) to
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determine the role of oceans, soils and the atmosphere in lichen Hg burdens. Stable
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carbon (δ13C) and nitrogen (δ15N) isotope ratios in lichens were also quantified to assess
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whether lichen physiology influenced Hg accumulation. This study is the first to show the
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transfer of marine-derived MMHg to coastal terrestrial Arctic food webs, with
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implications for biomagnification into higher trophic levels.
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MATERIALS AND METHODS
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Sample Collection and Preparation. Lichen and soil samples were collected in July
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2007 along transects extending from the ocean-inland on Bathurst (5 sites) and Devon (4
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sites) islands, Nunavut, Canada (Figure 1, Table S1). Both islands are sparsely vegetated
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over the majority of their landmasses 19 and home to populations of endangered Peary
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caribou (R. tarandus pearyi). Soils along both transects were turbic cryosols with
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sporadic organic zones overlying continuous permafrost 20. The location of our transects
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on these two islands were selected as a natural control-impact experiment to determine
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whether the influence of marine waters had an impact on terrestrial MMHg accumulation.
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The start of the transect on the eastern coast Bathurst Island was located in proximity to
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several open-water polynyas, whereas there were no open water regions near our transect
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on the western coast of Devon Island (Figure 1). Polynyas provide perennial access to
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open water areas and are one of the few areas for constant ocean-atmosphere exchange in
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a region otherwise locked in by sea ice for the majority of the year.
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Three bulk lichen samples were collected at each site from soil surfaces. The top
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2-5 cm of soil underlying lichens were then sampled using a stainless steel soil corer. At
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one site where lichens on soil were not abundant, lichens were also collected from the
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surface of a rock. All samples were collected using “clean hands-dirty hands” sampling
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protocol for trace metals (EPA Method 1669) and stored in sterile polyethylene Whirl-
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Paks®. Samples were frozen within hours of collection and subsequently stored at -20°C
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until processing and analysis.
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Because dust particles can be important components of overall contaminant loads
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10, 21, 22
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samples were not washed prior to analyses. Lichens were identified and separated by
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species. In total, 9 species representing 3 families were identified, including one unknown
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species (Table S2). Thamnolia vermicularis was found at all sites on both islands, while
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Flavocetraria cucullata and Vulpiceda tilesii were found at all sites on Bathurst Island.
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and are unlikely to be selectively removed by caribou during foraging, lichen
Lichen and soil samples were freeze-dried and homogenized with either an acid-
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washed glass mortar and pestle (lichens) or a stainless steel coffee grinder (soils).
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Samples were then sub-sampled for the analyses described below. However, due to
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insufficient mass, not all analyses could be performed on all lichen samples. As a result,
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analyses were prioritized as follows: Hg (MMHg then THg), δ13C and δ15N, and
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lithogenic and marine elements. Soils were also analyzed for % organic carbon (OC) and
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% calcium carbonate (CaCO3) content.
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Mercury Analyses. MMHg was first extracted from lichen and soils using distillation.
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MMHg concentrations were then determined using isotope-dilution gas chromatography
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inductively-coupled plasma mass spectrometry 23 (ID-GC-ICP/MS; Tekran 2700
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Methylmercury Analyzer coupled with a Perkin Elmer Elan DRC-e ICP-Mass
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Spectrometer) at the accredited and internationally intercalibrated University of Alberta
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Biogeochemical Analytical Service Laboratory (BASL). MM201Hg was added to samples
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as a species-specific internal standard prior to the distillation to correct for procedural
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recoveries. Standard reference material (SRM) IAEA-405 (estuarine sediment,
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International Atomic Energy Agency) was used to assess method accuracy.
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All samples were analyzed for THg concentrations using thermal decomposition,
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pre-concentration and atomic absorbance spectrophotometry (Milestone DMA-80 direct
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Hg analyzer) at the Canada Centre for Inland Waters (CCIW; Burlington, ON, Canada).
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SRMs TORT-2 (lobster hepatopancreas, National Research Council (NRC)), MESS-3
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(marine sediment, NRC), SRM-2976 (mussel, National Institute of Standards and
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Technology (NIST)) and SRM1556b (oyster, NIST) were used as quality controls.
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Additional quality control and protocol details are described in the Supplementary
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Information.
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δ 13C and δ 15N: Both lichens and soils were analyzed for δ13C and δ15N at the BASL
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using a EuroVector EuroEA3028-HT elemental analyzer coupled to a GV Instruments
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IsoPrime continuous-flow isotope ratio mass spectrometer. 1.2 mg and 6-7 mg of lichen
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sample were used to quantify δ13C and δ15N, respectively. 2.5 mg or 25 mg of soils were
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analyzed depending on whether they were organic or mineral. δ13C and δ15N ratios were
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calculated according to equation 1, where R is the ratio of 13C/12C or 15N/14N, and X is the
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stable isotope signature of C or N. Rsample is measured relative to Rstandard of Pee Dee
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Belemnite for C and ambient air for N:
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X (‰) =
!!"#$%& !!"#$%#&%
− 1 × 1000
(1)
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SRM NIST 8415 (whole egg powder) was used for quality assurance and control, with
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standard deviations of 0.1 and 0.2% for δ13C and δ15N, respectively.
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Lithogenic and marine elemental analyses. Following HF-HNO3 digestion (see
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Supplementary Information), lichen and soil samples were analyzed for concentrations of
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46 elements by ICP/MS at the Canadian Centre for Isotopic Microanalysis (University of
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Alberta), and for concentrations of Ca, Mg, Fe, Na, and Al by inductively coupled plasma
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optical emission spectroscopy (ICP/OES) at the BASL.
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Soil %OC and %CaCO3 content: 100 mg of lichen or 200 mg of soil were heated in a
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muffle furnace at 550°C for 4 h to determine %OC content, then subsequently at 950°C
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for 2 h to determine %CaCO3 24.
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Data Analysis. All statistical analyses were completed in R 25. Principal component
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analyses (PCA) were performed on soil and lichen lithogenic and marine element
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concentrations to elucidate possible factors driving soil composition at a given sub-site
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(e.g., marine aerosols versus local geology). Soil PC scores were then used in a
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subsequent multiple regression analysis as measures of soil elemental composition.
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Separate multiple linear regression analyses were completed to assess the
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importance of each factor (PC scores, δ13C, δ15N, %OC and %CaCO3) in determining
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soil MMHg and THg concentrations and the percentage of THg as MMHg (%MMHg).
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Models were compared and the most parsimonious model was selected using Akaike
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Information Criteria (AIC). In cases where assumptions of linearity, normality,
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homoscedasticity and/or auto-correlation were violated, regression coefficients were
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obtained by bootstrap analysis.
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RESULTS AND DISCUSSION
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Soil composition. Like other Arctic locales 26, 27, the soils on both Bathurst and Devon
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islands were generally low in %OC content (median: 6.20%; range: 0.84% to 59.8%).
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%CaCO3 ranged between 0.45% and 36.4% (median: 12.1%). %OC and %CaCO3 were
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significantly higher in soils collected on Devon Island (medians 13.8% and 23.3%) than
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in those collected on Bathurst Island (medians 4.70% and 8.71%) (%OC: t =-3.59, p