View Online / Journal Homepage Journal of Dynamic Article LinksC< Environmental Monitoring Cite this: DOI: 10.1039/c2em30132f www.rsc.org/jem PAPER Investigations of mercury concentrations in walleye and other fish in the Athabasca River ecosystem with increasing oil sands developments†

Marlene S. Evans*a and Andre Talbotb

Received 12th October 2011, Accepted 3rd May 2012 DOI: 10.1039/c2em30132f

Recent studies have reported an increasing trend of mercury concentrations in walleye (Sander vitreus) from the Athabasca River, north eastern Alberta (Canada); these studies were based on three years of comparison and attributed the mercury increase to expanding oil sands developments in the region. In order to conduct a more comprehensive analysis of mercury trends in fish, we compiled an extensive database for walleye, lake whitefish (Coregonus clupeaformis), northern pike (Esox lucius) and lake trout (Salvelinus namaycush) using all available data obtained from provincial, federal, and industry- funded monitoring and other programs. Evidence for increasing trends in mercury concentrations were examined for each species by location and year also considering fish weight and length. In the immediate oil sands area of the Athabasca River, mercury concentrations decreased (p < 0.001) in walleye and lake whitefish over 1984–2011. In western Lake Athabasca and its delta, mercury concentrations decreased (p < 0.0001) in northern pike (1981–2009) although no trend was evident for walleye (1981–2005) and lake trout (1978–2009). Mercury concentrations in lake trout from Namur Lake, a small lake west of the oil sands area, were higher in 2007 than 2000 (p < 0.0001); it is difficult to ascribe this increase to an oil sands impact because similar increases in mercury concentrations have been observed in lake trout from similar sized lakes in the Northwest Territories. While mercury emissions rates have increased with oil sands development and the landscape become more disturbed, mercury concentrations remained low in water and sediments in the Athabasca River and its tributaries

Downloaded by McGill University on 05 June 2012 and similar to concentrations observed outside the development areas and in earlier decades. Our fish database was assembled from a series of studies that differed in study purpose, design, and analytical Published on 31 May 2012 http://pubs.rsc.org | doi:10.1039/C2EM30132F methods. Future monitoring programs investigating mercury trends in fish should be more rigorous in their design.

Introduction aEnvironment Canada, Aquatic Ecosystem Protection Research Division, 11 Innovation Boulevard, Saskatoon, SK, S7N 3H5 Canada. E-mail: The extraction of oil from Alberta’s oil sands is a controversial [email protected]; Fax: +1-306-975-5143; Tel: +1-306-975-5310 activity, particularly open-pit mining.1–4 One concern is that bEnvironment Canada, Aquatic Ecosystem Protection Research Division, mining activities are resulting in a significant increase in metal 105 McGill Street, Montreal, QC, H2Y 2E7 Canada. E-mail: Andre. loading, including mercury, to the Athabasca River and its delta [email protected]; Fax: +1-514-283-1719; Tel: +1-514-283-2509 1,5 † Electronic supplementary information (ESI) available. See DOI: with a concomitant increase in mercury concentrations in fish. 10.1039/c2em30132f Specifically it was reported that mean mercury concentrations in

Environmental impact Anthropogenic activities redistribute mercury in the environment and can result in increased mercury concentrations in fish locally and over broad areas. There are concerns that with the expansion of the Alberta (Canada) oil sands operations since the late 1990s, mercury concentrations have increased in fish in the lower Athabasca River ecosystem. We assess all available data on mercury concentrations in four species of fish over this area and conclude that there is no evidence that mercury concentrations have increased in the majority of investigated fish populations. While mercury levels did increase between two time periods in lake trout in one lake, mercury levels also are increasing in lake trout in northern Canada with global events the apparent driver. Since the data which we analyzed were assembled from a series of studies with different designs, an improved monitoring system will be required to reach more definitive conclusions as oil sands developments continue.

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walleye (Sander vitreus) from the lower Athabasca River 3. Is there evidence that mercury concentrations in fish har- increased from 0.32 mgg1 in 1975, to 0.36 mgg1 in 1992 to 0.41 vested from the broader Athabasca River watershed over 2000– mgg1 in 2005 as a result of the expanding industry.5 However, 2011 are greater than mercury concentrations in fish collected in this study suffered from a number of limitations. The 1975 and the same areas in the 1970s, 1980s and 1990s? 1992 mercury means were based on sites situated along a more 4. Are mercury concentrations in surface sediments and water in than 200 km length of the Athabasca River from the Fort the Athabasca River, its tributaries and the Athabasca River delta McMurray area north to the Athabasca delta while mercury greater than mercury concentrations measured in the same areas in means in 2005 were based on sites sampled over a 40 km reach in the 1970s, 1980s and 1990s before the industry expanded? the immediate oil sands development area. The 1975 analyses We addressed these questions by first compiling a comprehensive were based on whole body fish whereas 1992 and 2005 analyses database for walleye (Sander vitreus), lake whitefish (Coregonus were based on fillet: mercury concentrations are lower in whole clupeaformis), northern pike (Esox lucius) and lake trout (Salvelinus fish than fillet.6 In addition, other variables such as individual namaycush) using all available data on mercury concentrations fish length and weight which are known to strongly influence obtained from provincial, federal, and industry-funded monitoring mercury concentrations in fish7 were not considered. Finally, the andotherprograms;additionaldatasuchasfishlengthandweight study considered only three years of mercury measurements were included as variables for analyses. We also examined historic when more data were available from the oil sands monitoring and recent mercury monitoring data (water and sediments) to program and other sources. assess changes in mercury concentrations in Athabasca River water Mercury concentrations in fish are influenced by many and sediments with the expanding oil sands industry. More features of their environment and their biology. Mercury comprehensive analyses of these sediment and water data are the concentrations vary with fish size, age, and trophic feeding; subject of manuscripts in preparation. where fish populations are old, slow growing, and piscivorous such fish can have high mercury concentrations which exceed the 0.5 mgg1, commercial sale guideline.7,8 Mercury transformations Methods from the inorganic to organic form are more conducive in Study area shallow, productive lakes with extensive watersheds than in large lakes. Therefore, predaceous fish living in shallow, productive The Athabasca River is part of the larger Mackenzie River Basin lakes tend to have higher mercury concentrations than fish living watershed originating in the Columbia ice fields and flowing in large, deep and cold lakes. When fish are exposed to effluents 1230 km north into western Lake Athabasca; the river length from various industries (e.g., gold extraction, chloro-alkali from Fort McMurray to Lake Athabasca is approximately plants, and pulp and paper bleaching) which use large quantities 300 km (Fig. 1). The lake outflow is a few tens of kilometers to of mercury in their processing and this mercury is methylated, the north where it joins the Peace River to form the Slave River fish can become highly contaminated.9 The release of high which then flows into Great Slave Lake, the headwaters of the concentrations of sulfur dioxide and nitrogen oxides in atmo- Mackenzie River. The Athabasca River historic flow below Fort Downloaded by McGill University on 05 June 2012 spheric emissions can result in the formation of ‘‘acid rain’’ which McMurray is 19 547 million m3 per year (19.5 km3 per year) with can in turn reduce the pH of poorly buffered lakes resulting in an tributary rivers (Mackay, Muskeg, Steepbank, Firebag, Ells and Published on 31 May 2012 http://pubs.rsc.org | doi:10.1039/C2EM30132F enhancement of mercury methylation rates; in such instances Tar rivers) contributing an additional 10% to the flow.16,17 mercury concentrations may be elevated in fish.10 Surface mining and oil sands extraction operations began in Mercury concentrations are commonly measured in commer- 1967 with Suncor’s first disturbance of the landscape occurring cial and sports fish by Canadian provincial and federal govern- northwest of Fort McMurray; this lease operation closed in 2002 ments and measurements are also required as part of many (Table 1). In 1973 Syncrude first disturbed the landscape for its industry monitoring programs. This monitoring is done because Mildred Lake operations located north of Suncor. Since 2000 mercury biomagnifies in food webs and, at high concentrations, there has been a northward expansion in oil sands activities with can have toxicological effects posing some risk to human open-pit mining occurring near the river where bitumen is close health.11–13 While the majority of these assessments are periodic, enough to the surface to be mined. In situ steam-assisted gravity there are a small number of long-term programs monitoring drainage (SAGD) extraction occurs elsewhere and has a smaller mercury trends in fish, e.g., the lake trout and walleye monitoring environmental footprint; this industry is expanding south of Fort program on the Great Lakes and the lake trout and burbot McMurray and to the east and west of the open-pit mining. monitoring program in the Northwest Territories.7,14,15 The amount of land surface disturbed by open pit mining has In this paper, we took a comprehensive approach in addressing been increasing with the expansion of the industry from 9600 ha the question as to whether mercury concentrations are increasing in 1980 to 71 500 ha in 2010 with the greatest rate of increase in fish in the Athabasca River watershed with the expansion of through the mid to late 2000s (Fig. 2, Government of Alberta18); the oil sands industry. Specifically we investigated: in 1974 the disturbed footprint may have been as small as 40 1. Is there evidence of an increase in mercury concentrations in ha.19 Mined bitumen must be heated to remove undesirable fish collected from the immediate oil sands area of the Athabasca solids and reduce its density and viscosity; the processing also River with the expansion of the oil sands industry through 2000– removes some sulfur, nitrogen and heavy metals.4 Water in the 2010? treatment is reused as oil sands process water or stored in 2. Is there evidence of an increase in mercury concentrations in tailings ponds. Suncor, as an earlier facility, is allowed to release fish collected 200 km downstream in the Athabasca River delta industrial waste water and runoff water which includes water with the expansion of the oil sands industry? from two of its coke settling ponds. This discharge, which has

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Mercury determinations in fish

Mercury concentrations have been determined periodically in walleye, lake whitefish, northern pike and lake trout (and other species) by various government agencies and as part of the oil sands monitoring program at various times over the past four decades. A brief description of their ecology is provided in the Electronic Supplementary Information (ESI)†. Data were obtained from reports or from electronic databases made avail- able to us; details are shown in Tables 2–5. In brief, these studies were as follows.

Early (1975–1993) mercury determinations in fish In August 1975, Lutz and Hendzel22 conducted a baseline study of mercury concentrations in fish at 16 locations extending over 250 km from just upstream (south) of Fort McMurray, down- stream (north) to Lake Athabasca and Lake Claire, and included tributary rivers and the Lake Athabasca outflow (Fig. 1). Mercury concentrations (whole fish) were determined in eight fish species, including walleye, northern pike, and lake whitefish; fish weight was measured. Total mercury concentrations were determined using the method of Hendzel and Jamieson23 and the standard for these analyses was based on a composite of previ- ously run fish. Data were reported as site means. In 1984, Moore et al.24 investigated mercury concentrations in nine species of fish from 24 lakes and rivers in Alberta. Walleye, lake whitefish and northern pike were sampled on the Athabasca River a few km downstream of Suncor, northern pike at a site in western Lake Athabasca, and walleye and northern pike at Christina Lake. Analytical methods were described in detail and are not repeated here; the laboratory participated in the year- round National Interlaboratory Mercury in Fish Quality

Downloaded by McGill University on 05 June 2012 Assurance program conducted four times a year by the Federal Department of Fisheries and Oceans (DFO). Data were reported

Published on 31 May 2012 http://pubs.rsc.org | doi:10.1039/C2EM30132F for individual fish including length (fork), wet weight, and mercury concentrations (dorsal fillet). Over the late 1970s to the mid 1990s the Fish Inspection Agency of DFO periodically assessed mercury concentrations in fish collected from across Canada. While this program has been discontinued, unpublished data were obtained from DFO. Analytical methods were reported by Lockhart et al.8 Mercury concentrations (fillet) were assessed in western Lake Athabasca trout, walleye, northern pike, lake trout and lake whitefish on 1 to 7 occasions, Christina Lake walleye and northern pike on 2–4 occasions and Jackson Lake northern pike on two occasions; fish length and weight also were measured. Data were reported for Fig. 1 Athabasca River and delta showing the sites sampled by Lutz and individual fish. 25 Hendzel,22 Donald et al.25 and RAMP.30 In 1992, Donald et al. determined mercury concentrations (fillet), weight, and fork length in walleye collected at three sites along the Athabasca River and in the same area as Lutz and Hendzel22,26 (Fig. 1). Data were reported as site means. been declining since the late 1990s (Fig S1†) is relatively small; in 2005 it was 15.1 m3 min1 or 0.00794 km3 year1, which Regional aquatic monitoring program in the oil sands area represents ca. 0.039% of the average annual flow of the Atha- (1998–2011) basca River below Fort McMurray.20 Bitumen is upgraded on site. Mercury is emitted to the atmosphere during this pro- With the expansion of the oil sands industry in the late 1990s, the cessing with estimated emission rates increasing from 22.8 kg in Regional Aquatic Monitoring Program (RAMP) was put in 2001 to 133 kg in 2010;21 this rate of increase has accelerated place to monitor water, sediments, fish and benthic invertebrates through the mid to late 2000s (Fig. 2). primarily in the Athabasca River and its tributaries. This

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Table 1 History and capacity of open-pit mining operations operating north of Fort McMurray and as reported in RAMP.17 Also shown is the history for in situ mines. * is the combined capacity for the Steepbank and Millennium mines

Company/development Capacity (barrels per day) Year of first disturbance 2010 status

Surface mining Suncor Energy Inc. Lease 86/17 280 000 1967 Closed in 2002 Steepbank mine 294 000* 1997 Operational Millennium mine * 2000 Operational Steepbank debottleneck phase 3 4000 2007 Operational North Steepbank mine extension 180 000 2007 Operational Millennium debottling 23 000 2008 Operational Syncrude Mildred Lake and Aurora stages 1 and 2 290 700 1973 Operational Mildred Lake and Aurora stage 3 116 300 2006 Operational Shell Canada Muskeg River mine 155 000 2000 Operational Jackpine mine phase 1A 100 000 2006 Operational Canadian natural resources Horizon phase 1 110 000 2004 Operational Imperial oil Kearl Lake phase 1 110 000 2009 Construction In situ mining Suncor Energy Inc. Firebag phases 1 and 2 95 000 2002 Operational Firebag phase 3 52 500 2004 Construction MacKay River 33 000 2000 Operational Nexen Inc. Long Lake 72 000 2003 Operational Husky Energy Sunrise 200 000 2007 Construction Conoco Phillips Canada Surmont phase 1 27 000 2004 Operational Surmont phase 2 83 000 2010 Construction Devon Energy Corp Jackfish phase 1 35 000 2005 Operational Jackfish phase 2 35 000 2008 Construction MEG Energy Corp Christina Lake phase 1 3000 2005 Operational Christina Lake phase 2 22 000 2007 Operational Downloaded by McGill University on 05 June 2012 Published on 31 May 2012 http://pubs.rsc.org | doi:10.1039/C2EM30132F

concentrations were determined in walleye and lake whitefish on five occasions along ca. 7.5 km long reaches of the Athabasca River in the vicinity of the Steepbank and Muskeg River outflows, northern pike from the Muskeg River on three occa- sions, northern pike from the Clearwater River on four occasions and walleye on one occasion; Lake Claire located in the Peace– Athabasca delta was sampled once (Fig. 1). Mercury concentrations also were measured in fish from various lakes often as part of Alberta Sustainable Resource Department’s stock assessment programs. Thirty-five to 150 km to the south, mercury concentrations were measured in northern pike and walleye from Christina Lake and pike, Fig. 2 Disturbed landscape by oil sands activities over 1987–2010 and walleye, and whitefish from Winefred and Gregoire Lakes. mercury emissions over 2000–2010. Data from Richens (personal Fifty to sixty km to the west, mercury concentrations were communication) and Environment Canada.44 measured in lake trout from Namur Lake and whitefish, walleye and northern pike from Gardiner Lake and Big Island Lakes. Sixty five to ninety km to the northeast, mercury program has included periodic determinations of mercury concentrations were measured in lake whitefish, northern pike concentrations in fish from the Athabasca River, tributaries or and walleye from Jackson, Net, Keith and Brutus Lakes; nearby lakes for details and primary data see ref. 27. Prior to mercury measurements were based on fillet. Most sampling was 2002, analyses were conducted on a composite of fish fillet, conducted only once. whereas fillet from individual fish were analyzed in later years. Up to 2005, RAMP mercury analyses were based on fillet with Fork length and weight were routinely measured. Mercury analyses using EPA 200.3/200.8-ICP-MS methodology.28 In

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Table 2 Mean (1 standard deviation) length, weight and mercury concentrations in walleye in the lakes and rivers in the Fort McMurray oil sands area and the Peace–Athabasca delta (PAD) and western Lake Athabasca; Quatre Forches from the lake outflow. Ranges are given for Lutz and Hendzel22 for weight. See Fig. 1 for site locations. Analyses are on fillet except where noted. Two data sets are reported for the Steepbank and Muskeg reaches of the Athabasca River in 2005. The first is based on all walleye analyses in 2005 and downloaded from RAMP.27 The second is based only of fish which could be sexed and is from Table 5. 1–11 in available data RAMP.30 N refers to the number of fish collected. n.d. refers to No data. See text for further explanation

Location Year N Length (mm) Weight (g) Mercury (mgg1) Study

Athabasca R. oil sands Station 8a 1975 11 n.d. 620 (190–1700) 0.27 0.10 Lutz and Hendzel22 Station 9a 1975 17 n.d. 740 (300–1280) 0.29 0.12 Lutz and Hendzel22 Site 11 at Horse R. Moutha 1975 6 n.d. 990 (410–2340) 0.43 0.20 Lutz and Hendzel22 Site 12, Muskeg R. moutha 1975 4 n.d. 1000 (760–1370) 0.38 0.17 Lutz and Hendzel22 Site 13 Mackay R. Moutha 1975 2 n.d. 1260 (1020–1500) 0.36 0.18 Lutz and Hendzel22 Suncor 1984 21 440.5 88.4 936.7 571.0 0.43 0.30 Moore et al.24 Km 230 1992 3 386 654.3 405.3 0.29 0.03 Donald et al.25 Km 300 1992 10 377.3 467.0 173.2 0.27 0.09 Donald et al.25 Steepbank reach – springb 1998 10 448.2 37.0 935.5 277.2 0.25 0.06 RAMP58 Steepbank reach – fallb 1998 13 460.8 77.0 1208.5 658.3 0.30 0.07 RAMP58 Steepbank, McLean, 2001 10 498.8 68.5 1510.5 653.8 0.41 0.07 RAMP59 Donaldb Steepbank & Muskeg 2002 25 400.0 110.6 830.1 596.1 0.36 0.22 RAMP60 reaches Steepbank & Muskeg 2003 25 437.5 88.4 1040.9 690.2 0.39 0.17 RAMP28 reaches Steepbank & Muskeg 2005 28 435.7 118.7 1126.7 835.6 0.37 0.23 RAMP30 reaches Steepbank & Muskeg 2005 25 464.5 102.3 1288.6 791.8 0.41 0.21 RAMP30 reaches Steepbank & Muskeg 2008 26 416.4 84.1 885.4 594.3 0.27 0.16 RAMP61 reachesc Steepbank & Muskeg 2011 31 455.0 78.5 1069.4 488.8 0.34 0.18 RAMP62 reaches Other rivers Clearwater River 2004 2 440.5 88.4 936.7 571.0 0.40 0.15 RAMP29 PAD and Lake Athabasca Lake Athabasca 1977 5 391.1 54.3 1006.0 508.5 0.52 0.23 DFO63 Lake Athabasca 1981 45 399.8 34.6 862.1 224.2 0.29 0.11 DFO63 Lake Athabasca 1988 8 389.5 16.9 762.8 68.3 0.34 0.10 DFO63 Lake Athabasca 1989 5 391.8 19.5 679.0 109.6 0.34 0.06 DFO63 Lake Athabasca 1991 10 405.1 40.0 951 285.8 0.33 0.15 DFO63 Downloaded by McGill University on 05 June 2012 Lake Athabasca 1992 15 389.7 33.6 1096.4 269.5 0.31 0.09 DFO63 Lake Athabasca 1993 5 418.7 29.8 1088.0 244.1 0.42 0.06 DFO63 Published on 31 May 2012 http://pubs.rsc.org | doi:10.1039/C2EM30132F Richardson Lake site 4a 1975 4 n.d. 990 (410–2340) 0.17 0.10 Lutz and Hendzel22 Richardson Lake 2005 20 461.7 50.0 962.0 303.1 0.38 0.21 Hatfield Consultants33 Lake Claire 2003 2 445.0 77.8 1131.0 359.2 0.20 0.02 RAMP28 Old Fort Bay 2005 5 491.0 31.7 1411.0 294.1 0.38 0.21 Hatfield Consultants33 Athabasca R. Site 5a 1975 14 n.d. 1140 (600–2250) 0.38 0.12 Lutz and Hendzel22 Athabasca R. 1992 9 478.6 1060.7 352.4 0.38 0.08 Donald et al.25 Quatre Forchesa 1975 1 n.d. 190 0.11 Lutz and Hendzel22 Lakes Christina Lake 1982 5 417.0 11.7 1414.0 165.5 0.38 0.20 DFO63 Christina Lake 1987 20 355.4 102.5 1063.4 843.3 0.32 0.26 DFO63 Christina Lakeb 2003 13 536.8 71.1 2011.5 902.4 0.41 0.17 RAMP28 Winefred Lake 2004 24 438.2 148.3 1450.4 1300.0 0.13 0.07 RAMP29 Gregoire Lake 2002 27 399.2 132.2 911.8 770.2 0.13 0.10 RAMP60 Gregoire Lake 2007 21 401.9 124.5 953.2 713.0 0.16 0.12 RAMP64 Big Island Lake 2008 20 375.0 103.2 990.9 1025.4 0.08 0.05 RAMP61 Gardiner Lake 2008 31 455.5 150.7 1538.0 1215.4 0.29 0.18 RAMP61 Jackson Lakec 2009 22 425.2 129.4 1105.7 925.6 0.21 0.13 RAMP65 Brutus Lakec 2010 19 370.1 100.1 585.8 442.7 0.30 0.14 RAMP17 Net Lakec 2010 19 363.0 97.4 636.2 461.1 0.67 0.32 RAMP17 a Whole body. b Composite determinations. c Tissue plugs.

2004, mercury measurements were made on a subset of fillet River.30 Analyses conducted after 2006 were performed using the and fillet plug samples using northern pike sampled from the CVAFS method and used either fillet or tissue plugs. Commer- Clearwater River; these analyses were performed using cold cial laboratories were used to conduct these analyses; RAMP vapor atomic fluorescence spectrophotometry (CVAFS) requires that all its laboratories be accredited by the Canadian methods.29 A similar comparative study was conducted in 2005 Association for Environmental Analytical Laboratories using lake whitefish and walleye caught from the Athabasca (CAEL).

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Table 3 Mean (1 standard deviation) length, weight and mercury concentrations in lake whitefish in the lakes and rivers in the Fort McMurray oil sands area and the Peace–Athabasca delta (PAD) and western Lake Athabasca. Ranges are given for Lutz and Hendzel22 for weight. See Fig. 1 for site locations. Analyses are on fillet except where noted. N refers to the number of fish collected. n.d. refers to No data

Location Year N Length (mm) Weight (g) Mercury (mgg1) Study

Athabasca R. oil sands Station 8a 1975 15 n.d. 1040 (510–1890) 0.11 0.04 Lutz and Hendzel22 Station 9a 1975 13 n.d. 840 (440–1170) 0.09 0.04 Lutz and Hendzel22 Suncor area 1984 10 388.2 32.3 888.2 219.0 0.08 0.04 Moore et al.24 Steepbank reachb 1998 7 430.6 28.6 1149.0 275.1 0.09 0.01 RAMP58 Steep. to Ft. McMurrayb 2001 10 450.0 25.4 1407.5 167.9 0.11 0.00 RAMP59 Steep. & Muskeg reaches 2002 25 429.1 34.4 1241.4 285.5 0.13 0.10 RAMP60 Steep. & Muskeg reaches 2003 25 443.8 46.2 1476.5 487.1 0.10 0.04 RAMP28 Steep. & Muskeg reaches 2005 26 439.6 49.1 1375.2 527.2 0.09 0.04 RAMP30 Steep. & Muskeg reaches 2008 20 396.6 43.1 964.5 299.8 0.05 0.04 RAMP61 Steep. & Muskeg reaches 2011 24 435.3 43.1 1267.3 400.2 0.08 0.05 RAMP62 PAD and Lake Athabasca Athabasca delta 1977 3 343.3 5.8 585.0 15.0 0.10 0.06 DFO63 Lake Athabasca 1981 10 455.9 29.2 1075.9 198.2 0.05 0.02 DFO63 Lake Athabasca 2000 6 352.4 35.2 560.8 96.2 0.07 0.03 Evans40 Lake Clairea 1975 3 n.d. 470 (120–790) 0.07 0.03 Lutz and Hendzel22 Lake Claire 2003 2 715.0 162.6 1063.5 587.6 0.11 0.06 RAMP28 Richardson Lakea 1975 39 620 (30–1520) 0.07 0.04 Lutz and Hendzel22 Richardson Lake 2005 21 396.1 37.3 1075.2 322.6 0.06 0.02 Hatfield Consultants33 Old Fort Bay 2005 26 371.7 45.7 766.5 313.0 0.08 0.04 Hatfield Consultants33 Lakes Gregoire Lake 2002 12 491.3 2.1 2187.5 35.4 0.04 0.02 RAMP60 Gregoire Lake 2007 13 452.1 69.9 1364.5 635.4 0.04 0.01 RAMP64 Christina Lakeb 2003 13 450.6 63.9 1294.3 627.7 0.10 0.06 Winefred Lake 2004 18 451.9 51.3 1260.8 394.1 0.08 0.05 RAMP29 Big Island Lake 2008 16 381.9 103.7 928.5 599.3 0.03 0.01 RAMP61 Gardiner Lake 2008 14 414.4 60.7 1158.9 513.3 0.07 0.03 RAMP61 Jackson Lakec 2009 17 386.9 76.7 1260.9 860.9 0.04 0.03 RAMP65 Brutus Lakec 2010 12 362.1 51.0 553.6 180.3 0.11 0.04 RAMP17 Keith Lakec 2010 11 322.3 59.2 420.0 229.5 0.04 0.02 RAMP17 Net Lakec 2010 8 373.3 69.1 862.9 462.0 0.12 0.05 RAMP17 a Whole body. b Composite determinations. c Tissue plugs.

Downloaded by McGill University on 05 June 2012 Other studies of mercury in fish (2000–2010) measured and therefore not considered in our analyses. Arithmetic means and standard deviations were calculated for each species by Published on 31 May 2012 http://pubs.rsc.org | doi:10.1039/C2EM30132F In 2000, mercury concentrations were determined in lake trout location and year. Next, mean mercury concentrations for each from Namur Lake (October) and western Lake Athabasca species and location were examined for obvious time trends, i.e., (March) as part Environment Canada studies investigating were mean mercury concentrations changing over time? While 1975 spatial patterns in contaminant biomagnification in northern data are based on whole body analyses and later data were based Canada.7,31 Concentrations were determined in dorsal muscle 23 on fillet, the former data were given less weight in our comparisons following the method of Hendzel and Jamieson Lake trout were 6 as mercury concentrations are lower in whole fish body than fillet. collected from western Lake Athabasca over 2007–2009 as part Since different size fish were measured in different years, compar- of a larger project investigating flame retardants in lake trout32 isons had to be based on fish of similar sizes, e.g., mean mercury and northern pike from Richardson Lake in 2009: collections concentrations in walleye of an average weight of ca. 1000 g were generally were made in March. Fish length (total and fork), compared across years with similar comparisons made with fish of weight and age were determined. Mercury concentrations were smaller weights. Such comparisons were somewhat subjective and determined by CVAFS methods. lacked rigor but were useful for considering major and/or consis- In August 2005, Hatfield Consultants33 assessed mercury tent trends in mercury concentrations with time. Similarly, spatial concentrations in walleye, lake whitefish and northern pike from patterns in mercury concentrations in fish caught in lakes over Richardson Lake and Old Fort Bay. Fish length (total and fork), 2000–2010 can be compared with spatial patterns observed in lakes weight and age were determined. Analyses were conducted by in earlier times. CVAFS methods and by the same laboratory used by RAMP. Analysis of variance (General Linear Model, GLM) was per- formed to investigate trends in mercury concentrations. Length and year were the independent variables and log Hg the Data analyses 10 dependent variable; a length–year interaction also was included. Data were compiled into Excel files and organized by fish species, Data collected in 1975 were not suitable for such analyses as data location, and year and included mercury concentration, length, and were reported as site means and not individual fish. Only a few weight for individual fish with the exception of Lutz and Hendzel22 locations for each species had a sufficient database to merit where original data consisted of site means. Fish age was seldom statistical time trend analyses. These were as follows.

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Table 4 Mean (1 standard deviation) fork length, weight and mercury concentrations in northern pike in the lakes and rivers in the Fort McMurray oil sands area and the Peace–Athabasca delta (PAD) and western Lake Athabasca. Ranges are given for Lutz and Hendzel22 for weight. See Fig. 1 for site locations. Analyses are on fillet except where noted. N refers to the number of fish collected. n.d. refers to No data

Location Year N Length (mm) Weight (g) Mercury (mgg1) Study

Athabasca R. oil sands Suncor area 1984 3 522.0 92.8 1108.7 666.3 0.28 0.16 Moore et al.24 Other rivers Muskeg Rivera 1975 9 550 (140–1460) 0.08 0.02 Lutz and Hendzel22 Muskeg Riverb 2001 10 606.4 28.6 1720.0 311.1 0.13 0.01 RAMP59 Muskeg River 2002 6 344.2 185.4 515.0 536.4 0.11 0.09 RAMP60 Muskeg River 2004 5 545.2 39.2 1180.0 270.1 0.22 0.03 RAMP28 Clearwater Rivera 1975 1 n.d. 390 0.10 Lutz and Hendzel22 Clearwater Rivercd 2004 13 566.6 141.0 1590.3 1274.6 0.20 0.14 RAMP29 Clearwater Riverb 2006 26 481.2 168.4 560.5 716.4 0.18 0.09 RAMP66 Clearwater Riverb 2007 34 510.4 180.9 1402.8 1402.8 0.15 0.13 RAMP64 Clearwater Riverb 2009 30 466.7 137.2 801.2 653.6 0.13 0.05 RAMP65 PAD and Lake Athabasca Lake Clairea 1975 23 1000 (250–3450) 0.22 0.06 Lutz and Hendzel22 Lake Claire 2003 3 613.3 180.4 2358.0 957.5 0.42 0.25 RAMP28 Athabasca delta 1977 1 585.2 1500 0.20 DFO63 Lake Athabascaa 1975 28 n.d. 1070 (80–2500) 0.19 0.06 Lutz and Hendzel22 Lake Athabasca 1981 10 608.7 42.3 1779.4 411.6 0.28 0.11 DFO63 Lake Athabasca 1984 10 614.8 98.0 2000.1 082.5 0.29 0.06 DFO63 Richardson Lakea 1975 32 1440 (100–5220) 0.15 0.08 Lutz and Hendzel22 Richardson Lake 2005 11 661.5 105.72 2117.8 956.6 0.25 0.20 Hatfield Consultants33 Richardson Lake 2009 20 733.2 104.1 3347.0 1604.5 0.28 0.12 Evans40 Old Fort Bay 2005 7 802.0 180.7 4657.1 2155.4 0.55 0.28 Hatfield Consultants33 Lakes Christina Lake 1982 4 649.6 34.6 2525.3 498.6 0.49 0.08 DFO63 Christina Lake 1984 8 586.1 126.3 2010.4 1656.8 0.27 0.19 DFO63 Christina Lake 1993 5 649.8 84.1 2373.6 821.3 0.53 0.19 DFO63 Christina Lake 1995 5 625.8 111.9 2366.4 820.7 0.45 0.12 DFO63 Christina Lakeb 2003 13 699.1 149.7 2962.3 2345.8 0.42 0.15 RAMP28 Winefred Lake 2004 10 626.6 88.0 1940.0 779.5 0.09 0.03 RAMP29 Gregoire Lake 2002 25 506.4 177.6 1092.0 1301.1 0.15 0.16 RAMP60 Gregoire Lake 2007 26 540.4 155.0 1184.6 941.9 0.21 0.17 RAMP64 Big Island Lake 2008 12 557.0 58.9 1453.8 595.1 0.08 0.02 RAMP61 Gardiner Lake 2008 11 642.0 61.4 2040.5 660.4 0.19 0.07 RAMP61 Jackson Lake 1978 8 558.9 50.9 1244.3 263.8 0.26 0.12 DFO63 Jackson Lake 1987 10 513.5 51.8 1261.7 369.0 0.35 0.19 DFO63 Downloaded by McGill University on 05 June 2012 Jackson Lakec 2009 1 323 220.0 0.05 RAMP65 Brutus Lakec 2010 8 559.5 44.4 1163.8 291.5 0.36 0.08 RAMP17 Published on 31 May 2012 http://pubs.rsc.org | doi:10.1039/C2EM30132F Keith Lakec 2010 4 531.8 68.0 972.5 485.3 0.08 0.03 RAMP17 Net Lakec 2010 8 517.5 74.6 922.5 397.4 0.49 0.27 RAMP17

a Whole body. b Composite determinations. c Tissue plugs. d Fillet measurements by Flett; fillet analyses by ELS ¼ 0.35 0.21 mgg1; fillet analyses by Flett ¼ 0.24 0.14 (mgg1).

For the Athabasca River in the immediate oil sands area, three sites a few kilometers downstream of Suncor oil sands a sufficient database existed for mercury trend analyses based on operations possibly due to a combination of acid conditions results for walleye and lake whitefish (Tables 2 and 3). The first created by leaching from sulfur pits and mercury releases from coke series of analyses investigated time trends in mercury concentra- storage piles; while there was no evidence that these localized tions in walleye and lake whitefish over 1984–2008. A second run elevated mercury concentrations in benthos had affected mercury was performed with 1984 data excluded. In 1983, mercury concentrations in fish25 it was prudent to conduct a second trend concentrations were elevated in benthic invertebrates collected at analyses with these data excluded. Following remedial actions, by

Table 5 Mean (1 standard deviation) length, weight and mercury concentrations in lake trout in the lakes in the Fort McMurray oil sands area and western Lake Athabasca. Ranges are given for Lutz and Hendzel22 for weight. See Fig. 1 for site locations. Analyses are on fillet

Location Year N Fork length (mm) Weight (g) Mercury (mgg1) Study

Lake Athabasca 1978 5 520.0 13.8 1840.8 217.6 0.22 0.12 DFO63 Lake Athabasca 2000 20 738.7 59.2 4623.1 1416.9 0.27 0.07 Evans et al.7 Lake Athabasca 2007 10 681.6 69.9 3519.2 1234.1 0.31 0.07 Evans40 Lake Athabasca 2008 20 647.9 43.6 3056.5 554.3 0.30 0.08 Evans40 Lake Athabasca 2009 20 651.0 28.4 3077.1 562.2 0.24 0.61 Evans40 Namur Lake 2000 18 573.0 18.1 2396.2 238.3 0.27 0.03 Evans et al.7 Namur Lake 2007 16 555.8 20.0 1794.4 181.5 0.45 0.05 Evans40

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1994 mercury concentrations in benthos in this localized area were were subjected to three series of mercury analyses, i.e.,filletanal- the same as in upstream areas.25 Analysis of variance also was yses using two different laboratories and plug analyses using one of conducted for northern pike from the Clearwater River; northern the two laboratories. Pike analyses in 2006, 2007 and 2008 were pike, walleye, and lake trout from western Lake Athabasca; lake based on plugs. Mean mercury (plugs) concentrations (Table 4) trout data from Namur Lake; and whitefish, pike and walleye from ranged from 0.13 mgg1 in 2009 (average length 466.6 mm) to Gregoire Lake. 0.20 mgg1 in 2004 (566.6 mm fish). Variations in mercury concentration were explained only by fish length (Table 6). Mean mercury concentrations in northern pike fillet from the Results Muskeg River (Table 4) ranged from 0.11 mgg1 (2002) to m 1 Mercury concentrations and time trends in fish from the oil sands 0.22 gg (2004); 2001 analyses are based on two composite area of the Athabasca River and its tributaries samples. Smaller fish were sampled in 2002 than 2004 and sample size was small. Overall, data are insufficient to statistically assess Mean mercury concentrations in walleye (fillet) collected in the trends in mercury concentrations in pike in the Muskeg River. immediate oil sands area (Table 2) ranged from 0.27 mgg1 (1992 and 2008) to 0.43 mgg1 (1984) with higher mercury concentra- Mercury concentrations and time trends in fish in western Lake tions tending to be associated with years in which heavier fish Athabasca River and delta were analyzed. There was a significant (p < 0.001) decreasing trend in mercury concentrations based on both the 1984–2011 Mercury concentrations in walleye (whole body) were higher in and 2002–2011 time series: fish length also contributed to the 1975, when only five large (1006 g) fish were analyzed, than in the variance in mercury concentration (Table 6). Using log mercury seven later years of study including 1993 when the fillet of larger length regressions developed for each year and a median fish fish were analyzed (Table 2). Variations in mercury concentration length of 432 mm, length adjusted mercury concentration was in walleye from western Lake Athabasca and Richardson Lake 0.35 mgg1 in 1984, 0.32 mgg1 in 2002, 0.33 mgg1 in 2003, over 1981–2005 were explained only by fish length (Table 6). 0.28 mgg1 in 2005, 0.25 mgg1 in 2008 and 0.27 mgg1 in 2011. While mercury concentrations were measured in lake whitefish Mean mercury concentrations in lake whitefish fillet ranged fillet in western Lake Athabasca and its delta on four occasions from 0.05 mgg1 in 2008 to 0.13 mgg1 in 2002; higher mercury over 1981–2005, the database is insufficient (i.e., data reported as concentrations tended to be associated with years in which site means, small numbers of fish analyzed in later years) for heavier fish were analyzed (Table 3). There was a significant (p < assessing time trends with the expansion of the oil sands industry 0.001) decreasing trend in mercury concentrations based on (Table 3). However, mercury concentrations in lake whitefish in 2002–2011 and 1984–2011 analyses (Table 6). Richardson Lake and Old Fort Bay in 2005 were generally Lutz and Hendzel measured whole body mercury concentration similar to concentrations observed in earlier years for fish of in one small (390 g) northern pike from the Clearwater River in similar mean weights suggesting no major change. 1975. In fall 2004, 13 pike were investigated from this location as Mean mercury concentrations in northern pike fillet from Downloaded by McGill University on 05 June 2012 part of the RAMP tissue monitoring program. These collections western Lake Athabasca were similar over 1981, 1984, 2005, and

Published on 31 May 2012 http://pubs.rsc.org | doi:10.1039/C2EM30132F Table 6 Multiple regressions describing variations in walleye and mercury (Hg) concentrations in the Fort Murray oil sands area where Y ¼ year, L ¼ fork length (mm), W ¼ weight (g) and A ¼ age (year). Data are from Moore et al.24 and RAMP (2003, 2004, 2005 and 2008). Also shown is northern pike (1981, 1984 and 2009) from western Lake Athabasca and delta and lake trout from Namur Lake (2000, 2007). R is the coefficient of determination. See text for additional explanation

Years Regression nR2 Fp

Athabasca R. Walleye 1984–2008 log Hg ¼ 9.8214 0.0056Y + 0.0020L 154 0.47 67.89 <0.0001 2002–2008 log Hg ¼ 25.279 0.01330Y + 0.0020L 134 0.51 69.27 <0.0001 Lake Whitefish 1984–2011 log Hg ¼ 12.0966 0.0071Y + 0.0023L 130 0.19 14.58 <0.0001 2002–2011 log Hg ¼ 44.807 0.0233Y + 0.00019L 120 0.23 17.79 <0.0001 Clearwater R Northern pike (2004–2009) log Hg ¼1.4120 + 0.0011L 94 0.56 117.70 <0.0001 L. Athabasca Northern pike 1981–2009 log Hg ¼ 12.0616 0.0067Y + 0.0011L 49 0.64 40.19 0.0001 Walleye 1981–2005 log Hg ¼ 1.2082 + 0.001L 103 0.20 25.72 <0.0001 Namur Lake Lake trouta (2000, 2007) log Hg ¼153.35 + 0.076Y 16 0.91 142.58 <0.0001 Gregoire L. (2002, 2007) Whitefish log Hg ¼2.5640 + 0.0024L 24 0.59 31.26 <0.0001 Pike log Hg ¼2.11491 + 0.0024L 50 0.82 224.90 <0.0001 Walleyeb log Hg ¼ 26.9511 0.0143Y + 0.0014L 24 0.80 42.35 <0.0001 a Large trout (>527 mm). b Small walleye (<433 mm).

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2009; however, fish length and weight increased over the three study years (Table 4). Variations in mercury concentration were explained by year and fish length; the regression (Table 6) was significant at p ¼ 0.001. Estimated mean mercury concentration for a 657 mm pike was 0.34 mgg1 on 1981, 0.30 mgg1 in 1984, 0.18 mgg1 in 2005 and 0.21 mgg1 in 2009. Mercury concentrations in lake trout fillet from western Lake Athabasca were highly variable in 1978 although fish size was not (Table 5). The five fish analyzed for mercury in 1978 were smaller (and heavier) than fish caught in 2000–2009 and thus were not included in trend analyzes. No factor explained overall vari- ability in mercury concentrations over 2000–2009. Fig. 3 Measured mercury concentrations (1975 – whole body; 1992, 2005 fillet) and weight for walleye caught in the lower Athabasca River Mercury time trends on walleye based only on 1975, 1992, and 22 25 2005 studies and delta as reported by Lutz and Hendzel (whole body), Donald et al. and RAMP.30 Fillet measurements for 1975 walleye estimated from While Timoney and Lee5 reported that mean mercury concen- walleye regression provided by Peterson et al.6 trations in walleye in the lower Athabasca River increased from 1975 to 1992 to 2005, we did not observe such a trend in our more concentrations, the estimated mean mercury concentration in the m 1 comprehensive analyses which included more data and was based fillet of walleye collected in 1975 was 0.61 gg which is higher than the measured mercury concentrations in the 1992 and 2005 on a site specific approach. They also did not consider fish 34 weight. Therefore, we repeated their analyses using the same caught fish. If USEPA’s conversion factor of: fillet mercury ¼ approach and sites that appear to have been used in generating concentration whole body mercury concentration/0.7 is used, m 1 their mean mercury concentrations but we also considered fish the estimated fillet mercury concentration is lower at 0.46 gg . weight, i.e., was the increase in mercury concentration associated These comparisons can be extended by considering walleye data collected in the oil sands area of the Athabasca River. In this with increasing fish weight? 22 With a n ¼ 59 for the Lutz and Hendzel22 study, we assume instance, sites 8, 9, 11, 12, and 13 from Lutz and Hendzel are used m 1 that average mercury concentrations were based on the 59 to develop a weighted mean mercury concentration (0.32 gg ) walleye collected at Quatre Forches and sites 4, 5, 8, 9, 11, 12, and fish weight (797 g) and sites 230 km and 300 km from Donald 25 ¼ m 1 and 13 (Table 2), i.e., at sites extending over more than 300 km of et al. (weighted mean mercury concentration 0.27 gg and fish weight ¼ 510 g). Mercury concentration in fillet for 1975 the Athabasca River from the Fort McMurray area north to the 6 Athabasca delta and Lake Athabasca outflow (Fig. 1). The caught fish was again estimated from Peterson et al. Heavier fish weighted mean mercury concentration for walleye collected from were collected over 1998–2011 than in 1975, 1984 and 1992 Downloaded by McGill University on 05 June 2012 these eight sites was 0.32 mgg1 and weighted mean fish weight (Fig. 4a). However estimated fillet mercury concentration in 1975 was 880.9 g. Mean mercury concentration was based on whole and measured mercury concentrations in 1984 fish were higher than Published on 31 May 2012 http://pubs.rsc.org | doi:10.1039/C2EM30132F body measurements rather than fillet. in later years; over 1992–2011, there was a general tendency for With a reported n ¼ 12 for 1992,5 average mercury concentra- higher mercury concentrations to be associated with years in which tions in walleye must be based on the nine fish collected from site fish were heavier (Fig. 4b). The regression of fish weight and 2 ¼ 35 km and the three walleye from site 230 km of the Athabasca mercury concentrations was significant for 1992–2011 data (R ¼ ¼ ¼ River but not the ten walleye from site 300 km (Table 2), i.e. over 0.48; f 6.59, p 0.04) for 1992–2011 data but not significant (p a slightly shorter 195 km length of the Athabasca River than the 0.09) when 1984 data were included (Fig. 4c); mean mercury Lutz and Hendzel22 study. While the weighted mean mercury concentration was above the 95% confidence interval for the 1992– concentration for walleye increased to 0. 36 mgg1 in 1992 (fillet), 2011 regression. Estimated mercury concentration in walleye fillet weighted mean fish weight also increased to 959.3 g in 1992. for fish caught in 1975 were even further outside the 95% prediction With a reported n ¼ 25 for 2005 walleye,5 the average mercury interval for the mercury-weight regression. concentration (fillet) of 0.41 mgg1 is based on walleye collected along the Steepbank and Muskeg River reaches of the Athabasca Mercury concentrations and time trends in fish from other lakes which could be sexed (Table 2). These fish had an average weight of 1288.6 g. Mercury concentrations were measured in whitefish, pike and Synthesizing these calculations, while mean mercury concen- walleye in Gregoire Lake in 2002 and again in 2007 (Tables 2–4). tration in walleye increased over three years of sampling so did Overall, larger whitefish were collected in 2007 than 2002: varia- fish weight (Fig. 3). Since mercury concentration increases with tions in mercury concentration in whitefish were explained only by fish weight, we cannot dismiss the possibility that the reported5 length (Table 6). Larger pike also were collected in 2007 than 2002. increasing trend in walleye mean mercury concentrations was Variations in mercury concentrations in pike were explained by strongly related to the increasing size of fish being sampled in length (Table 6) for 216–775 mm pike; a 1190 mm pike (0.81 mgg1 successive years. Furthermore, mean mercury concentrations of Hg), identified as an outlier in the GLM, was not included in the walleye in 1975 were based on whole body whereas 1992 and analyses. There was a significant (p < 0.05) length and year inter- 2005 analyses were based on fillet. Using the walleye regression action for mercury concentrations in walleye and so fish were developed by Peterson et al.6 for body versus fillet mercury dividedintotwosizegroups.Variationinmercuryconcentrationin

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small (<433 mm) walleye was explained by year (a decrease) and length (Table 6). The year–length interaction persisted for large fish with a positive log Hg versus length slope for 2002 fish and a negative slope for 2007 fish. Mean mercury concentrations (fillet) in walleye and northern pike sampled in Christina Lake (Tables 2 and 4) were similar in 1982, 1987, and 2003 and exhibited no trend of increase. Mercury concentrations were measured in northern pike on four occasions with the most recent, 2003, being based on two composite fish which precluded their use in statistical analyses. Visual inspec- tion of mean mercury concentrations and fish size revealed no evidence of a trend (Table 4). Mercury concentrations were higher in lake trout from Namur Lake in 2007 than 2000 (Table 5). There was a significant inter- action between trout length and mercury concentrations. Therefore, analyses were conducted for small (<527 mm) and large (>527 mm) fish, median length was used to separate large and small fish. Mercury concentrations were greater (p < 0.0001) in large fish between the two years (0.36 0.16 mgg1 in 2000 and 0.33 0.18 mgg1 in 2007) of study (Table 6). Other determinations of mercury concentrations in walleye, northern pike, and lake whitefish over 2000–2010 were performed too infrequently for statistical analyses to be conducted; mercury concentrations in these fish were similar to mercury concentrations in the same species collected from western Lake Athabasca and its delta which is under a strong Athabasca River influence.

Comparisons with mercury concentrations in fish in the Northwest Territories Mercury concentrations in the fish investigated in this study were low; concentrations observed in the 1980s generally were similar to concentrations observed in the 2000s when similar size fish Downloaded by McGill University on 05 June 2012 were compared. Since the study region consists of wide expanses of boreal forest and muskegs with a low human population Published on 31 May 2012 http://pubs.rsc.org | doi:10.1039/C2EM30132F density (less than 5 people per km2), earlier data, especially lake data, could be considered characteristic of pristine environments. More pristine environments are to be found in northern Canada and the study conducted by Lockhart et al.8 can be used as another basis of comparison for mercury concentrations in fish in the broader oil sands area and in pristine areas: the primary caveat is that fish in the north are generally old and slow growing whereas fish in southern Canada, including Alberta are younger with faster growth rates35 and greater potential for growth dilution of mercury. However, warmer temperatures and gener- ally higher productivity rates in southern Canada may favor greater mercury methylation rates than those found in the north. Considering the Northwest Territories and length-adjusted walleye (438 mm walleye) populations, 38% had mercury concen- trations of <0.2 mgg1, 38% concentrations between 0.2 and 0.5 of Fig. 4 Time trends in walleye mean weight and mercury concentration mgg1 and24%hadconcentrations>0.5mgg1.8 Forthisstudy,the for fish caught from the Athabasca River in the oil sands area. Data from percentages were 11%, 83%, and 6% respectively where fish were Table 2 with 1975 data based on weighted means. Mercury concentra- not length adjusted; walleye length averaged 425 mm. A concen- tions are for fillet with 1975 concentrations estimated from the regression m 1 from Peterson et al.6 with whole body mean also shown. The regression tration of 0.2 gg is used as an advisory guidelines for subsistence line (panel c) and 95% confidence interval is based on mean fish weight consumers of fish, i.e., long-term consumption patterns of >100 g 1 and mercury concentration (fillet) for 1992–2011 collections with 1975 per day while 0.5 mgg is the guideline for the commercial sale of and 1984 collections displayed separately. *years shown in Fig. 3. See text fish; certain commercially caught fish which exceed this guide but for additional explanation. are not regularly consumed can be sold with an advisory, e.g.,shark and marlin.12

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For 430 mm lake whitefish populations in the NWT, 87% had landscape. Fugitive and secondary sources of emissions can be mercury concentrations of <0.2 mgg1, 13% had concentrations significant sources of contamination including: dust eroded from between 0.2 and 0.5 mgg1 and no populations exceeded >0.5 the exposed landscape; gases and particulates released from vehicle mgg1.8 For this study area, the percentages were 100%, 0%, and exhaust and operation, ore extraction, road construction; land 0% respectively where fish length averaged 422 mm. clearing; and forest fires.4,36,37 Together these sources contribute to For NWT length adjusted (622 mm) northern pike populations, local atmospheric pollution with chemicals reaching the landscape 17% had mercury concentrations of <0.2 mgg1,64%had through dry fall (particulates) and precipitation (gaseous, dis- concentrations between 0.2 and 0.5 mgg1 and 19% had concen- solved, small particulates) pathways. Concentrations decrease with trations >0.5 mgg1. For this study area, the percentages were 36%, distance from the disturbance (due to dilution and loss over an 58%, and 6% respectively; pike length averaged 573 mm. increasing expanding area) typically reaching background levels ca. For 555 mm lake trout populations in the NWT, 29% had 25–50 km away.2,3,36–38 mercury concentrations of <0.2 mgg1, 51% had concentrations Two studies have investigated oil sands emission impacts on lake between 0.2 and 0.5 mgg1 and 20% had concentrations >0.5 acidification and productivity on lakes in the oil sands region;16,39 mgg1.8 For this study area, the percentages were 0%, 100%, and sediment cores were collected in 2003 from 12 lakes ranging from 0% respectively where fish populations were not length adjusted. 35 to 300 km from the oil sands development. Mercury concen- Lake trout were large, averaging 624 mm. trations in surface sediments ranged from 67–138 ng g1 with no obvious pattern related to the oil sands operations. While all cores Discussion showed evidence of industrial contamination and nutrient enrich- ment with potential drivers being climate change, forest fires and While mercury concentrations have been reported to have anthropogenic nitrogen deposition, these changes could not be increased in walleye in the Athabasca River with the expanding oil directly linked to oil sands impacts. The exception was Lake NE7, sands operations,5 the reported trend was influenced by the fact asmall(11.2ha),shallow(maximumdepth2m)lakelocatedca. 35 that mean fish weight increased over the three years of comparison. km east of the oil sands development, which showed evidence of Moreover the trend was also influenced by the fact that mercury increased acidification. Mercury time trends were reported only for determinations were based on whole body in the first study year the core from this lake. Concentrations increased from ca. 60 ng g1 and fillet in the next two study years; mercury concentrations in the early to mid 1880s to 100–170 ng g1 in recent years; mercury generally are higher in fish fillet than whole body.6 When all flux rates increased from 4 mgm2 per year to 11 mgm2 per year. In available data for mercury concentrations in fish were considered 2009, a sediment core was collected from Namur Lake; mercury and comparisons based on similar river reaches, there was concentrations increased from 90 ng g1 in the early 1990s to 104– a significant trend for mercury concentrations to decline in walleye 114ngg1 in recent years and mercury flux rates from 16.6 ng m2 over 1984–2011 and walleye and lake whitefish over 2002–2011 in peryearto47.3ngm2 per year.40 These increases in mercury flux the Steepbank and Muskeg reaches of the Athabasca River. rates are similar to those observed in lakes far removed from major Furthermore, there was a significant trend for mercury concen- mercury emitters, i.e.,Muiret al.41 estimated that average mercury Downloaded by McGill University on 05 June 2012 trations to decline in northern pike in the western Lake Athabasca flux rates had increased from 6.6 mgm2 per year to 11.4 mgm2 per year in Arctic lakes, 14.9 to 25.5 mgm2 per year in subarctic lakes Published on 31 May 2012 http://pubs.rsc.org | doi:10.1039/C2EM30132F over 1981–2009 while walleye and lake trout concentrations remained unchanged. Only in Namur Lake were mercury and 24.9 to 63.5 mgm2 peryearintemperatelakessincetheonset concentrations significantly higher in lake trout in 2007 than 2000. of the Industrial Revolution. Ongoing Environment Canada sedi- The explanations as to why mercury concentrations have not ment core studies in the oil sands area are providing for stronger increased in walleye, pike and lake whitefish in the oil sands area of characterizations of mercury, other metals and PAH fluxes in small the Athabasca River despite the accelerating increase in open pit lakes within 50 km of the oil sands operations where localized mining and bitumen extraction and upgrading are based on impacts are likely to be greater due to the lower dilution of emission considerations of mercury emission and deposition rates, mercury and closer proximity to fugitive emissions.42,43 exposure, other ecosystem changes, and monitoring design. Proximity to a major mercury emitter does not always result in high mercury concentrations in sediments and/or fish as illus- trated from several Canadian studies around major mercury Mercury emission and deposition rates emitters. The oldest of these emitters, the copper–zinc smelter Oil sands operations, like other mining operations, result in the located in Flin Flon (Manitoba) was constructed in 1931 and had release of metals and other contaminants into the environment. As an estimated mercury emission rate of 19 900 kg per year up until fuel is consumed and the ore treated, chemicals are released in 1993.44 By 1985, lakes within a few kilometers of the smelter had emissions. The nature of these emissions depends on the facility and highly contaminated sediments with mercury concentrations the engineering controls designed to minimize contamination, ranging from 2690–9220 ng g1 versus 30–220 ng g1 in lakes particularly local contamination where dilution is least intense. more than 68 km from the smelter.45 However, mercury Large particulates settle to the landscape faster than small partic- concentrations in northern pike (fillet) were lowest (0.09 0.03 ulates; chemicals released in gaseous form have higher dispersal mgg1) in lakes near the smelter and highest (0.47 0.25 mgg1) capabilities than chemicals released on particulates. Stack height in lakes 68–84 km northwest; fish size and age were similar in all (which affects vertical distance and travelling time to the landscape) lakes. Mercury uptake by fish in the Flin Flon lakes may have and the emission temperature (which causes plumes to rise when it been inhibited by the high selenium concentrations in sediments is warmer than the surrounding air) also affect the time required for impacted by smelter emissions; high mercury concentrations in chemical emissions (as gases, liquids, and particulates) to reach the pike from the lakes to the northwest may have been partially

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related to the slight acidity of these lakes which may have favored sources (i.e., fugitive dust from the landscape) may be the more mercury methylation.45 important pathways of mercury into the local aquatic environ- While mercury emission rates for the oil sands area are signifi- ment than emissions from stacks including the oil sands where cant and increasing, they are lower than in Wabuman Lake (Fig. 5). the exposed landscape is substantial and poorly weathered. There are four large coal-fired power plants in close proximity to Wabuman Lake with the first plant constructed in 1956 and the last Mercury exposure: water and sediments and water in 1989;46 the combined emissions from these four power plants were 387–732 kg per year over 2000–2010. Despite these high There is little evidence that mercury exposure in sediment and emission rates, mercury concentrations remain low (80–120 ng g1) waters has changed appreciably for the fish investigated in this in the upper 5 cm of sediments although greater than background study. The earliest records for mercury concentrations in water are concentrations deeper in sediment cores (25–50 ng g1). Similarly, from RAMP; only concentrations measured using ultra-trace mercury concentrations in northern pike collected from Wabuman sampling techniques (detection limits 1.2 ng L1:theICPMSby Lake were generally similar to concentrations measured in pike in DRC-II1 method) are considered reliable. Mercury concentrations other distant lakes.40,47 were low ranging from 1.2–19 ng L1 (mean 2.7 ng L1)withthe The zinc–lead smelter located in a Columbia River valley in three highest values (3–12 ng L1) associated with spring flow in the Trail, British Columbia, had estimated mercury emissions rates of Athabasca and Ells River when suspended sediment concentrations 70–80 kg per year over 1998–1999;36 while most metals tended to were high. Concentrations have not changed measurably in recent occur in elevated concentrations in soils within a few kilometers of years and water pH remains slightly basic (8.2 0. 6). Lakes are the smelter, this was not observed for mercury. Goodarzi et al.37 more sensitive to acidification from emissions than rivers; however, suggested that mercury concentrations in soil were controlled there is no evidence that pH has changed in the lakes investigated in predominately by local soil factors; mercury, especially elemental theRAMPacid-sensitivelakeprogram.Lakesinthisprogramare mercury, was too volatile to deposit close to the smelter. Volatili- dominated by small (median area 1.32 km2,meandepth1.8m)and zation losses were particularly great in dry years. Secondary sources humic (mean dissolved organic carbon 21.5 mg L1) lakes and such as fugitive dust also were influential in affecting elevated metal many are acidic; these small shallow lakes are unlikely to support concentrations close to the smelter. A recent study showed no the large predatory fish investigated in this paper because of peri- evidence of elevated mercury concentrations in water, sediments odic winter kills during prolonged ice cover. Namur Lake has and fish downstream of the smelter.48 shown no trend in pH with 2000 pH (7.09) similar to that measured Atmospheric emissions have substantial capacity for dilution. in 2007 (7.05). However, some evidence of acidification was Stacks typically are several tens to a couple of hundreds of meters detected in a sediment core in only one of the 12 lakes investigated high with emissions in the form of heated plumes; these plumes by Curtis et al.;16 lake NE7 is particularly small (0.1 km2)and continue to rise and cool and then are carried horizontally with shallow (maximum depth 1.8 m). the prevailing winds within a moving air cell; direction and speed Mercury concentrations also remain low in the surface sediments depends on local meteorology. The air overlying the landscape is in the lakes and rivers where mercury concentrations have been Downloaded by McGill University on 05 June 2012 turbulent with daily heating and cooling cycles which limits the determined in fish and similar to concentrations measured in earlier settling rate of chemicals in the gaseous, vapor and small times. For example, Lutz and Hendzel22 reported that mercury Published on 31 May 2012 http://pubs.rsc.org | doi:10.1039/C2EM30132F particulate form except during precipitation events. Unlike concentrations in surface sediments at their 16 study sites investi- effluents discharged into a river or lake, emission plumes are not gated in 1975 ranged from <10 ng g1 to 50 ng g1 (dry weight); constrained in their direction of travel which allows for greater higher concentrations were associated with sediments in the Peace dispersal and dilution. It is this mobility in mercury emissions and Athabasca delta where fine silts and clays accumulate. A similar that has contributed to their global dispersal by atmospheric range (30–63 mg g1) was reported in Donald et al.25 for sediments pathways to all regions of the world. Secondary atmospheric collected in a similar area in 1976. In 1992, mercury concentrations in Athabasca River delta sediments ranged from 50–89 ng g1;25 mercury had a similar range (<50–86 ng g1)inthesameareain 1998 and 1999.40 Under the RAMP 1999–2010 program, mercury concentrations in river, tributary and delta sediments were below detection limits (50 ng g1) for most (>80%) of the 260 samples analyzed. With the two exceptions, detectable mercury concentra- tions ranged from 10–100 ng g1 with an average concentration of 60 ng g1; a sample collected from Isadore Lake in 2008 had a mercury concentration of 210 ng g1 and a Stanley Creek sample in 2003 had a mercury concentration of 130 ng g1.Thegreater range in mercury concentrations is partially due to the greater number of samples that were analyzed over the course of the RAMP studies than earlier studies (1990s) and the inclusion of lakes. Low mercury concentrations in tributary waters and sediments Fig. 5 Time trends in mercury emissions by four coal-fired power plants despite the strong presence of bitumen in some sediment samples in the Wabamun Lake area and the oil sands area (Fort McMurray), and are partially related to the fact that although bitumen is highly all of Alberta. Data from T. Richens, personal communication and enriched in polycyclic aromatic hydrocarbons (PAHs), mercury Environment Canada.44 concentrations are not high. This is illustrated by considering the

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co-occurrence of mercury and C2-dibenzothiophene (a major Monitoring design constituent of bitumen) at high and low concentrations of this 1 Monitoring design is important in the ability to detect trends in PAH;asedimentsamplecontaining4ngg C2-dibenzothiophene 53 mercury concentrations in fish. Sensitive sampling design hadamercuryconcentrationof40ngg 1 whereas a bitumen-rich includes considerations of how many fish are measured at a given sample containing 3690 ng g 1 of C2-dibenzothiophene contained 27 time, the size range of fish analyzed, what metrics are measured 80 ng g 1 mercury. Thus water flowing past exposed bitumen beds (in addition to mercury concentration), how often samples are do not become enriched in mercury; nor are eroded sediments rich collected, and the analytical methods used. Monitoring design in mercury. Moreover, with the exception of Suncor, industrial also depends on the purpose of the study. waste water is not released into the river; Suncor’s 2011 release rate In general, the monitoring data analyzed in this study were is less than 0.014% of the Athabasca River flow rate. The annual obtained as part of programs designed to periodically assess release of mercury in water by Suncor Energy Inc Oil Sands at Fort 21 mercury levels in fish, often from a fish advisory purpose, where McMurray has declined from 2 kg in 2000 to 0.051 kg in 2010. only a small number of fish were measured sporadically at While there is compelling evidence of elevated mercury, other various locations, particularly for the period prior to the major metals, and PAH concentrations collected in snow samples 1–4 expansion of the oil sands industry in the 2000s. Therefore, while collected in the vicinity of oil sands operations which have been 42 the results of analysis of variance indicated that year was confirmed with recent study, the contribution of these contami- a significant factor affecting variability in mercury concentra- nants to tributary flow during snow melt events is poorly quantified tions in lake whitefish and walleye in the Athabasca River and but dilution is likely to be intense. northern pike in western Lake Athabasca over the length of the The vast majority (90%) of Athabasca River water flowing record, it is not possible to attribute possible cause, particularly past the oil sands development area originates from upstream of where the trend was of a decline. Fort Murray and contributes to 90% of its downstream flow pass In order to more effectively monitor time trends in mercury the oil sands development area with the tributaries contributing concentrationsinfish(asopposedtoperiodicassessmentsfroman only ca. 10% to the flow, i.e., dilution of tributary flow is advisory perspective), the monitoring program needs to be more immense; these tributaries also have a low contribution to 17 rigorous in its design including a sampling frequency sufficient to Athabasca River sediment load. Moreover, with the Athabasca detect change, e.g., as in the annual lake trout and burbot moni- River flow rate in the order of kilometers per day, the residence toring being conducted in the Northwest Territories and lake trout time of water in the oil sands area is short. Similarly, the resi- and walleye on the Great Lakes.7,14,15 More frequent sampling dence time of fine silts, clays and sands is likely to be short given allows for a greater statistical power to detect change as the data- the strong seasonality in hydrological flow with very high flows base builds faster and the influence of climatic (warm years versus and scour during spring melt. Thus, released contaminants are cold years) can be investigated in addition to the rapidly expanding rapidly transported downstream and do not accumulate. oil sands industry. Metrics such as fish age and stable isotope analyses aid in the interpretation of the factors affecting or masking

Downloaded by McGill University on 05 June 2012 Other ecosystem changes changes in mercury concentrations and these have seldom been measured. If climate change is affecting the fundamental ecology of Mercury concentrations were significantly higher (p < 0.0001) in Published on 31 May 2012 http://pubs.rsc.org | doi:10.1039/C2EM30132F the area, then these metrics will be needed in interpreting mercury lake trout from Namur Lake (surface area 42 km2 and located trends (or their lack) as carbon sources, trophic level feeding and northeast of the oil sands operations) in 2007 than in 2000. This growth ages all may be expected to change. is in contrast to no temporal change being detectable in Lake Sampling location needs to be considered more systematically. Athabasca (lake surface area 7900 km2) lake trout. Only two The most frequent monitoring has been of walleye and whitefish years of study were conducted in Namur Lake. Similar increases from the Athabasca River in the immediate development area. This in mercury concentrations have been observed in lake trout in 49 monitoring provides valuable information from a fish advisory similar-size lakes in the Northwest Territories. In addition, 14 perspective. While burbot are not being monitored under RAMP, Carrie et al. observed a marked increase in mercury concen- they were for persistent organic contaminants and mercury under trations in burbot harvested from the Fort Good Hope area of the Northern River Basins Study54 and could be included under an the Mackenzie River; this increase was related to a warming enhanced Athabasca River monitoring program. It is noteworthy trend (1.9 C since the early 1970s) which they hypothesized that trends of mercury increase have been detected in burbot in the enhanced mercury methylation rates and the delivery of mercury Mackenzie River and Great Slave Lake; burbot, possibly because to the aquatic ecosystems. While a similar warming trend (ca. 1.4 of its sedentary nature, may be more sensitive to the factors C since the early 1970 to 2008 or 0.04 C per year (ref. 50)) has enhancing the increased bioavailability of mercury in the environ- been observed at Fort McMurray, the rate of increase has been ment than pelagic warm-water fish such as pike and walleye. lower (0.014 C per year) in recent years (1984–2008); there However, this monitoring may not provide the desired sensitivity to evidence from the sediment record of increasing lake produc- 16 40 detect trends in mercury exposure; water and sediments have short tivity including at Namur Lake. However, it is not possible residence times and large fish are mobile. with the available data to ascribe the higher mercury concen- Monitoring of mercury (and other contaminant) concentra- trations in Namur Lake trout in 2007 (mean air temperature 1.98 tions of forage fish in the tributaries merits consideration as C) than 2000 (mean air temperature 0.33 C) to oil sands effects; tributary fish would be more directly exposed to ground water global warming and increased atmospheric inputs of mercury and episodic pulses of water flowing off the landscape, e.g., snow and nitrogen from global sources must also be considered in 9,41,51,52 melt, storms; forage fish may be less mobile than large, predatory evaluating temporal differences.

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fish. Forage fish have proved useful in contaminant trend techniques using certified laboratories. If different laboratories monitoring in the Great Lakes, in part because of their relatively are used or methods are changed, then round robin studies sedentary nature which allows for the investigation of time trends should be conducted to ascertain that all studies are providing in local environments.55,56 The disadvantage to forage fish similar results; invariably there are differences between labora- monitoring is that they are short lived and generally do not attain tories, albeit small, but such differences could mask and hence the high mercury concentrations observed in larger fish preda- reduce the sensitivity to detect trends. tors; nor are they important in the domestic, sport and commercial fisheries. Conclusions The Athabasca delta and western Lake Athabasca merit an improved fish contaminant monitoring program. Sediments carried Based on available data, there is no evidence to support the downstream with Athabasca River flow are deposited in the delta contention that mercury concentrations are increasing in fish as and lake; significant mercury methylation may occur in shallow, a result of expanding oil sands development. Mercury concentra- weedy areas, particularly in summer. There is a small commercial tions in water and surface sediments remain low and, in the fishery at Fort Chipewyan, located on the outflow from Fort Athabasca River and its delta, similar to concentrations measured ChipewyanandinhabitedbyCree,ChipewyanandMetis,and in earlier times. While we detectedadecreasingtrendformercury others. Wood Buffalo National Park offices are in Fort Chipewyan concentrations in walleye and lake whitefish in the oil sands and the Peace–Athabasca delta is a major ecological feature of the development area, the interpretation of the potential factors Park. Environment Canada has been monitoring lake trout since influencing these trends is constrained by the fact that the analyses 2007 for flame retardants32 and mercury. Lake trout are present in are based on only five years of data collected during the expansion the western Lake Athabasca only during the cooler months of the of oil sands and limited data before the expansion; analytical year and warm water species such as pike and walleye merit methods have changed. Most of the monitoring has been con- consideration in addition to burbot. ducted in the Athabasca River where the residence time of water is Consideration also needs to be given to monitoring at locations short and the dilution capacity of tributary inflows immense, and in not under the direct influence of the Athabasca River and where lakes more than 50 km from the developments. An improved water and sediment residence times are longer, i.e.,lakes.Assedi- monitoring system is required to reach more definitive conclusions ment core studies have shown that mercury flux rates are increasing regarding mercury trends in fish with the expansion of the oil sands in the oil sands region, as elsewhere,16,41,52 mercury trend monitoring industry and other changes associated with global warming. of fish in a subset of lakes is needed to track global and oil sands emission impacts. Namur Lake, to the west of the oil sands devel- Acknowledgements opment, merits additional attention and is a good candidate for Primary data were made available by Marilyn Hendzel (CFIA, trend studies. Such mercury trend monitoring would complement Winnipeg), Michael Paterson (DFO, Winnipeg), David Depew and the trend monitoring in the NWT where mercury levels are Linda Campbell (Queen’s University, Kingston), and Heather increasing in lake trout in the NWT; Namur Lake has shown Downloaded by McGill University on 05 June 2012 Keith (Hatfield Consultants, West Vancouver). Northern pike and a pronounced increase in mercury sediment flux rates. Lakes lake trout were collected from western Lake Athabasca and downwind of Fort McMurray also merit attention. Gregoire Lake, Published on 31 May 2012 http://pubs.rsc.org | doi:10.1039/C2EM30132F Richardson Lake by Robert Grandejambe (Fort Chipewyan) as 30 km southeast of Fort McMurray, is a candidate lake; this lake is part of a larger National Chemical Management Plan study led by relatively close to the developments and is not well-buffered against Sean Backus, Environment Canada, Burlington, Ontario. Jona- potential acidic deposition from snow or rainfall.57 To the east, there than Keating (Environment Canada, Saskatoon) finalized figures. are a good series of candidate lakes in Saskatchewan, e.g.,Pine- Helpful comments to this manuscript were provided by Derek house Lake and La Loche support domestic fisheries while lakes Muir (Environment Canada, Burlington), Fred Wrona (Environ- further to the east on the Laurentian Shield such as Cree Lake could ment Canada, Victoria), Al Colodey (Environment Canada, North merit some attention; a mercury trend monitoring program has Vancouver), Yves Laurent (Environment Canada, Montreal) and begun at Reindeer Lake even further to the east and closer to Flin Kim Janzen (Environment Canada, Saskatoon). Special appreci- Flon as part of flame retardant monitoring.32 Ideally lakes within 30 ation is extended to two anonymous reviewers. km of the developments would be monitored for mercury time trends in fish. However, most are small and shallow and unlikely to support predatory fish populations. Kearl and McCelland are large References lakes (Fig. 1) but also shallow and weedy lakes; they apparently do 1 K. P. Timoney, A Study of Water and Sediment Quality as Related to not support predatory fish because of periodic winter kills but Public Health Issues, Fort Chipewyan, Alberta, Treeline Ecological forage fish may merit some consideration for mercury trend moni- Research, Sherwood Park, AB, 2007. 2 E. N. Kelly, J. W. Short, D. W. Schindler, P. V. Hodson, M. Ma, toring. Gregoire Lake to the south has already been mentioned. A. K. Kwan and B. L. Fortin, Proc. Natl. Acad. Sci. U. S. A., 2009, The inability to detect trends in this study was compounded in 106, 22346–22351. part by the fact that measurements have been based on whole 3 E. N. Kelly, D. W. Schindler, P. V. Hodson, J. W. Short, R. Radmanovich and C. C. Nielsen, Proc. Natl. Acad. Sci. U. S. A., body and fillet; differences in analyses based on tissue plugs and 2010, 107, 16178–16183. 6 fillets were less likely to have been important. Several labora- 4 P. Gosselin, S. E. Hrudey, M. A. Naeth, A. Plourde, R. Therrien, tories, using different methods, conducted these analyses over the G. Van Der Kraak and Z. Xu, Environmental and Health Impacts of decades, although the larger issue is the infrequent and incon- Canada’s Oil Sands Industry, Royal Society of Canada Expert panel report, Ottawa, ON, 2010. sistent sampling prior to the expansion of the oil sands industry. 5 K. P. Timoney and P. Lee, The Open Conservation Biology Journal, Future monitoring studies should be based on consistent 2009, 3, 65–81.

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