Article

Cite This: Environ. Sci. Technol. XXXX, XXX, XXX−XXX pubs.acs.org/est

Total Mercury and Methylmercury in Lake Water of Canada’s Oil

Sands Region
Craig A. Emmerton,*,† Colin A. Cooke,†,‡ Gregory R. Wentworth,† Jennifer A. Graydon,§
Andrei Ryjkov,∥ and Ashu Dastoor∥
†
Environmental Monitoring and Science Division, Alberta Environment and Parks, Edmonton, Alberta T5J 5C6, Canada
‡
Department of Earth and Atmospheric Sciences and §Department of Biological Sciences, University of Alberta, Edmonton, Alberta
T6G 2R3, Canada
∥
Air Quality Research Division, Environment and Climate Change Canada, Dorval, Quebec H9P 1J3, Canada
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*
S Supporting Information
Downloaded via KAOHSIUNG MEDICAL UNIV on September 19, 2018 at 12:47:31 (UTC).

ABSTRACT: Increased delivery of mercury to ecosystems is a common

consequence of industrialization, including in the Athabasca Oil Sands
Region (AOSR) of Canada. Atmospheric mercury deposition has been
studied previously in the AOSR; however, less is known about the impact
of regional industry on toxic methylmercury (MeHg) concentrations in
lake ecosystems. We measured total mercury (THg) and MeHg
concentrations for five years from 50 lakes throughout the AOSR.
Mean lake water concentrations of THg (0.4−5.3 ng L−1) and MeHg
(0.01−0.34 ng L−1) were similar to those of other boreal lakes and <5% of
all samples exceeded Provincial water quality guidelines. Lakes with the
highest THg concentrations were found >100 km northwest of oil sands
mines and received runoff from geological formations high in metals
concentrations. MeHg concentrations were highest in those lakes, and in
smaller productive lakes closer to oil sands mines. Simulated annual
average direct deposition of THg to sampled lakes using an atmospheric chemical transport model showed <2% of all mercury
deposited to sampled lakes was emitted from oil sands activities. Consequently, spatial patterns of mercury in AOSR lakes were
likely most influenced by watershed and lake conditions, though mercury concentrations in these lakes may be perturbed with
future development and climatic change.

■ INTRODUCTION
The Athabasca Oil Sands Region (AOSR) is the largest of
three oil sands deposits in northeastern Alberta, Canada, which
combine together as one of the world’s largest oil reserves.1
Surface mining near the Athabasca River has resulted in
substantial disturbances to landscapes and airborne emissions
from dust and vehicles.2 Nearby utility and upgrading facilities
have generated point source emissions of varying composition3
and considerable stockpiles of liquid and solid waste products.
Together, these features and activities represent key sources of
pollutants, including heavy metals and organic contaminants,
to the local atmosphere, landscapes, and aquatic resources.4,5
Heavy metal mercury (Hg) is a contaminant of concern in
industrialized regions.6 Burning of coal and other fossil fuels,
extraction of gold, smelting, and chemical production and use
have resulted in significant increases in atmospheric Hg
concentrations7 and loading to terrestrial and aquatic
ecosystems.8 Once in these ecosystems, Hg may be transported
to anoxic environments (e.g., flooded soils, wetlands,
hypolimnia, lake sediments9,10) and be methylated into the
neurotoxic form methylmercury (MeHg) by sulfate-reducing,
methanogenic, and iron-reducing bacteria.11,12 MeHg can then
biomagnify through food webs to high concentrations in top
predatory species (e.g., piscivorous fish, large birds, and
mammals13). Considering the proximity to intensive industry
and the potential ramifications of Hg in the environment, the
occurrence and fate of Hg in the AOSR has been of public and
scientific focus.14,15
Previous studies of Hg cycling within the AOSR have
yielded conflicting results. We know of no studies to measure
Hg emissions from point sources in the region; however, oil
sands operations do not appear to be an important source of
gaseous Hg (Hg0) emissions.16 Instead, long-range transport
and forest fire inputs dominated temporal trends in
atmospheric Hg0 concentrations in the AOSR over a three-
year period.16 Wet atmospheric deposition of Hg was directly
measured in the AOSR for nearly two years and showed
concentrations and deposition rates comparable to those of
other sites across Canada, despite contributions from oil sands
Received: March 29, 2018
Revised: August 21, 2018
Accepted: September 4, 2018

© XXXX American Chemical Society A DOI: 10.1021/acs.est.8b01680

Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Environmental Science & Technology Article

Figure 1. Map of lakes sampled for unfiltered total mercury and methylmercury concentrations in the Athabasca Oil Sands Region during
midsummer from 2012 to 2016. Unsampled lakes used for mercury depositional modeling (see Materials and Methods) are also shown. An asterisk
(*) within lake markers indicates those lakes sampled using a float-equipped helicopter (see Materials and Methods).

emissions.17,18 Hg has been measured in a variety of
environmental receptors in the AOSR. Blum et al.19 found
that Hg concentrations in epiphytic lichens throughout the
AOSR were comparable to those of other remote regions and
much lower than those adjacent to industrial sources of Hg. In
bottom sediments of lakes throughout the AOSR, Neville et
al.20 found Hg concentrations in surficial lake sediments to be
similar regardless of distance from oil sands activities. Cooke et
al.21 used lake sediment cores to reconstruct both spatial and
temporal patterns in Hg deposition. They found no evidence
that oil sands operations have enhanced Hg deposition to
regional lakes. A similar finding was reported by Wiklund et
al.22 in their study of lakes from the Peace-Athabasca Delta. In
contrast, the snowpack works by Kirk et al.23 and Willis et al.24
offer the clearest evidence to date that oil sands operations are
a source of Hg and MeHg to local watersheds. The studies
quantified elevated loads of particle-bound total Hg (THg; all
forms of Hg in a sample) and MeHg in snow samples collected
closer to open-pit mines and bitumen upgraders, compared to
B DOI: 10.1021/acs.est.8b01680
further away. Despite the role of atmospheric deposition in
delivering Hg to receiving environments (i.e., watersheds,
lakes25,26), site-specific conditions cannot be overlooked as
important factors influencing net MeHg production and MeHg
biomagnification in aquatic ecosystems.27−30
MeHg concentrations in surface waters can be dependent on
the occurrence and transportability of organic matter.28,30,31
Dissolved organic carbon (DOC) has been found to bind and
transport Hg to aquatic ecosystems for potential biological
uptake.32 DOC is also a source of carbon for microbial
metabolism and associated Hg methylation in anoxic environ-
ments.30,33,34 Wetland and organic soil coverage in a watershed
(a potential source of organic matter to aquatic systems) has
also been cited as a critical factor influencing MeHg
production.27,31 The presence of Hg in aquatic ecosystems
may also correlate closely and positively with other factors
including water temperature,35 and SO42−, metals, and nutrient
concentrations in water.10,29,32,36,37 Conversely, pH38,39 and
redox potential29 can have negative associations with Hg
Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Environmental Science & Technology Article

Table 1. Medians of Selected Physical and Chemical Characteristics of Lake Clusters (Figure 1) Sampled for Mercury
Concentrations in the Athabasca Oil Sands Region, Northeastern Alberta, Canadaa
LV
LA (1000s WA watershed land cover chl-a cond (μS TDP TDN DOC TFe (μg color
lake cluster (n) (ha) m3) (ha) WA:LA (%B,F,U,M) (μg L−1) cm−1) pH (μg L−1) (μg L−1) (mg L−1) L−1) (mg L−1)
Birch Mountains 130 659 3,059 11 44,15,18,0 29 61 6.9 53 782 22 274 189
(11)
Caribou 233 3,500 2,795 12 76,8,1,0 11 34 7.1 13 568 21 347 221
Mountains (5)
Canadian Shield 140 3,518 3,789 25 0,44,46,0 4 55 7.5 4 461 14 155 76
(5)
NE Fort 62 1,004 1,121 15 4,70,8,0 22 48 7.1 11 866 24 140 121
McMurray
(11)
W Fort 46 816 467 20 3,57,35,0 36 63 7.6 17 1,205 34 164 151
McMurray (8)
Stony 138 795 962 6 2,64,17,3 15 14 5.6 13 524 17 238 96
Mountains
(10)
a
Notes: LA-lake area; LV-lake volume; WA-watershed area; B,F,U, M-bog, fen, upland, manmade; chl-a-chlorphyll-a; cond-specific conductivity;
TDP-total dissolved phosphorus; TDN-total dissolved nitrogen; DOC-dissolved organic carbon; TFe-total iron.

concentrations in aquatic ecosystems. Landscape disturbances
within watersheds have also been shown to affect the mobility,
methylation, and concentration of Hg,40 including in the
AOSR.41
Though findings from previous studies have improved our
understanding of Hg cycling in the AOSR, we comparatively
know little about Hg concentrations within important
methylating environments such as lake ecosystems. Further,
understanding how Hg concentrations in AOSR lakes vary
relative to patterns of atmospheric Hg deposition and site-
specific conditions is important, but unknown, for all users of
aquatic resources in the AOSR. Here, we present five years of
midsummer unfiltered THg and unfiltered MeHg concen-
trations from the surface waters of 50 lakes within the AOSR.
The majority of these lakes rest within undisturbed catchments
and they are located at varying distances from oil sands
facilities. Our specific objectives were to (1) compare THg and
MeHg concentrations in lakes against relevant surface water
quality guidelines, (2) determine how THg and MeHg
concentrations in lakes vary in space relative to oil sands
facilities, and (3) identify the physical and chemical conditions
within the lakes and their watersheds that associate closest with
their THg and MeHg concentrations.
Several thousand ephemeral and permanent lakes >1 ha in
surface area45 occur radially within a few hundred kilometers of
oil sands facilities (median lake area ± SE: 4.2 ± 12 ha). In this
study, we monitored the 50 diverse, well-mixed lakes of the
Acid Sensitive Lakes Monitoring Program.46 These lakes were
originally selected based on several factors including (1) an
analysis of potentially acid sensitive lake systems in the
AOSR,47 (2) increasing distance from open-pit mining
operations, (3) accessibility, primarily by float plane (sampled
median lake area: 131 ± 92 ha; range: 3−4349 ha), and (4)
differences in geographical and environmental conditions48
(“lake clusters”; Table 1; Figure 1). Lakes within the Caribou
and Birch mountain clusters are primarily at high elevations,
have bog-rich watersheds underlain by organic cryosol soils
and shale and siltstone bedrock, and have typically stained and
moderately productive surface waters. Canadian Shield lakes
are large, clear, and unproductive, with watersheds covered by
upland forests, thin soils, granitic outcrops, and fens. The NE/
W Fort McMurray and Stony Mountain lake watersheds are
dominated by fen cover but are slightly more developed than
other watersheds. The surface waters of these lakes are
productive, moderately stained, and underlain by mesisolic
soils and shale, sandstone, and siltstone rock.

■ MATERIALS AND METHODS

Regional Description and Study Lakes. The AOSR
(Figure 1) resides mostly within the Boreal Plains ecozone of
western Canada, which is characterized by extensive coverage
of low-relief forests (Picea and Pinus spp.), bog and fen
lowlands, and glacially derived lakes. Boreal Shield covers a
northeast portion of the region and is dominated by granite
outcrops, Picea and Pinus forests, fen wetlands, and numerous
large glacial lakes. The climate in northeastern Alberta is
continental with warm to cold summers.42 Daily mean air
temperature at Fort McMurray is 1.0 °C (range: −5.1 to 7.0
°C) with mean annual precipitation of 419 mm (32% as
snow43). Human activities and resulting land disturbances
across the AOSR are primarily related to oil and gas
exploration and recovery. However, these activities are most
visibly concentrated north of Fort McMurray, and for the
purposes of this paper, we will use site AR644 (Figure 1)
(herein “oil sands facilities”) as a general locator of these
features.
C DOI: 10.1021/acs.est.8b01680
Lake Water Quality Sampling and Chemical Anal-
yses. All 50 remote Acid Sensitive Lakes were sampled once
annually during the peak boreal growing season in July and
August. Most lakes were accessed by float plane, except for
nine lakes which were sampled by a float-equipped helicopter
(Figure 1). Near the center of each lake, a multiprobe
instrument (Hydrolab Minisonde, MS-5) was used to measure
the water column for several physical parameters (water
temperature, pH, specific conductivity, dissolved oxygen, redox
potential, and turbidity). At the same location, unfiltered THg
and unfiltered MeHg samples were directly collected into new,
acid-rinsed amber glass bottles at 30 cm depth using ultraclean
protocols.49 Duplicate samples and field and trip blanks for
THg and MeHg analysis were collected periodically through-
out the program for quality control purposes (Table S1). All
THg and MeHg samples were preserved immediately after
collection with trace-metal-grade HCl at 0.4% and 0.5% of the
sample volumes, respectively. For additional chemical analyses,
multiple integrated water samples were collected from the
entire (well-mixed) measured euphotic zone of each lake using
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a Tygon sampling tube with a one-way valve. These samples
were pooled in a plastic carboy, manually mixed, and poured
into plastic bottles for chemical analyses. All water samples
were sent for chemical analyses the same day as collection.
All chemical analyses were performed at accredited
laboratories within acceptable holding times and using
standard methods and internal quality control practices. THg
samples were analyzed at Innotech Alberta (2012−14) and the
University of Alberta Biogeochemical Analytical Service
Laboratory (BASL; 2015−16) using EPA method 163150
with minor modifications (see Supporting Information).
Reported detection limits for THg were 0.035 to 0.080 ng
L−1 for Innotech and 0.06 ng L−1 for BASL. THg laboratory
duplicates had relative percent differences within 15% (mean:
1%). All MeHg samples were analyzed at the BASL using
isotope dilution and EPA method 163051 with minor
modifications (see Supporting Information). Reported detec-
tion limits of MeHg were 0.010 to 0.016 ng L−1 and laboratory
duplicates had relative percent differences within 24% (mean:
2%). Using THg and MeHg results of all samples, we
calculated the proportion of THg as MeHg (%MeHg) to use
as a proxy for MeHg production in aquatic ecosystems.27
The BASL was also used to analyze samples for additional
chemical parameters including physical chemistry (color, total
alkalinity), major ions (Na+, K+, Ca2+, Mg2+, HCO3−, Cl−,
SO42−), nutrients (total nitrogen (TN), total dissolved N
(TDN), dissolved inorganic N (NO 3 − , NH 4 + ), total
phosphorus (TP), total dissolved P (TDP)), carbon (DOC),
and chlorophyll-a concentration. Total and dissolved metals
(e.g., Al, B, Fe, Mn, Ni, Pb, V, Zn and others; see Table S2)
were measured at Innotech Alberta. For dissolved measure-
ments, samples were passed through filters with a 0.45-μm
pore-size before analysis. All analyses were performed using
standard methods and sample handling protocols.
Numerical and Spatial Analyses. Most measured
parameters had fewer than 10% of samples below method
detection limits, including 0% for THg samples and 7% for
MeHg samples. Therefore censored values were replaced with
one-half the method detection limit.52 Samples with non-
detects comprising more than 20% of all sample data were not
included in any analyses. THg and MeHg concentrations of all
samples were directly compared with Federal and Provincial
surface water quality guidelines for protection of aquatic
life.53,54
Spatial distribution of mean THg, MeHg concentrations,
and mean %MeHg of the 50 lakes across all years was
visualized using an inverse-distance weighting algorithm
between lakes and creation of a contour surface in ArcMap
(ArcGIS v. 10.3.1; ESRI, Redlands, CA, USA). A power of two
and a 15-lake search neighborhood was defined in the
algorithm. The location of higher Hg concentration contours
relative to oil sands surface-mining facilities was used as a
qualitative assessment of potential depositional impacts of oil
sands emissions on lakes. Spatial hot-spot analysis (Getis-Ord
Gi* statistic55) was used to identify lakes with locally high THg
and MeHg concentrations and %MeHg. This analysis was
performed using an inverse distance algorithm and Euclidean
distances between lakes in ArcMap. As an additional
quantitative assessment of the potential impact of oil sands
activities on THg concentrations in sampled lakes, we used a
regional chemical transport model to simulate the emissions,
transport, and direct deposition of THg from oil sands
activities, wildfires, and other sources (i.e., long-range trans-
D DOI: 10.1021/acs.est.8b01680
Article
port) to sampled lake watersheds. Spatially distributed THg
deposition rates (including particle-bound Hg) to ecosystems
for 2011 to 2015 in Canada were simulated by the Hg version
of Environment and Climate Change Canada’s operational air-
quality forecast model GEM-MACH (Global Environmental
Multiscale, Modeling Air Quality and Chemistry model),
GEM-MACH-Hg (see Supporting Information for additional
detail).
Unconstrained Principal Components Analysis (PCA) with
supplementary variables was used to analyze associations
among Hg species, chemistry, and watershed characteristics
data of the 50 lakes (Canoco v. 5.03; Biometris, The
Netherlands; Table S2). This PCA approach defines
ordination axes ad-hoc (THg, MeHg, %MeHg) and they
represent linear combinations of other explanatory parameters.
Individual lakes were also underlain onto the axes to identify
lakes most responsible for strong associations between Hg and
explanatory variables.
■ RESULTS AND DISCUSSION
Hg in AOSR Lakes Relative to Regulatory Guidelines
and Other Northern Lakes. THg and MeHg concentrations,
and %MeHg in northern lakes is underreported in the
literature relative to Hg body burdens in biota directly or
indirectly consumed by humans.56,57 However, sampling
surface waters for THg and MeHg concentrations represents
a potential exposure of MeHg to food webs without time-
consuming, destructive sampling of biota. Mean (±SE) THg
concentrations of the 50 sampled lakes was 2.05 ± 0.17 ng L−1
(median: 1.79 ng L−1) and ranged from 0.36 (Lake S1) to 5.33
(Lake BM6) ng L−1 with a right-skewed distribution. Over the
five years of monitoring (245 samples), the Provincial chronic
water quality guideline for THg (5 ng L−1) was exceeded 10
times, most predominantly in three lakes (BM5, BM6, and
BM8) located in the Birch Mountains (Figure 2). Exceedances
were distributed across all sampling years, but occurred more
frequently during 2012, 2014, and 2016 (Figure S1). WF1 was
the only lake outside of the Birch Mountains to exceed
guidelines, which occurred only in 2012. Other lakes showed
little temporal variation in THg concentrations. Acute
guidelines for THg were not exceeded during any year in
any lake.
All MeHg concentrations were well below water quality
guidelines (Figure 2). Mean MeHg concentration across all
lakes was 0.097 ± 0.011 ng L−1 (median: 0.086 ng L−1) with a
larger relative range of concentrations from <0.01 (NE10) to
0.344 ng L−1 (BM8) compared to THg. Variability of
concentrations over time within lakes was also generally larger
for MeHg (Figure S2) compared to THg. Between years, lakes
within the Caribou, Canadian Shield, Northeast of Fort
McMurray, and the Stony Mountain clusters changed little.
However, selected lakes of the Birch Mountains and West of
Fort McMurray were highly variable between years with peak
MeHg concentrations in 2013 and 2016.
No guidelines for aquatic life protection exist for %MeHg.
Mean %MeHg in the sampled lakes (Figure 2) was 5.26 ±
0.67% (median: 3.76%) with a range of 1.2 (NE10) to 22.0%
(BM10). Between sample years, most lakes exhibited low
variability in %MeHg though a few lakes within the Birch
Mountain and West of Fort McMurray clusters were highly
variable between years (Figure S3). BM10, for example, had
very high %MeHg in 2016 (48%) and was a substantial outlier
relative to other Birch Mountain lakes after 2013. Several lakes
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Environmental Science & Technology
Figure 2. Unfiltered total mercury (THg) and methylmercury
(MeHg) concentrations and proportion of THg as MeHg (%
MeHg) of sampled lakes in the Athabasca Oil Sands Region during
the midsummers of 2012−2016. Individual lakes within clusters are
also labeled. Chronic and acute surface water quality guidelines for
Alberta (ASWQ) and chronic guidelines for Canada (CCME-PAL;
see Materials and Methods) are shown as horizontal lines for THg
and MeHg.
West of Fort McMurray were highly variable between years
with WF6 showing a particularly high ratio in 2013 (44%).
Our lake Hg monitoring revealed concentrations mostly
below Provincial and Federal water quality guidelines, and
concentrations of similar magnitude and variability as other
northern lakes across the boreal and subarctic (Table 2). For
example, Braaten et al.37 reported a similar range of Hg
concentrations in a survey of 46 boreal lakes from southeastern
Norway. These other studies, in conjunction with results from
our lake monitoring program, suggest Hg concentrations in
AOSR lakes are not elevated relative to other regions.20−22
However, it is an important exercise to understand
contemporary factors influencing Hg concentrations in
AOSR lakes considering projected oil sands expansion.58
Hg in AOSR Lakes and Proximity to Current Oil Sands
Operations. A southeasterly decrease of THg concentrations
in sampled lakes was evident across the AOSR (Figure 3a).
The highest THg concentrations were found in the Birch and
Caribou Mountain lakes, approximately 150−300 km north-
west of oil sands facilities. The Birch Mountain cluster
E DOI: 10.1021/acs.est.8b01680
Article
included lakes considered hot-spots of THg concentrations
(e.g., BM5−BM8; Table S3). In contrast, lakes located closer
to current oil sands facilities typically had lower THg
concentrations, which was a different spatial pattern from the
regional snowpack, which showed higher concentrations in
study sites located closer to current oil sands operations.23,24
Further, lakes in the Birch Mountain cluster, which generally
had relatively high THg concentrations, did include large lakes
with some of the lowest THg concentrations in the data set
(e.g., Legend Lake (BM1) and Namur Lake (BM2)). Because
of inconsistencies of THg concentrations in lakes across space
relative to industrial emissions of Hg (i.e., AR6 in Figure 1), we
suggest factors other than atmospheric Hg emissions from oil
sands facilities likely control lake water THg concentrations.
Lakes with high MeHg concentrations also occurred in the
Birch Mountains (Table S3) and were concurrently high in
THg concentrations (Figures 2 and 3a,b). Because these lakes
are far from oil sands emissions and potential inputs of
industrial Hg, their high MeHg concentrations may have been
related to methylation of local sources of THg in the
watersheds. Several lakes west of Fort McMurray also had
high MeHg concentrations with hotspots in BM10, WF4, and
WF6 (Figures 2 and 3b; Table S3); however, these lakes had
lower THg concentrations despite their closer proximity to oil
sands facilities and potential sources of inorganic Hg
deposition (Figure 3a; Figure S4). Consequently, %MeHg
was much higher in these lakes (Figure 3c) including %MeHg
hotspots in BM10, WF4−WF6 (Table S3). This result suggests
that MeHg concentrations in these lakes were more related to
efficient in-lake methylation of Hg and less associated with
external supply of inorganic Hg from either their watersheds or
direct atmospheric deposition. Differing conditions in lakes
similarly close to oil sands emissions (i.e., just to the east and
downwind of the oil sands) further corroborates this
hypothesis (Figure 3c). Collectively, THg, MeHg, and %
MeHg patterns in sampled lakes across the AOSR are not what
would be expected if significant industrial sources of Hg were
present within oil sands facilities. This suggests that AOSR
lakes and their watersheds do not receive substantial
deposition of Hg during the open-water season, or our
sampled lakes were outside of the area receiving most oil
sands-related Hg deposition.
We simulated source-specific total and annual THg
deposition to watersheds of all 50 sampled lakes from August
2011 to December 2015 in the AOSR using the GEM-MACH-
Hg model (Table S4). For each of the 50 lake watersheds,
modeled THg deposition was dominated by inputs from other
sources (e.g., long-range transport; mean ± SE:, 97.0 ± 0.1%
of total Hg deposition; 32.8 ± 0.4 μg m−2 yr−1) while wildfires
accounted for 2.6 ± 0.1% (0.9 ± 0.0 μg m−2 yr−1) (Figure 4).
Oil sands sources only accounted for 0.4 ± 0.0% (0.1 ± 0.0 μg
m−2 yr−1) of total Hg deposition to our study lakes. Sampled
lakes closest to oil sand facilities (i.e., 25−35 km away) were
estimated to receive <2% of all atmospherically deposited Hg
from oil sands sources. Because the few lakes closest to oil
sands facilities were not sampled in this study, we simulated
deposition onto 10 unsampled lakes closer than 25 km from oil
sand facilities (Figures 1 and 4). These lakes better aligned in
space to previous Hg snowpack studies.23,24 We found that
though relative deposition of Hg from oil sands activities did
increase to these lakes, it was not larger than 7% of all received
deposition from the atmosphere (Table S4). These results,
together with spatial patterns of Hg in the AOSR and results
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Table 2. Unfiltered Total Mercury (THg) and Methylmercury (MeHg) Concentrations and the Proportion of THg as MeHg
(%MeHg) from Surface Waters (0−2 m Depth) of Selected Northern Lakes from This Study and Others
ecoregion (location) lakes (no.) period sampled THg (ng L−1) MeHg (ng L−1) %MeHg source
Mixedwood (Ontario, Canada) 1 May−Oct 1.7 26
Mixedwood (Ontario, Canada) 1 all year 1.7 0.04 4 27
Mixedwood (Minnesota, USA) 10 May−Sep 1.9−5.0 36
Mixedwood (Minnesota, USA) 17 May, Jul, Sep 0.5−3.3 <0.04−0.30 6−13 31
Mixedwood (Wisconsin, USA) 15 May, Oct 0.5−4.4 0.04−0.83 6−30 32
Boreal (Alberta, Canada) 50 Jul−Aug 0.4−5.3 0.01−0.34 1−22 this study
Boreal (Quebec, Canada) 5 Jun, Sep 0.4−3.3 0.04−0.57 6−18 39
Boreal (southern Norway) 9 Jun 1.2−2.6 0.05−0.19 3−9 30
Boreal (southeastern Norway) 46 Mar−Jun 1.2−6.6 0.04−0.70 1−27 37
Boreal (southeastern Norway) 4 Jun−Sep 1.7−4.3 0.02−0.16 1−6 73
Boreal (Ontario, Canada) 27 Jul−Aug 0.3−2.9 <0.00−0.04 0−3 81
Boreal/Subarctic (NWT,a Canada) 18 open-water 0.1−3.1 0.00−0.16 0−36 66
Subarctic (NWT, Canada) 6 Jun−Aug 1.8−3.4 0.05−0.18 2−13 82
Subarctic (NWT, Canada) 26 open-water 0.7−4.7 74
Subarctic (northern Norway) 5 Mar−Jun 0.5−1.6 <0.02−0.06 3−4 37
a
Notes: NWT: Northwest Territories

Figure 3. Inverse distance weighting modeling of (a) unfiltered total mercury (THg) and (b) unfiltered methylmercury (MeHg) surface water
concentrations, and (c) proportion of THg as MeHg (%MeHg) of sampled lakes in the Athabasca Oil Sands Region during the midsummers of
2012−2016.

from other studies (see Introduction), suggest that site-specific
conditions within sampled lakes and watersheds are likely most
important to the ultimate concentrations measured in surface
lake waters.
Site-Specific Factors and Their Associations with Hg
in AOSR Lakes. We used PCA to assess site-specific
associations between Hg concentrations in lake water and
other water quality and watershed metrics (Table S2). We
found THg concentrations were strongly and positively
associated with water color, TDP, and several metal
concentrations including Al, Fe, Cd, Cr, Pb, and V in AOSR
lakes (Figure 5). These associations were acute in particular
high-elevation lakes in the Birch, Caribou, and Stony
mountains. Comparatively, DOC concentrations were not
closely associated with THg or water color in AOSR lakes,
despite widespread wetland coverage in the watersheds of most
sampled lakes. We also observed relatively poor associations
F DOI: 10.1021/acs.est.8b01680
between TDP and several markers of algal productivity
including concentrations of N, TP, and chlorophyll-a in
AOSR lakes, which is not typical for waters receiving runoff
from nutrient-rich organic soils.59 Consequently, the strong
associations observed between TDP, Al, Fe, other metals, and
water color (Figure 5), suggests an important influence of
inorganic phosphorus and metals sources, perhaps as
phosphorus−metal oxide complexes,59 in lakes with high
THg concentrations. Because total metals were mostly in
dissolved form (Table S5), this suggests that these complexes
were colloidal-sized (i.e., < 0.45 μm in size). These chemical
associations are also consistent with runoff through the metal-
rich marine shales of the Birch, Caribou, and Stony
mountains,60 which can include cinnabar61 and therefore likely
inorganic Hg sources. These conclusions are supported by
Neville et al.20 who found that THg in lake sediments within
the AOSR associated closest with silt fractions, rather than
Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Environmental Science & Technology
Figure 4. Modeled atmospheric total mercury (THg) deposition (wet
+ dry; 2011−2015) to sampled lakes from either oil sands or wildfire
sources relative to total atmospheric Hg deposition using the Global
Environmental Multiscale, Modeling Air Quality and Chemistry
Model (see Materials and Methods). Deposition proportions to 10
unsampled lakes (30 km−xx) closer to oil sands facilities are also
shown.
Figure 5. Unconstrained Principal Components Analysis for
unfiltered total mercury (THg), methylmercury (MeHg), and
proportion of THg as MeHg (%MeHg) variables (blue arrows)
relative to explanatory variables (gray arrows) and sampled lakes (gray
outlined circles). See Table S2 for full variable descriptions and Figure
1 for lake locations.
organic matter, suggesting a minerogenic source of THg to
lakes.
MeHg was less strongly associated in ordination space with
measured chemical and landscapes features, as compared to
THg (Figure 5). NH4+ and TP were important correlates of
MeHg, with weaker and positive associations with SO42− and a
few metals, including Ba and Mn. Some of these positive
associations are consistent with Hg methylation environments
in general. For example, metabolism of sulfate-reducing
bacteria and related Hg methylation occurs effectively in
high SO42− waters and sediments as these processes use this
oxidized compound as a metabolic electron donor.62 The close
G DOI: 10.1021/acs.est.8b01680
Article
association among NH4+, TP, and MeHg concentrations may
be a reflection of high algal productivity in the lakes most
responsible for the strong association (e.g.,WF4−6, BM10).
Deposition of algal cells to sediments provides a fresh input of
labile carbon to sediments and promotes mineralization of
organic matter and decomposition-related anoxia.63 This may
result in increased Hg methylation64 by planktonic and
aggregated bacteria,65 ammonification, and shifts in redox
conditions in sediments causing subsequent releases of Hg and
nutrients to the water column. The strong association of TP
with MeHg, but less so with TDP or measurements related to
algal productivity, was less straightforward to interpret (see
next section). The influence of lake volume was also a notable
factor negatively associated with MeHg concentrations as the
pelagic water chemistry of larger lakes is typically less impacted
by methylating regions along the lake margins.37,66
%MeHg was strongly and positively correlated with in situ
turbidity and TDN concentration and correlated slightly
weaker with chlorophyll-a and DOC concentrations (Figure
5). These positive associations, driven by lakes with low THg
concentrations (Figure S4), suggest Hg methylation rates were
higher in lakes with greater productivity and algal biomass. In
higher productivity conditions, increased oxygen use by
decomposers in sediments receiving high labile organic matter
deposition rates and related anoxia in sediments would be
expected to drive Hg methylation rates.29 Though TP and TN
were associated closely in lakes within the high-productivity−
high %MeHg cluster west of Fort McMurray, a wider influence
of P sourced from colloid-sized inorganic complexes could
explain the separation in ordination space between N and P
overall and also explain the separation of THg from %MeHg
(Figure 5). Other measurements correlating weakly and
negatively with %MeHg included watershed runoff yield and
%fen coverage in the watershed. These watershed character-
istics describe faster-flushing watersheds which would limit the
accumulation of MeHg in lakes and lower %MeHg values.67
However, targeted mass balance chemical monitoring of lakes
would be the most appropriate means of understanding the
role of Hg in runoff and its impacts on lake water
concentrations.
Future Stressors on Hg Distribution in Lakes of the
AOSR. Though site-specific factors likely most influenced Hg
concentrations in sampled lakes across the AOSR, these
systems are expected to endure increasing oil-sands-related
impacts in the future, including surface mining expansions and
increases in dust-related deposition. These activities will likely
provide additional atmospheric Hg loading to lakes; however,
even a doubling of modeled THg deposition to our sampled
watersheds would still result in only minor increases in total
deposition (Table S4). Considering Hg is often mobilized to a
greater extent within watersheds cleared for human develop-
ment,40 an important unknown driver of future Hg loading to
these lakes will be the degree to which their watersheds will be
disturbed by anthropogenic activities.
The Boreal Plains ecoregion is also expected to experience
future rapid climatic change in several forms including
increases in air temperature, growing season duration, and
precipitation.68 These changes may have varying impacts on
Hg cycling in watersheds. For example, increasing air
temperatures over longer growing seasons may bolster Hg
methylation rates and gross MeHg production within AOSR
lakes as microbial metabolism is strongly and positively
associated with ambient temperatures.35,69,70 Increasing
Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Environmental Science & Technology
precipitation in the form of rainfall can be expected to mobilize
inorganic and organic matter and therefore downstream Hg
loading to certain lakes. Darkening surface waters within lakes
due to increased terrestrial loading of DOC71 may also
decrease MeHg losses via photodemethylation,72,73 and thus
sustain MeHg concentrations in lakes. Recent work, however,
has shown that high DOC systems may also inhibit Hg
methylation because of the predominance of recalcitrant forms
of organic matter.74 The frequency of weather conditions
suitable for wildfires has also increased significantly in recent
years in Alberta.75 Though wildfires may be expected to deliver
more Hg to lake watersheds, they are typically a small
contributor to Hg deposition on a regional scale76 (Table S4)
and fire-related impacts on lake Hg cycling are typically short-
lived.77 Finally, biomagnification of Hg up food webs may be
affected indirectly by increasing productivity recently observed
within AOSR lakes.78 Increasing productivity in freshwaters
can both support greater Hg methylation rates29,79 or hinder
Hg accumulation in foodwebs due to growth dilution
processes.36,80 Our ordination analysis suggests moderately
positive associations between lakes with higher MeHg
concentrations and those with higher nutrient contents and
algal densities (Figure 5). When considered together, these
multiple (and possibly concurrently occurring) potential
impacts from direct and indirect climate stressors severely
complicate future understanding of Hg cycling in AOSR lakes.
Results from this study suggest that site-specific conditions,
rather than Hg deposition from oil sands atmospheric
emissions, drive contemporary Hg concentrations in AOSR
lakes. However, in-lake influences on Hg cycling, and other
parameters of interest, can be complex and highly variable,
potentially masking climate- or industrial-related changes over
time. Consequently, we recommend a greater focus on whole-
ecosystem monitoring of a subset of similar lake-types in the
AOSR to answer specific scientific questions related to sources
and fate of contaminants of concern in these systems, including
other trace metals released by oil sands activities (e.g., Pb, V).
Further, improved lake monitoring programs in the AOSR
should be coupled with an increased focus on the ultimate
uptake of MeHg in sport fish and both potential human health
risks and benefits associated with their consumption.
■
ASSOCIATED CONTENT
*
S Supporting Information
The Supporting Information is available free of charge on the
ACS Publications website at DOI: 10.1021/acs.est.8b01680.
Two text sections, five tables, and four figures (PDF)
■
AUTHOR INFORMATION
Corresponding Author
*Phone: 780-229-7279; e-mail: craig.emmerton@gov.ab.ca.
ORCID
Craig A. Emmerton: 0000-0001-9511-9191
Colin A. Cooke: 0000-0002-7417-5263
Notes
The authors declare no competing financial interest.
■
ACKNOWLEDGMENTS
Funding for this study was provided by the Joint Canada−
Alberta Oil Sands Monitoring Program. We thank the
tremendous effort by field monitoring staff at Alberta
H DOI: 10.1021/acs.est.8b01680
Article
Environment and Parks, particularly Jessica Pope, Chris
Ware, and Bob Werner. Helicopter support was provided by
Phoenix Heli-Flight in Fort McMurray, Alberta and float plane
transportation by Voyage Air in Buffalo Narrows, Saskatch-
ewan. We also thank Dr. Mingsheng Ma at the BASL for
analytical support. We also appreciated feedback from various
Alberta Environment and Parks scientists and Dr. Daniel
Andrews. Rebekah Adams and Alex Lake provided manuscript
support.
■
REFERENCES
(1) Shastri, A.; Mungai, M.; Härm, M.; Preegel, G.; Tarus, V.;
Zubaviciute, A. World Energy Resources Oil 2016; World Energy
Council, 2016. URL: https://www.worldenergy.org/publications/
2016/world-energy-resources-2016/.
(2) Landis, M. S.; Pancras, J. P.; Graney, J. R.; White, E. M.;
Edgerton, E. S.; Legge, A.; Percy, K. E. Source apportionment of
ambient fine and coarse particulate matter at the Fort Mackay
community site, in the Athabasca oil sands region, Alberta, Canada.
Sci. Total Environ. 2017, 584, 105−117.
(3) Simpson, I. J.; Blake, N. J.; Barletta, B.; Diskin, G. S.; Fuelberg,
H. E.; Gorham, K.; Huey, L. G.; Meinardi, S.; Rowland, F. S.; Vay, S.
A.; Weinheimer, A. J.; Yang, M.; Blake, D. R. Characterization of trace
gases measured over Alberta oil sands mining operations: 76 speciated
c-2-c-10 volatile organic compounds (VOCs), CO2, CH4, CO, NO,
NO2, NOv, O-3 and SO2. Atmos. Chem. Phys. 2010, 10 (23), 11931−
11954.
(4) Huang, R. F.; McPhedran, K. N.; Yang, L. L.; Gamal El-Din, M.
G. Characterization and distribution of metal and nonmetal elements
in the Alberta oil sands region of Canada. Chemosphere 2016, 147,
218−229.
(5) National Pollutant Release Inventory. URL: https://www.canada.
ca/en/environment-climate-change/services/national-pollutant-
release-inventory/tools-resources-data.html.
(6) Canadian Mercury Science Assessment 2016. Chapter 9. Mercury
cycling in ecosystems and the response to changes in anthropogenic
emissions. Clean Air Regulatory Agenda, Environment and Climate
Change Canada, Government of Canada, 2016; pp 437−556.
(7) Schuster, P. F.; Krabbenhoft, D. P.; Naftz, D. L.; Cecil, L. D.;
Olson, M. L.; Dewild, J. F.; Susong, D. D.; Green, J. R.; Abbott, M. L.
Atmospheric mercury deposition during the last 270 years: A glacial
ice core record of natural and anthropogenic sources. Environ. Sci.
Technol. 2002, 36 (11), 2303−2310.
(8) Boening, D. W. Ecological effects, transport, and fate of mercury:
A general review. Chemosphere 2000, 40 (12), 1335−1351.
(9) Kelly, C. A.; Rudd, J. W. M.; Bodaly, R. A.; Roulet, N. P.;
St.Louis, V. L.; Heyes, A.; Moore, T. R.; Schiff, S.; Aravena, R.; Scott,
K. J.; Dyck, B.; Harris, R.; Warner, B.; Edwards, G. Increases in fluxes
of greenhouse gases and methyl mercury following flooding of an
experimental reservoir. Environ. Sci. Technol. 1997, 31 (5), 1334−
1344.
(10) Eckley, C. S.; Hintelmann, H. Determination of mercury
methylation potentials in the water column of lakes across Canada.
Sci. Total Environ. 2006, 368 (1), 111−125.
(11) Branfireun, B. A.; Bishop, K.; Roulet, N. T.; Granberg, G.;
Nilsson, M. Mercury cycling in boreal ecosystems: The long-term
effect of acid rain constituents on peatland pore water methylmercury
concentrations. Geophys. Res. Lett. 2001, 28 (7), 1227−1230.
(12) Parks, J. M.; Johs, A.; Podar, M.; Bridou, R.; Hurt, R. A., Jr.;
Smith, S. D.; Tomanicek, S. J.; Qian, Y.; Brown, S. D.; Brandt, C. C.;
Palumbo, A. V.; Smith, J. C.; Wall, J. D.; Elias, D. A.; Liang, L. The
genetic basis for bacterial mercury methylation. Science 2013, 339,
1332.
(13) Scheuhammer, A. M.; Meyer, M. W.; Sandheinrich, M. B.;
Murray, M. W. Effects of environmental methylmercury on the health
of wild birds, mammals, and fish. Ambio 2007, 36 (1), 12−18.
(14) Timoney, K. P.; Lee, P. Does the Alberta tar sands industry
pollute? The scientific evidence. Open Conserv. Biol. J. 2009, 3, 65−81.
Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Environmental Science & Technology
(15) Evans, M. S.; Talbot, A. Investigations of mercury
concentrations in walleye and other fish in the Athabasca River
ecosystem with increasing oil sands developments. J. Environ. Monit.
2012, 14 (7), 1989−2003.
(16) Parsons, M. T.; McLennan, D.; Lapalme, M.; Mooney, C.;
Watt, C.; Mintz, R. Total gaseous mercury concentration measure-
ments at Fort McMurray, Alberta, Canada. Atmosphere 2013, 4 (4),
472−493.
(17) Lynam, M. M.; Dvonch, J. T.; Barres, J. A.; Morishita, M.;
Legge, A.; Percy, K. Environ. Pollut. 2015, 206, 469.
(18) Canadian Mercury Science Assessment 2016. Chapter 4.
Atmospheric processes, transport, levels, and trends, Clean Air
Regulatory Agenda, Environment and Climate Change Canada.
Government of Canada, 2016; pp 135−228.
(19) Blum, J. D.; Johnson, M. W.; Gleason, J. D.; Demers, J. D.;
Landis, M. S.; Krupa, S. Mercury concentration and isotopic
composition of epiphytic tree lichens in the Athabasca oil sands
region. Dev. Environ. Sci. 2012, 11, 373−390.
(20) Neville, L. A.; Patterson, R. T.; Gammon, P.; Macumber, A. L.
Relationship between ecological indicators (arcellacea), total mercury
concentrations and grain size in lakes within the Athabasca oil sands
region, Alberta. Environ. Earth Sci. 2014, 72 (2), 577−588.
(21) Cooke, C. A.; Kirk, J. L.; Muir, D. C. G.; Wiklund, J. A.; Wang,
X. W.; Gleason, A.; Evans, M. S. Spatial and temporal patterns in trace
element deposition to lakes in the Athabasca oil sands region
(Alberta, Canada). Environ. Res. Lett. 2017, 12 (12), 124001.
(22) Wiklund, J. A.; Hall, R. I.; Wolfe, B. B.; Edwards, T. W. D.;
Farwell, A. J.; Dixon, D. G. Has Alberta oil sands development
increased far-field delivery of airborne contaminants to the Peace-
Athabasca delta? Sci. Total Environ. 2012, 433, 379−382.
(23) Kirk, J. L.; Muir, D. C. G.; Gleason, A.; Wang, X. W.; Lawson,
G.; Frank, R. A.; Lehnherr, I.; Wrona, F. Atmospheric deposition of
mercury and methylmercury to landscapes and waterbodies of the
Athabasca oil sands region. Environ. Sci. Technol. 2014, 48 (13),
7374−7383.
(24) Willis, C. E.; Kirk, J. L.; St.Louis, V. L.; Lehnherr, I.; Ariya, P.
A.; Rangel-Alvarado, R. B. Sources of methylmercury to snowpacks of
the Alberta oil sands region: A study of in situ methylation and
particulates. Environ. Sci. Technol. 2018, 52 (2), 531−540.
(25) Watras, C. J.; Morrison, K. A.; Back, R. C. Mass balance studies
of mercury and methyl mercury in small temperate/boreal lakes of the
northern hemisphere. In Global and Regional Mercury Cycles: Sources,
Fluxes and Mass Balances; Springer: Dordrecht, 1996; pp 329−358.
(26) Harris, R. C.; Rudd, J. W.; Amyot, M.; Babiarz, C. L.; Beaty, K.
G.; Blanchfield, P. J.; Bodaly, R. A.; Branfireun, B. A.; Gilmour, C. C.;
Graydon, J. A.; et al. Whole-ecosystem study shows rapid fish-mercury
response to changes in mercury deposition. Proc. Natl. Acad. Sci. U. S.
A. 2007, 104 (42), 16586−16591.
(27) St. Louis, V. L.; Rudd, J. W. M.; Kelly, C. A.; Beaty, K. G.;
Bloom, N. S.; Flett, R. J. Importance of wetlands as sources of methyl
mercury to boreal forest ecosystems. Can. J. Fish. Aquat. Sci. 1994, 51
(5), 1065−1076.
(28) Watras, C. J.; Morrison, K. A.; Host, J. S.; Bloom, N. S.
Concentration of mercury species in relationship to other site-specific
factors in the surface waters of northern Wisconsin lakes. Limnol.
Oceanogr. 1995, 40 (3), 556−565.
(29) MacMillan, G. A.; Girard, C.; Chetelat, J.; Laurion, I.; Amyot,
M. High methylmercury in arctic and subarctic ponds is related to
nutrient levels in the warming eastern Canadian arctic. Environ. Sci.
Technol. 2015, 49 (13), 7743−7753.
(30) Moreno, C. E.; Fjeld, E.; Lydersen, E. The effects of wildfire on
mercury and stable isotopes (delta n-15, delta c-13) in water and biota
of small boreal, acidic lakes in southern Norway. Environ. Monit.
Assess. 2016, 188 (3), 178.
(31) Wiener, J. G.; Knights, B. C.; Sandheinrich, M. B.; Jeremiason,
J. D.; Brigham, M. E.; Engstrom, D. R.; Woodruff, L. G.; Cannon, W.
F.; Balogh, S. J. Mercury in soils, lakes, and fish in Voyageurs National
Park (Minnesota): Importance of atmospheric deposition and
ecosystem factors. Environ. Sci. Technol. 2006, 40 (20), 6261−6268.
I DOI: 10.1021/acs.est.8b01680
Article
(32) Watras, C. J.; Back, R. C.; Halvorsen, S.; Hudson, R. J. M.;
Morrison, K. A.; Wente, S. P. Bioaccumulation of mercury in pelagic
freshwater food webs. Sci. Total Environ. 1998, 219 (2−3), 183−208.
(33) Gu, B.; Bian, Y.; Miller, C. L.; Dong, W.; Jiang, X.; Liang, L.
Mercury reduction and complexation by natural organic matter in
anoxic environments. Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 1479−
1483.
(34) Schaefer, J. K.; Rocks, S. S.; Zheng, W.; Liang, L.; Gu, B.;
Morel, F. M. M. Active transport, substrate specificity, and
methylation of Hg(II) in anaerobic bacteria. Proc. Natl. Acad. Sci.
U. S. A. 2011, 108, 8714−8719.
(35) Bodaly, R. A.; Rudd, J. W. M.; Fudge, R. J. P.; Kelly, C. A.
Mercury concentrations in fish related to size of remote Canadian
Shield lakes. Can. J. Fish. Aquat. Sci. 1993, 50 (5), 980−987.
(36) Gabriel, M. C.; Kolka, R.; Wickman, T.; Nater, E.; Woodruff, L.
Evaluating the spatial variation of total mercury in young-of-year
yellow perch (perca flavescens), surface water and upland soil for
watershed-lake systems within the southern boreal shield. Sci. Total
Environ. 2009, 407 (13), 4117−4126.
(37) Braaten, H. F. V.; de Wit, H. A.; Fjeld, E.; Rognerud, S.;
Lydersen, E.; Larssen, T. Environmental factors influencing mercury
speciation in subarctic and boreal lakes. Sci. Total Environ. 2014, 476,
336−345.
(38) Kelly, C. A.; Rudd, J. W. M.; Holoka, M. H. Effect of pH on
mercury uptake by an aquatic bacterium: Implications for Hg cycling.
Environ. Sci. Technol. 2003, 37 (13), 2941−2946.
(39) Chetelat, J.; Amyot, M.; Garcia, E. Habitat-specific
bioaccumulation of methylmercury in invertebrates of small mid-
latitude lakes in North America. Environ. Pollut. 2011, 159 (1), 10−
17.
(40) Engstrom, D. R.; Balogh, S. J.; Swain, E. B. History of mercury
inputs to Minnesota lakes: Influences of watershed disturbance and
localized atmospheric deposition. Limnol. Oceanogr. 2007, 52 (6),
2467−2483.
(41) Kelly, E. N.; Schindler, D. W.; Hodson, P. V.; Short, J. W.;
Radmanovich, R.; Nielsen, C. C. Oil sands development contributes
elements toxic at low concentrations to the Athabasca River and its
tributaries. Proc. Natl. Acad. Sci. U. S. A. 2010, 107 (37), 16178−
16183.
(42) Peel, M. C.; Finlayson, B. L.; McMahon, T. A. Updated world
map of the Koppen-Geiger climate classification. Hydrol. Earth Syst.
Sci. 2007, 11 (5), 1633−1644.
(43) Environment and Climate Change Canada. Canadian Climate
Normals, 2018. http://climate.weather.gc.ca/climate_normals/.
(44) Kelly, E. N.; Short, J. W.; Schindler, D. W.; Hodson, P. V.; Ma,
M. S.; Kwan, A. K.; Fortin, B. L. Oil sands development contributes
polycyclic aromatic compounds to the Athabasca river and its
tributaries. Proc. Natl. Acad. Sci. U. S. A. 2009, 106 (52), 22346−
22351.
(45) Cael, B. B.; Seekell, D. A. The size-distribution of earth’s lakes.
Sci. Rep. 2016, 6, 29633.
(46) Hatfield Consultants. Regional Aquatics Monitoring in Support of
the Joint Oil Sands Monitoring Plan: 2015 Final Program Report; 2016;
1272 pp.
(47) Trew, D. O. The sensitivity of Alberta lakes to acidic
deposition. In Proceedings of the Fourth Annual Workshop for the
Alberta Lake Management Society, September 30−October 1, 1995,
Lac La Biche, AB; 60 pp.
(48) Gibson, J. J.; Birks, S. J.; Yi, Y.; Vitt, D. H. Runoff to boreal
lakes linked to land cover, watershed morphology and permafrost
thaw: A 9-year isotope mass balance assessment. Hydrological Processes
2015, 29 (18), 3848−3861.
(49) Method 1669: Sampling Ambient Water for Trace Metals at EPA
Water Quality Criteria Levels; U.S. Environmental Protection Agency:
Washington, DC, 1996.
(50) Method 1631, Revision E: Mercury in Water by Oxidation, Purge
and Trap, and Cold Vapor Atomic Fluorescence Spectrometry; U.S.
Environmental Protection Agency: Washington, DC, 2002.
Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Environmental Science & Technology
(51) Method 1630, Methyl Mercury in Water by Distillations, Aqueoius
Ethylation, Purge and Trap, and Cold Vapor Atomic Fluorescence
Spectrometry; U.S. Environmental Protection Agency: Washington,
DC, 1998.
(52) Antweiler, R. C. Evaluation of statistical treatments of left-
censored environmental data using coincident uncensored data sets.
II. Group comparisons. Environ. Sci. Technol. 2015, 49 (22), 13439−
13446.
(53) CCME. Canadian Council of Ministers of the Environment
(CCME); 2003, http://st-ts.ccme.ca/ (accessed Jan, 2018).
(54) Alberta Environment & Sustainable Resource Development
(ESRD). Environmental Quality Guidelines for Alberta Surface Waters;
Water Policy Branch, Policy Division. Edmonton, Alberta, 2014; 48
pp.
(55) Ord, J. K.; Getis, A. Local spatial autocorrelation statistics -
distributional issues and an application. Geographical Analysis 1995,
27 (4), 286−306.
(56) Canadian Mercury Science Assessment 2016. Chapter 10.
Mercury in terrestrial and aquatic biota across Canada: Geographic
variation; Clean Air Regulatory Agenda, Environment and Climate
Change Canada, Government of Canada, 2016; pp 557−626.
(57) Canadian Mercury Science Assessment 2016. Chapter 6. Mercury
fate and methylation in freshwater aquatic ecosystems. Clean Air
Regulatory Agenda, Environment and Climate Change Canada,
Government of Canada, 2016; pp 285−322.
(58) CAPP. 2017 Crude Oil Forecast, Markets and Transportation;
Canadian Association of Petroleum Producers, 2017.
(59) Chapin, F. S.; Matson, P. A., Vitousek, P. M. Principles of
Terrestrial Ecosystem Ecology; Springer: New York, 2011.
(60) Dufresne, M. B.; Eccles, D. R.; Leckie, D. A. The Geological and
Geochemical Setting of the Mid-Cretaceous Shaftesbury Formation and
Other Colorado Group Sedimentary Unities in Northern Alberta; Alberta
Geological Survey, 2001.
(61) Rukhlov, A. S. Review of Metallic Mineralization in Alberta with
Emphasis on Gold Potential; Energy Resources Conservation Board,
Alberta Geological Survey, 2011.
(62) Gilmour, C. C.; Henry, E. A.; Mitchell, R. Sulfate stimulation of
mercury methylation in fresh-water sediments. Environ. Sci. Technol.
1992, 26 (11), 2281−2287.
(63) Wetzel, R. G. Limnology: Lake and River Ecosystems, 2nd ed.;
Saunders College Publishing: Orlando, FL, USA, 2001.
(64) He, T.; Feng, X.; Guo, Y.; Qiu, G.; Li, Z.; Liang, L.; Lu, J. The
impact of eutrophication on the biogeochemical cycling of mercury
species in a reservoir: A case study from Hongfeng Reservoir,
Guizhou, China. Environ. Pollut. 2008, 154, 56−67.
(65) Lin, T. Y.; Kampalath, R. A.; Lin, C.-C.; Zhang, M.; Chavarria,
K.; Lacson, J.; Jay, J. A. Investiagation of mercury methylation
pathways in biofilm versus planktonic cultures of Desulfovibria
desulfuricans. Environ. Sci. Technol. 2013, 47 (11), 5695−5702.
(66) Evans, M. S.; Lockhart, W. L.; Doetzel, L.; Low, G.; Muir, D.;
Kidd, K.; Stephens, G.; Delaronde, J. Elevated mercury concentrations
in fish in lakes in the Mackenzie river basin: The role of physical,
chemical, and biological factors. Sci. Total Environ. 2005, 351, 479−
500.
(67) Sellers, P.; Kelly, C. A.; Rudd, J. W. M. Fluxes of
methylmercury to the water column of a drainage lake: The relative
importance of internal and external sources. Limnol. Oceanogr. 2001,
46 (3), 623−631.
(68) Price, D. T.; Alfaro, R. I.; Brown, K. J.; Flannigan, M. D.;
Fleming, R. A.; Hogg, E. H.; Girardin, M. P.; Lakusta, T.; Johnston,
M.; McKenney, D. W.; Pedlar, J. H.; Stratton, T.; Sturrock, R. N.;
Thompson, I. D.; Trofymow, J. A.; Venier, L. A. Anticipating the
consequences of climate change for Canada’s boreal forest
ecosystems. Environ. Rev. 2013, 21 (4), 322−365.
(69) Ullrich, S. M.; Tanton, T. W.; Abdrashitova, S. A. Mercury in
the aquatic environment: A review of factors affecting methylation.
Crit. Rev. Environ. Sci. Technol. 2001, 31 (3), 241−293.
J DOI: 10.1021/acs.est.8b01680
Article
(70) Desrosiers, M.; Planas, D.; Mucci, A. Mercury methylation in
the epilithon of Boreal Shield aquatic ecosystems. Environ. Sci.
Technol. 2006, 40 (5), 1540−1546.
(71) Köhler, S. J.; Kothawala, D.; Futter, M. N.; Liungman, O.;
Tranvik, L. In-lake processes offset increased terrestrial inputs of
dissolved organic carbon and color to lakes. PLoS One 2013, 8 (8),
e70598.
(72) Lehnherr, I.; St.Louis, V. L. Importance of ultraviolet radiation
in the photodemethylation of methylmercury in freshwater
ecosystems. Environ. Sci. Technol. 2009, 43 (15), 5692−5698.
(73) Poste, A. E.; Braaten, H. F. V.; de Wit, H. A.; Sorensen, K.;
Larssen, T. Effects of photodemethylation on the methylmercury
budget of boreal Norwegian lakes. Environ. Toxicol. Chem. 2015, 34
(6), 1213−1223.
(74) French, T. D.; Houben, A. J.; Desforges, J. P. W.; Kimpe, L. E.;
Kokelj, S. V.; Poulain, A. J.; Smol, J. P.; Wang, X. W.; Blais, J. M.
Dissolved organic carbon thresholds affect mercury bioaccumulation
in arctic lakes. Environ. Sci. Technol. 2014, 48 (6), 3162−3168.
(75) Jolly, W. M.; Cochrane, M. A.; Freeborn, P. H.; Holden, Z. A.;
Brown, T. J.; Williamson, G. J.; Bowman, D. Climate-induced
variations in global wildfire danger from 1979 to 2013. Nat. Commun.
2015, 6, 7537.
(76) Fraser, A.; Dastoor, A.; Ryjkov, A. How important is biomass
burning in Canada to mercury contamination? Atmos. Chem. Phys.
2018, 18, 7263−7286.
(77) Kelly, E. N.; Schindler, D. W.; St. Louis, V. L.; Donald, D. B.;
Vladicka, K. E. Forest fire increases mercury accumulation by fishes
via food web restructuring and increased mercury inputs. Proc. Natl.
Acad. Sci. U. S. A. 2006, 103 (51), 19380−19385.
(78) Summers, J. C.; Kurek, J.; Kirk, J. L.; Muir, D. C. G.; Wang, X.
W.; Wiklund, J. A.; Cooke, C. A.; Evans, M. S.; Smol, J. P. Recent
warming, rather than industrial emissions of bioavailable nutrients, is
the dominant driver of lake primary production shifts across the
Athabasca oil sands region. PLoS One 2016, 11 (5), e0153987.
(79) Meng, B.; Feng, X. B.; Chen, C. X.; Qiu, G. L.; Sommar, J.;
Guo, Y. N.; Liang, P.; Wan, Q. Influence of eutrophication on the
distribution of total mercury and methylmercury in hydroelectric
reservoirs. J. Environ. Qual. 2010, 39 (5), 1624−1635.
(80) Allen, E. W.; Prepas, E. E.; Gabos, S.; Strachan, W. M. J.;
Zhang, W. P. Methyl mercury concentrations in macroinvertebrates
and fish from burned and undisturbed lakes on the boreal plain. Can.
J. Fish. Aquat. Sci. 2005, 62 (9), 1963−1977.
(81) Lescord, G. L.; Emilson, E. J. S.; Johnston, T. A.; Branfireun, B.
A.; Gunn, J. M. Optical properties of dissolved organic matter and
their relation to mercury concentrations in water and biota across a
remote freshwater drainage basin. Environ. Sci. Technol. 2018, 52 (6),
3344−3353.
(82) Graydon, J. A.; Emmerton, C. A.; Lesack, L. F. W.; Kelly, E. N.
Mercury in the Mackenzie River delta and estuary: Concentrations
and fluxes during open-water conditions. Sci. Total Environ. 2009, 407
(8), 2980−2988.
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