Importance of Open Marine Waters to the Enrichment of TotalMercury and Monomethylmercury in Lichens in the Canadian HighArcticK. A. St. Pierre,*,† V. L. St. Louis,† J. L. Kirk,‡ I. Lehnherr,§ S. Wang,† and C. La Farge†

†Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada‡Aquatic Ecosystem Protection Research Division, Environment Canada, Burlington, Ontario L7R 4A6, Canada§Department of Geography, University of Toronto Mississauga, Mississauga, Ontario L5L 1C6, Canada

*S Supporting Information

ABSTRACT: Caribou, which rely on lichens as forage, are a dietary source ofmonomethylmercury (MMHg) to many of Canada’s Arctic Aboriginal people.However, little is understood about the sources of MMHg to lichens in theHigh Arctic. We quantified MMHg, total mercury (THg) and other chemicalparameters (e.g., marine and crustal elements, δ13C, δ15N, organic carbon,calcium carbonate) in lichen and soil samples collected along transectsextending from the coast on Bathurst and Devon islands, Nunavut, todetermine factors driving lichen MMHg and THg concentrations in the HighArctic. Lichen MMHg and THg concentrations ranged from 1.41 to 17.1 ngg−1 and from 36.0 to 361 ng g−1, respectively. Both were highly enriched overconcentrations in underlying soils, indicating a predominately atmosphericsource of Hg in lichens. However, MMHg and THg enrichment at coastal siteson Bathurst Island was far greater than on Devon Island. We suggest that thisvariability can be explained by the proximity of the Bathurst Island transect toseveral polynyas, which promote enhanced Hg deposition to adjacent landscapes through various biogeochemical processes. Thisstudy is the first to clearly show a strong marine influence on MMHg inputs to coastal terrestrial food webs with implications forMMHg accumulation in caribou and the health of the people who depend on them as part of a traditional diet.

■ INTRODUCTION

In the Canadian High Arctic, Aboriginal peoples rely heavily onhigh trophic level organisms such as marine mammals, Arcticchar (Salvelinus alpinus) and caribou (Rangifer tarandus) as partof their traditional country diet.1 While hunting and eatingthese foods provide many social and nutritional benefits,2 theyare also sources of certain pollutants that undergo long-rangetransport to the Arctic, and then bioaccumulate in organismsand biomagnify through food chains.3 One of these pollutants isthe neurotoxin monomethylmercury (MMHg). Though lowerin MMHg concentrations than marine mammals, caribourepresent the most important dietary source of MMHg to mostCanadian Arctic Aboriginal people with the exception of theBaffin Inuit, based on estimates of the frequency with whichcaribou is consumed.4 Lichens are the most important foragefor Arctic caribou in winter, when they can make up 77% of thecaribou diet.5,6

Lichens are unique terrestrial organisms that form asymbiotic relationship between fungi, algae, and cyanobacteria.7

Lichens grow on diverse substrates and are often the dominantautotroph in polar ecosystems. They are typically slow growingand lack cuticle or stomata, which permit direct nutrient andpollutant ad- or absorption to the lichen thalli.8,9 Unfortunately,lichens have the highest MMHg and total Hg (THg; all forms

of Hg in a sample) concentrations of all caribou forage types.5

Potential sources of inorganic Hg to lichens include wet9

deposition, dry deposition of aerosols and larger particulatematter,10 and direct gaseous elemental Hg (Hg0) uptake.11

Though never investigated, possible sources of MMHg tolichens include wet deposition and dry deposition of aerosolsand larger particulate matter, but also methylation of inorganicHg to MMHg on or within lichen, as well as adsorption ofMMHg from soils. Another potential source of MMHg tolichens in coastal terrestrial environments is the atmosphericdeposition of MMHg originating from the photodemethylationof DMHg.12 DMHg is often the dominant form of organic Hgin seawater,13 but is extremely volatile and readily evades to theatmosphere where it can be rapidly photodegraded to MMHgthen deposited to nearby landscapes.14,15 In Alaska, Norway,and Hudson Bay,16−18 higher concentrations of total Hg (THg)in coastal lichens were attributed to higher gaseous oxidized Hg(GOM) and particulate bound Hg (PBM) deposition during

Received: January 20, 2015Revised: April 14, 2015Accepted: April 16, 2015Published: April 16, 2015

Article

pubs.acs.org/est

© 2015 American Chemical Society 5930 DOI: 10.1021/acs.est.5b00347Environ. Sci. Technol. 2015, 49, 5930−5938

springtime atmospheric Hg depletion events (AMDEs).18

However, trends in MMHg were not examined in these studies.To assess the role of marine waters as the source of MMHg

to terrestrial ecosystems, we collected lichens along transectsstarting at the coast and moving inland on Bathurst and Devonislands in the Canadian High Arctic, Nunavut. The easterncoast of Bathurst Island is located in proximity to severalpolynyas (Figure 1), unlike the western coast of Devon Island.It was hypothesized that concentrations of MMHg and THgwould be highest in lichens on Bathurst Island near the coastdue to the presence of polynyas and the unique biogeochemicalprocesses associated with these perennially open water areas.Lichens and their underlying soils were analyzed forconcentrations of lithogenic metals and elements associatedwith marine sources (Na, K, Ca, Sr) to determine the role ofoceans, soils and the atmosphere in lichen Hg burdens. Stablecarbon (δ13C) and nitrogen (δ15N) isotope ratios in lichenswere also quantified to assess whether lichen physiologyinfluenced Hg accumulation. This study is the first to show thetransfer of marine-derived MMHg to coastal terrestrial Arcticfood webs, with implications for biomagnification into highertrophic levels.

■ MATERIALS AND METHODS

Sample Collection and Preparation. Lichen and soilsamples were collected in July 2007 along transects extendingfrom the ocean-inland on Bathurst (5 sites) and Devon (4sites) islands, Nunavut, Canada (Figure 1, SupportingInformation Table S1). Both islands are sparsely vegetatedover the majority of their landmasses19 and home topopulations of endangered Peary caribou (Rangifer taranduspearyi). Soils along both transects were turbic cryosols withsporadic organic zones overlying continuous permafrost.20 Thelocation of our transects on these two islands were selected as anatural control-impact experiment to determine whether theinfluence of marine waters had an impact on terrestrial MMHgaccumulation. The start of the transect on the eastern coast ofBathurst Island was located in proximity to several open-waterpolynyas, whereas there were no open water regions near ourtransect on the western coast of Devon Island (Figure 1).Polynyas provide perennial access to open water areas and areone of the few areas for constant ocean-atmosphere exchange ina region otherwise locked in by sea ice for the majority of theyear.

Three bulk lichen samples were collected at each site fromsoil surfaces. The top 2−5 cm of soil underlying lichens werethen sampled using a stainless steel soil corer. At one site wherelichens on soil were not abundant, lichens were also collectedfrom the surface of a rock. All samples were collected using the“clean hands-dirty hands” sampling protocol for trace metals(EPA Method 1669) and stored in sterile polyethylene Whirl-Paks. Samples were frozen within hours of collection andsubsequently stored at −20 °C until processing and analysis.Because dust particles can be important components of

overall contaminant loads10,21,22 and are unlikely to beselectively removed by caribou during foraging, lichen sampleswere not washed prior to analyses. Lichens were identified andseparated by species. In total, 9 species representing 3 familieswere identified, including one unknown species (SupportingInformation Table S2). Thamnolia vermicularis was found at allsites on both islands, while Flavocetraria cucullata and Vulpicedatilesii were found at all sites on Bathurst Island.Lichen and soil samples were freeze-dried and homogenized

with either an acid-washed glass mortar and pestle (lichens) ora stainless steel coffee grinder (soils). Samples were thensubsampled for the analyses described below. However, due toinsufficient mass, not all analyses could be performed on alllichen samples. As a result, analyses were prioritized as follows:Hg (MMHg then THg), δ13C and δ15N, and lithogenic andmarine elements. Soils were also analyzed for % organic carbon(OC) and % calcium carbonate (CaCO3) content.

Mercury Analyses. MMHg was first extracted from lichensand soils using distillation. MMHg concentrations were thendetermined using isotope-dilution gas chromatography in-ductively coupled plasma mass spectrometry23 (ID-GC-ICP/MS; Tekran 2700 Methylmercury Analyzer coupled with aPerkinElmer Elan DRC-e ICP-Mass Spectrometer) at theaccredited and internationally intercalibrated University ofAlberta Biogeochemical Analytical Service Laboratory (BASL).MM201Hg was added to samples as a species-specific internalstandard prior to the distillation to correct for proceduralrecoveries. Standard reference material (SRM) IAEA-405(estuarine sediment, International Atomic Energy Agency)was used to assess method accuracy.All samples were analyzed for THg concentrations using

thermal decomposition, preconcentration, and atomic absorb-ance spectrophotometry (Milestone DMA-80 direct Hganalyzer) at the Canada Centre for Inland Waters (CCIW;

Figure 1. Location of sampling sites on Bathurst Island and Devon Island in the Canadian Arctic Archipelago. Approximate polynya locations inyellow, based on Hannah et al. (2009)45: KB, Karluk Brooman polynya; QC, Queen’s Channel and Penny Strait polynya; DUN, Dundas Islandpolynya; HG, Hell Gate-Cardigan Strait polynya. Site 1 of transects denoted by red circle (Bathurst Island) or square (Devon Island). SeeSupporting Information Table S1 for sampling site characteristics. Arctic Ocean Basemap (beta release, 2014) produced by Esri, GEBCO, NOAA,National Geographic, DeLorme, HERE, Geonames.org, and other contributors.

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Burlington, ON, Canada). SRMs TORT-2 (lobster hepatopan-creas, National Research Council (NRC)), MESS-3 (marinesediment, NRC), SRM-2976 (mussel, National Institute ofStandards and Technology (NIST)) and SRM1556b (oyster,NIST) were used as quality controls. Additional quality controland protocol details are described in the SupportingInformation.δ13C and δ15N. Both lichens and soils were analyzed for

δ13C and δ15N at the BASL using a EuroVector EuroEA3028-HT elemental analyzer coupled to a GV Instruments IsoPrimecontinuous-flow isotope ratio mass spectrometer. Lichensamples (1.2 and 6−7 mg) were used to quantify δ13C andδ15N, respectively. 2.5 or 25 mg of soils were analyzed,depending on whether they were organic or mineral. δ13C andδ15N ratios (X) were calculated according to eq 1, where R isthe ratio of 13C/12C or 15N/14N, and X is the stable isotopesignature of C or N. Rsample is measured relative to Rstandard ofPee Dee Belemnite for C and ambient air for N.

= − ×⎛⎝⎜

⎞⎠⎟X

R

R(‰) 1 1000sample

standard (1)

SRM NIST 8415 (whole egg powder) was used for qualityassurance and control, with standard deviations of 0.1% and0.2% for δ13C and δ15N, respectively.Lithogenic and Marine Elemental Analyses. Following

HF-HNO3 digestion (see Supporting Information), lichen andsoil samples were analyzed for concentrations of 46 elements byICP/MS at the Canadian Centre for Isotopic Microanalysis(University of Alberta), and for concentrations of Ca, Mg, Fe,Na, and Al by inductively coupled plasma optical emissionspectroscopy (ICP/OES) at the BASL.Soil %OC and %CaCO3 Content. 100 mg of lichen or 200

mg of soil were heated in a muffle furnace at 550 °C for 4 h todetermine %OC content, then subsequently at 950 °C for 2 hto determine %CaCO3.

24

Data Analysis. All statistical analyses were completed inR.25 Principal component analyses (PCA) were performed onsoil and lichen lithogenic and marine element concentrations toelucidate possible factors driving soil composition at a givensubsite (e.g., marine aerosols versus local geology). Soil PCscores were then used in a subsequent multiple regressionanalysis as measures of soil elemental composition.Separate multiple linear regression analyses were completed

to assess the importance of each factor (PC scores, δ13C, δ15N,%OC and %CaCO3) in determining soil MMHg and THgconcentrations and the percentage of THg as MMHg (%MMHg). Models were compared and the most parsimoniousmodel was selected using Akaike Information Criteria (AIC). Incases where assumptions of linearity, normality, homoscedas-ticity, or autocorrelation were violated, regression coefficientswere obtained by bootstrap analysis.

■ RESULTS AND DISCUSSIONSoil Composition. Like other Arctic locales,26,27 the soils

on both Bathurst and Devon islands were generally low in %OC content (median = 6.20%; range = 0.84−59.8%). %CaCO3ranged between 0.45% and 36.4% (median: 12.1%). %OC and%CaCO3 were significantly higher in soils collected on DevonIsland (medians 13.8% and 23.3%) than in those collected onBathurst Island (medians 4.70% and 8.71%) (%OC t = −3.59, p≪ 0.01; %CaCO3, t = −7.86, p ≪ 0.01; SupportingInformation Table S3). δ13C signatures in soils ranged between

−24.7‰ and −5.30‰ (median = −15.6‰) and werenegatively correlated with %OC (Pearson product-momentcorrelation, r = −0.244, p < 0.05). δ15N signatures rangedbetween −3.73‰ and 1.96‰ (median = 0.47‰). Overall,soils were highest in concentrations of Ca (0.14 ± 0.12 mgg−1), Mg (18.6 ± 25.6 mg g−1), and Fe (13.7 ± 6.20 mg g−1).Only Cd was below detection in soils and thus omitted fromfurther analyses. PCA results demonstrated that soil composi-tion differed between the two islands (Supporting InformationFigure S1), with concentrations of most heavy metals and therare earth elements higher on Bathurst Island and Na, K, Ca,Mn, Zn, and Sr concentrations higher on Devon Island. PC1and PC2 explained 56.9% and 16.2% of the variation in theelemental composition of soils, respectively (SupportingInformation Figure S1). Most of the elements contributedstrongly to PC1, except for Ba, Cr, and Zn, and the marineelements Ca, Mg, and Sr, suggesting that PC1 was a measure ofcrustal rather than marine influence (Supporting InformationTable S4). In fact, the crustal component (PC1) scores weresignificantly positively correlated with distance from the oceanon both Bathurst and Devon islands (Figure 2; R2 =0.64 and

0.74 on Bathurst and Devon islands, respectively). Theseresults suggest that soil elemental composition depends onproximity to the Arctic Ocean, such that lithogenic elementshave a greater influence on soil composition at sites furtherinland. The relationship between soil composition and distancefrom the ocean may reflect patterns of glacial retreat andsubsequent rebound, which have been shown to influencemodern-day geological composition.28 The strongly positivecrustal elements contributed negatively to PC2, which was alsopositively influenced by select rare earth elements, and Cr, Fe,Cu, and Zn.

Lichen Composition. Lichen %OC ranged between 32.9%and 99.8% (median = 83.4%), whereas %CaCO3 rangedbetween 0.04% and 36.7% (median = 5.1%). In tundraenvironments, lichen δ13C and δ15N signatures tend to reflectdifferences in nutrient uptake strategies.29,30 δ13C signatures canbe used to distinguish between carbon dioxide (CO2)acquisition strategies, in particular the presence or absence ofa CO2-concentrating mechanism (CCM).29 In the absence of aCCM, δ13C signatures in lichens tend closer to that of C3

Figure 2. First principal component scores (PC1) of soil elementalcomposition with distance from the ocean (km) on Bathurst andDevon islands, Nunavut.

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plants (−32 ± 1.6‰), whereas lichens with a CCM exhibithigher δ13C signatures (−26 to −16‰), indicative of higherphotosynthetic efficiency and lower photorespiration.29 Lichenδ13C signatures ranged between −30.8‰ and −20.8‰(median = −24.8‰; Supporting Information Table S5),demonstrating that lichens on Bathurst and Devon islandsutilize a range of CO2 acquisition strategies. Lichen δ15Nsignatures are indicative of nitrogen acquisition strategies andthus symbiont type (i.e., cyanobacterial or algal30). δ15N valuesclose to 0‰ indicate the ability to carry out nitrogen fixationand a cyanobacterial symbiont, whereas lower negative valuesare consistent with N acquisition through wet deposition. Onlyone sample of Peltigera rufescens had a cyanobacterial symbiont(δ15N = −0.88‰), and was thus the only lichen in ourcollection capable of directly fixing N2 from the atmosphere. Allother lichen samples had δ15N signatures ranging between−7.58‰ and −1.56‰ (median = −3.63‰; SupportingInformation Table S5), indicative of N acquisition throughwet deposition.31 The values observed in this study areconsistent with δ15N signatures in lichens from other Arcticlocales.32

Concentrations of elements were lower in lichens than soils,with a few exceptions (Ca, Sr, Ce) at some of our samplinglocations. Lichens were highest in concentrations of Ca (76.1 ±27.9 mg g−1), K (1.63 ± 0.47 mg g−1) and Fe (0.83 ± 0.97 mgg−1). Concentrations of Be, Cd, Nb, Sb, Eu, Tb, Ho, Tm, Lu,Hf, Ta, and Tl were consistently below detection in lichens, andthus were not included in further analyses.We calculated enrichment factors (EF) to assess the

importance of atmospheric sources of elements in lichensrelative to underlying soils using eq 233 and Al as the referenceelement.34

= xx

EF(element /reference element) in lichen

(element /reference element) in soil (2)

EFs < 1 indicated that there was no enrichment of a givenelement relative to underlying soils. EF between 1 and 10 aregenerally indicative of particulate deposition at local back-ground levels, while EF > 10 suggest significant atmosphericenrichment.35 There was little enrichment (EF < 1) of thecrustal elements Mn, Fe, Co, and Ni, and the rare earthelements in lichens relative to their underlying soils (Figure 3).Lichens were highly enriched (EF > 10) in K and Zn, alongwith the marine elements Na, Ca, and Sr.As with soils, PCAs were conducted on the lichen element

concentration matrices to assess possible factors drivingvariation in overall lichen composition. PC results demon-strated differences in lichen composition between the twoislands, which is likely a reflection of geological differencesbetween Bathurst and Devon islands. Separation of lichens inPC1 and PC2 space suggests that general lichen elementalcomposition may also be dependent on species rather than anyparticular spatial orientation on the islands. PC1 and PC2explained 58.2% and 11.4% of the variability, respectively(Figure 4). Elements with a predominantly crustal source,including the rare earth elements, Al, Cr, Fe, Mn, and Zr,loaded high on PC1 (crustal component). Elements with highEFs in the lichens, including the marine elements Ca, Mg, andSr, contributed strongly to PC2 (marine component). HighEFs indicate significant atmospheric sources of these elements,possibly from the marine environment, which is supported by a

decline in the EF of these elements with distance from theocean (Figure 5).

Mercury Concentrations in Soils and Lichens. MedianTHg concentrations were 2 orders of magnitude higher inlichens (66.8 ng g−1; range 36.0 to 361 ng g−1) than in the soilsunderlying them (0.18 ng g−1; range 0.98 to 86.4 ng g−1)(Table 1). Median MMHg concentrations were likewise 2orders of magnitude higher in lichens (4.27 ng g−1; range 1.41to 17.1 ng g−1) than in soils (0.09 ng g−1; range 0.01 to 4.35 ngg−1). As a result, median %MMHg was, on average, 12 timeshigher in lichens than in soils (median 6.8% and range 1.2% to13% in lichens; median 0.82% and range 0.10% to 9.4% insoils).Concentrations of THg in the lichens were within the same

order of magnitude as concentrations previously reported forArctic lichens (10−270 ng g−1; Supporting Information TableS6). MMHg concentrations in the lichens were also in the samerange as the only other concentrations reported for Arcticlichens (1.7 to 2.5 ng g−1), which were collected from theYukon Territory in northern Canada.5 There exist few peer-

Figure 3. Enrichment factors (EF) for THg, MMHg, and otherelements in lichens relative to aluminum in soils in order of increasingmean EF. Medians and 10th and 90th percentiles are shown.

Figure 4. Biplot of principal component (PC) scores of lichen non-Hgelemental composition. Samples are highlighted by sampling island(Bathurst Island, circles; Devon Island, squares) and species (color).

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reviewed estimates of THg or MMHg concentrations in non-wetland high Arctic soils with which to compare.36

Controls on THg and MMHg in Soils. To determine whichfactors controlled concentrations of THg and MMHg in soils,we conducted multiple regression analyses using soil PC1scores as a measure of crustal influence (see above), as well assoil %OC, %CaCO3, and δ15N. Soil δ13C signatures wereexcluded because of a high autocorrelation with %OC. SoilTHg concentrations were positively predicted by %OC, %CaCO3, and soil crustal element composition (PC1 scores) (R2

= 0.62, p ≪ 0.05; Supporting Information Table S7). Organicmatter in soils binds Hg,37−39 preventing re-emission to theatmosphere. Although little work has been done on Hg in HighArctic soils,40,41 the cement industry has shown that limestone(CaCO3) rock can contain significant quantities of Hg.42 Thepositive crustal component term in the THg model indicatedhigher THg concentrations in inland soils.Soil MMHg concentrations were best predicted by soil THg

concentrations and crustal element composition (PC1) (R2 =0.51, p ≪ 0.05). The low soil %MMHg (median 0.82%)suggests that very little inorganic Hg methylation is occurring inArctic soils. Alternatively, low %MMHg may reflect highdemethylation rates in soils, which would be unsurprising giventhe low OC content of the soils (Supporting Information TableS3); however additional experiments would need to beperformed to test this. Indeed, the fact that soil THgconcentrations are a strong predictor of soil MMHg suggests

that there is a common THg and MMHg source to soils, suchas geology and atmospheric deposition. Unlike for THg, thecrustal component (PC1) term was negative in the MMHgmodel, suggesting that there is a marine source of MMHg tocoastal soils, possibly from the demethylation of DMHg ormarine aerosol deposition (see detailed discussion below).

Sources of THg and MMHg in Arctic Lichens. EFs for THg(median = 155; range = 32−682) and MMHg (median = 1456;range = 54−21760) were far greater than for all other elementsanalyzed (Figure 3) indicating an important role of atmosphericdeposition as a source of both THg and MMHg to lichens.Unlike most other heavy metals, Hg can exist in a reducedgaseous elemental form (Hg0),43 which would presumably bemore available for uptake by lichens than particulate-boundcompounds. Trends in enrichment of THg and MMHg differedbetween the two islands. First, MMHg EFs were an order ofmagnitude higher on Bathurst Island (median EF = 3073) thanon Devon Island (median EF = 349) (t test on logged EFs F =15.7, p < 0.001). Second, EFs for THg and MMHg on DevonIsland were constant throughout the entire 24 km transect (t =0.65, p = 0.53, R2 = 0.05 for THg; t = 0.64, p = 0.54, R2 = 0.05for MMHg), whereas on Bathurst Island, EFs for THg andMMHg were exceptionally high within ∼10 km of the coast,but then decreased further inland to values similar to thoseobserved on Devon Island (Figure 5; t = −3.04, p = 1.4 × 10−2,R2 = 0.51 for THg; t = −1.52, p = 0.16, R2 = 0.20 for MMHg).These results indicate that there is spatial heterogeneity in the

Figure 5. Mean (±1 SE) THg and MMHg enrichment factors in lichens with distance from the coast (km) on Bathurst and Devon islands (also seeFigure 1). Arctic Ocean Basemap (beta release; 2014) produced by Esri, GEBCO, NOAA, National Geographic, DeLorme, HERE, Geonames.org,and other contributors.

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processes governing lichen THg and MMHg enrichment onBathurst Island, but not on Devon. In fact, these results lendsupport to the Global Regional Atmospheric Heavy Metals(GRAHM) deposition model, which predicted THg depositionto be higher on the eastern coast of Bathurst Island than onDevon Island.44

We propose that the factor underlying the observed coastalvariation between the two islands is proximity to large expansesof open marine waters throughout the year. The transect onDevon Island extended from the western coast, far from anyknown year-round open water areas, whereas the transect onBathurst Island was located adjacent to several polynyas (Figure1).45 In fact, the prevailing north/northwest winds46 in the areafavor the southeastward movement of sea ice away from theBathurst Island coast and the creation of open water areasthroughout most of the year. We hypothesize that polynyaopen water areas are sources of THg and MMHg to coastallichens by promoting the occurrence of AMDEs47 and acting ashotspots for the exchange of gaseous Hg species, such as Hg0

and DMHg, between the surface layer of the marine watercolumn and the atmosphere. In addition to the trends observedin THg and MMHg EFs, this hypothesis is also supported bythe higher enrichment of the marine elements (Na, Ca, Sr)observed in Bathurst Island lichens relative to those found onDevon Island (Figure 5).During AMDEs in the polar spring, Hg0 is oxidized through

photochemical reactions with halogens, which are stronglyassociated with open water areas in the Arctic Ocean.47 Becausethey have higher deposition velocities than Hg0, gaseousoxidized mercury (GOM) and particulate-bound mercury

(PBM) produced during AMDEs are rapidly deposited tonearby marine surfaces and landscapes. The short distance (<10km) over which we observed the elevated THg enrichment inlichens is indeed characteristic of AMDEs as the halogenchemistry underlying AMDEs48 are known only to affect coastalareas.49

Polynyas and open water leads are also important sites forthe evasion and subsequent rapid demethylation of DMHg,followed by deposition of MMHg to marine surfaces andnearby terrestrial environments.12 Recent measurements in theCanadian Arctic Archipelago, including sites near Bathurst andDevon islands, demonstrated the presence of both DMHg andMMHg in the atmosphere immediately overlying the seawatersurface (i.e., the marine boundary layer).50 The spatial patternin MMHg enrichment on Bathurst Island was very similar tothat of THg, with EFs highest at coastal sites and decreasingwithin 10 km, suggesting similar origins of atmospheric THgand MMHg to lichens.Interestingly, at sites more than 10 km from the coast, EFs

for both THg and MMHg are similar on Devon and Bathurstislands, suggesting a background level of atmospheric enrich-ment of Hg common to both islands (Figure 5). In addition tothese background levels of enrichment possibly reflecting a“general” marine source of THg and MMHg to islands in theCanadian Arctic Archipelago, there are three other possibleatmospheric sources of THg and/or MMHg to lichens, all ofwhich originate from long-range transport from distant sources:(1) direct uptake of Hg0, (2) wet deposition of oxidized Hgspecies, and (3) dusts.

Table 1. Lichen and Soil THg and MMHg Concentrations and %MMHg by Locationa

lichen soil

island site subsite n sp.b nc THg (ng g−1) nd MMHg (ng g−1) MMHg (%) THg (ng g−1) MMHg (ng g−1) MMHg (%)

Bathurst B1 A 3 0 3 3.25 ± 1.30 5.09 ± 3.00 0.04 ± 0.01 0.91 ± 0.49B 2 1 52.6 2 4.12 ± 0.28 7.46 6.65 ± 1.51 0.06 ± 0.03 0.93 ± 0.25C 3 1 56.2 3 3.85 ± 2.11 8.76 4.53 ± 0.40 0.06 ± 0.02 1.27 ± 0.69

B2 A 3 1 67.9 3 4.93 ± 1.35 9.56 14.5 ± 7.89 0.13 ± 0.60 0.91 ± 0.05B 3 1 56.3 3 3.28 ± 1.00 7.87 16.7 ± 3.91 0.10 ± 0.03 0.61 ± 0.29C 4 1 186 3 13.6 ± 2.99 6.54 Epilithic lichens (no substrate sample)

B3 A 2 1 36.1 2 3.43 ± 1.32 6.94 1.64 ± 0.95 0.02 ± 0.01 1.22 ± 0.35B 3 2 90.7 ± 33.8 3 4.73 ± 1.65 6.69 ± 2.30 3.05 ± 1.18 0.02 ± 0.01 0.73 ± 0.63C 4 2 88.5 ± 48.4 4 5.93 ± 1.65 8.63 ± 7.23 6.59 ± 5.31 0.02 ± 0.01 0.42 ± 0.32

B4 A 3 1 42.3 3 4.51 ± 2.31 5.55 7.80 ± 1.21 0.05 ± 0.03 0.56 ± 0.48B 3 1 50.0 2 3.66 ± 0.39 7.88 6.46 ± 0.41 0.04 ± 0.01 0.59 ± 0.11C 3 2 66.0 ± 28.9 2 5.13 ± 1.01 8.23 ± 2.06 8.78 ± 3.32 0.07 ± 0.03 0.76 ± 0.25

B5 A 4 2 56.6 ± 16.7 4 2.99 ± 0.97 5.91 ± 0.09 33.2 ± 0.72 0.19 ± 0.03 0.58 ± 0.09B 3 2 71.3 ± 27.9 3 3.79 ± 1.00 5.67 ± 0.35 28.7 ± 3.49 0.16 ± 0.03 0.55 ± 0.04C 3 2 66.7 ± 28.0 3 3.72 ± 1.10 5.06 ± 0.24 38.7 ± 2.11 0.22 ± 0.08 0.56 ± 0.12

Devon D1 A 1 1 66.3 1 3.95 5.97 11.3 ± 2.84 0.77 ± 0.47 6.35 ± 2.69B 1 1 44.7 1 4.96 11.1 28.7 ± 19.8 0.53 ± 0.40 1.52 ± 0.66C 1 1 69.7 1 3.56 5.10 76.5 ± 14.0 1.67 ± 0.90 1.94 ± 1.88

D2 A 3 3 170 ± 166 3 5.09 ± 1.49 5.43 ± 4.85 38.2 ± 21.8 2.11 ± 1.41 4.83 ± 2.89B 4 4 169 ± 124 5 4.95 ± 1.62 4.10 ± 3.66 53.6 ± 21.3 2.11 ± 1.81 1.92 ± 0.32

D3 A 1 1 54.3 1 6.65 12.3 11.5 ± 3.31 0.11 ± 0.06 1.05 ± 0.34B 1 1 45.4 1 4.36 9.61 9.96 ± 2.11 0.08 ± 0.05 0.76 ± 0.39

D4 A 3 1 43.0 3 4.84 ± 3.06 8.39 49.0 ± 30.4 0.65 ± 0.24 1.49 ± 0.38B 3 3 69.8 ± 24.9 3 4.45 ± 1.34 6.81 ± 2.24 16.5 ± 12.1 0.37 ± 0.48 1.55 ± 1.51C 3 1 73.6 2 4.46 ± 1.52 4.60 16.9 ± 14.5 0.12 ± 0.08 0.77 ± 0.45

aMeans ± SD (where available) are shown. bTotal number of species identified at site. cTotal number of samples from which THg and MMHg (%)means calculated. Depended on material availability. dTotal number of samples from which MMHg (ng g−1) mean calculated. Depended on materialavailability.

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There is substantial laboratory evidence for Hg0 uptake bylichens. For example, Vannini et al.11 recently showed thatlichens were capable of Hg0 uptake, but that accumulationefficiencies depended on temperature. We observed a negativerelationship between δ13C signatures and both THg andMMHg concentrations (Kendall correlation coefficient, r =−0.33 and −0.35, respectively, p < 0.05), suggesting thatlichens with a CCM may be more selective for CO2, therebyreducing concomitant uptake (active or passive) of otherelements in the atmosphere, including Hg0. We hypothesizethat lichens lacking a CCM would thus have higher uptake ofgaseous Hg species, due to their reduced selectivity for CO2.Other biological factors that could be important to Hg

accumulation in lichens are the relative proportion of dead toliving thalli and lichen age. Metal accumulation has been shownto differ between dead and living thalli in lichens.8 We mightalso expect older lichens to have higher MMHg and THgconcentrations if Hg accumulation rates were higher thangrowth rates. Neither of these factors could be controlled forgiven the nature of our samples; however given the strength ofthe spatial trend observed (Figure 5), these factors are notbelieved to play an important role in THg and MMHgaccumulation in Arctic locales on the spatial scale studied here.Given that it is hard to separate wet from dry deposition in

the Arctic because of generally low levels of precipitation in thissemidesert region, and the difficult logistics of working in thisenvironment, few estimates exist specifically for only wetdeposition of Hg. However, in the Canadian Arctic, THg andMMHg wet/dry loads in snowpacks have been estimated at 3.1± 7.0 and 0.0034 ± 0.0021 μg m−2.49 Sanei et al.51 estimatedwet deposition of THg at Churchill, Manitoba to be between0.5 and 2.0 μg m−2. On northern Ellesmere Island, rainfallMMHg flux estimates were minimal (mean 0.037 ± ng m−2

day−1).52 However, even with reliable estimates for wetdeposition, it would be difficult to actually quantify howmuch of the Hg is taken up by lichens in the environment.The relative importance of dust originating from distant

sources as a source of Hg to lichens depends on both winds andlichen physiology. Strong winds mobilize substantial amountsof particulate matter, which can have an impact on heavy metalconcentrations in lichens.10,53 In the Arctic, dusts are importantsources of heavy metals10 and are transported to the regionfrom distant locations (both natural and anthropogenic) by thedominant air masses.54,55 Another contaminant of concern andan element that we would expect to be transported over longdistances as particulate is lead (Pb).56 While we saw someenrichment of Pb (median EF = 10.0; range = 3−23), EFs weremuch lower than those for Hg, suggesting that particulatedeposition may be a contributing source to the backgroundlevels of Hg enrichment that we observed inland on BathurstIsland (median inland THg EF = 210, MMHg EF = 1800) andthroughout our transect on Devon Island (median THg EF =133, MMHg EF = 349). Lichen morphology, including thepresence of ridges, pits and grooves can play a critical role inthe accumulation of particulate-bound metals. While we did notexplicitly examine the role of lichen morphology in Hgaccumulation, the presence of ridges, pits and grooves increasesurface area to volume ratio and provide surfaces on whichdusts and other materials can preferentially accumulate.8,10

Although lichens may not actually incorporate dust-bound Hginto their tissues, dust particles would still be a source of Hg toconsider when evaluating foodweb dynamics. Dust particles can

be important components of overall contaminant load10,21,22 inlichens and are unlikely to be selectively removed by caribou.One important factor that could not be considered fully in

our analysis due to the absence of material was substrate type.However, lichens collected from the single bedrock site (2C onBathurst Island) had MMHg concentrations approximatelydouble those elsewhere (Table 1), emphasizing the importanceof substrate type in determining accumulation efficiencies.MMHg concentrations in F. cucullata samples collected fromsoils at site 2 were 4.4 and 6.5 ng g−1, but 11.6 ng g−1 in theepilithic sample. Although rock weathering and mineraltransformation57 and consequent uptake by lichens58 are welldocumented, rocks are not a source of MMHg. We hypothesizethat two factors may have led to higher MMHg concentrationsin epilithic lichens: (1) higher retention of MMHg in lichen inthe absence of MMHg diffusion into rock, as shown withlichens and other compounds with the substrate (e.g., ref 58)and (2) higher wind exposure on rock surfaces preventing theaccumulation of snow and thus greater, year-round exchangewith the atmosphere. In open areas of boreal forest, the half-lifeof inorganic Hg on lichens was estimated at 680 ± 180 daysfollowing the deposition of a spike of isotopically labeledinorganic Hg.59 Similar declines in MMHg were observed onvascular plant foliage in the boreal forest;60 however MMHgretention dynamics on lichens have not been investigated toour knowledge. Despite being theoretically solely dependent onatmospheric and particulate deposition, epilithic lichens havebeen rarely studied in the context of monitoring airbornecontaminants.61 Our results highlight their potential asbiomonitors.

Implications for Hg Accumulation in High ArcticCaribou. Caribou are an integral part of the traditional diet inmany regions of the Canadian Arctic and are the mostimportant dietary source of MMHg for most Canadian ArcticAboriginal People.4 Despite this, little work has previously beendone to understand MMHg dynamics at the base of theterrestrial Arctic food web. Here, we show that the proximity ofcaribou feeding grounds to perennially open marine waterslikely has a strong influence on MMHg burdens in cariboubecause lichens in feeding areas closer to open waters havehigher MMHg concentrations than those further inland. This isof particular significance as caribou migrate throughout theirrange in response to seasonal62 or unpredictable63 fluctuationsin food supplies, with dietary implications for the people whodepend on the caribou for nutrition. In fact, we speculate thatDMHg evasion from marine waters with subsequentdemethylation and deposition to adjacent landscapes may bea globally relevant source of MMHg to coastal landscapes (e.g.,California64).

■ ASSOCIATED CONTENT*S Supporting InformationAdditional details on the methods and supplementary datatables. This material is available free of charge via the Internetat http://pubs.acs.org.

■ AUTHOR INFORMATIONCorresponding Author*Phone: 1-780-492-0900. Fax: 1-780-492-9234. E-mail: kyra2@ualberta.ca.

NotesThe authors declare no competing financial interest.

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■ ACKNOWLEDGMENTS

We would like to thank Guangcheng Chen, Alvin Kwan,Mingsheng Ma, Crystal Dodge, Amber Gleason, CatherineWong, Jessica Power, and Lisa Szostek for preparing andanalyzing samples. The project was funded through the NaturalSciences and Engineering Research Council (NSERC)Discovery Grant Program, Natural Resources Canada’s PolarContinental Shelf Program, and ArcticNet grants to Vincent St.Louis, as well as Canadian Boreal Arctic Research (CBAR) andNorthern Scientific Training Program (NSTP) grants to JaneKirk and Igor Lehnherr.

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