Spatial Patterns of Methylmercury Risks to Common Loons

Article pubs.acs.org/est

Spatial Patterns of Methylmercury Risks to Common Loons and Piscivorous Fish in Canada David C. Depew,*,†,⊥ Neil M. Burgess,‡ and Linda M. Campbell†,¶ †

Department of Biology and School of Environmental Studies, Queen’s University, Kingston, Ontario K7L 3N6, Canada Ecotoxicology and Wildlife Health Division, Science and Technology Branch, Environment Canada, Mount Pearl, Newfoundland A1N 4T3, Canada

‡

S Supporting Information *

ABSTRACT: Deposition of inorganic mercury (Hg) from the atmosphere remains the principle source of Hg contamination for most aquatic ecosystems. Inorganic Hg is readily converted to toxic methylmercury (MeHg) that bioaccumulates in aquatic food webs and may pose a risk to piscivorous fish and wildlife. We conducted a screening-level risk assessment to evaluate the extent of risk to top aquatic piscivores: the common loon (Gavia immer), walleye (Sander vitreus), and northern pike (Esox lucius). Risk quotients (RQs) were calculated on the basis of a dietary Hg exposure indicator (HgPREY) modeled from over 230 000 observations of fish Hg concentrations at over 1900 locations across Canada and dietary Hg exposure screening benchmarks derived specifically for this assessment. HgPREY exceeded benchmark thresholds related to impaired productivity and behavior in adult loons at 10% and 36% of sites, respectively, and exceeded benchmark thresholds for impaired reproduction and health in fishes at 82% and 73% of sites, respectively. The ecozones of southeastern Canada characterized by extensive forest cover, elevated Hg deposition, and poorly buffered soils had the greatest proportion of RQs > 1.0. Results of this assessment suggest that common loons and piscivorous fishes would likely benefit from reductions in Hg deposition, especially in southeastern Canada.

■

INTRODUCTION The ecological impacts of mercury (Hg) exposure have been a topic of extensive investigation since several high-profile Hg poisoning events between the 1950s and 1970s (e.g., Minimata, Japan; English−Wabigoon River, northwestern Ontario).1 Use of Hg in antifungal seed dressings, direct discharge of Hg wastes from chlor-alkali plants, and Hg-based slimicides from pulp and paper mills were associated with overt neurological dysfunction and even death in a variety of wildlife species.1 Research has since indicated that Hg released to the atmosphere from anthropogenic activities, such as the smelting of metal ores, combustion of fossil fuels, and incineration of waste, has led to widespread contamination of aquatic and terrestrial ecosystems on a global scale.2 When atmospheric Hg is deposited in aquatic and terrestrial ecosystems, it may be methylated by bacteria3 to highly toxic methylmercury (MeHg) which readily accumulates in both aquatic and terrestrial food webs,4,5 placing organisms at the top of the food chain at the greatest risk. To date, comprehensive efforts to evaluate risks of aquatic MeHg exposure to wildlife have appropriately focused on piscivorous wildlife at sites of former industrial Hg pollution6 or those significantly impacted by local Hg emission sources (e.g., Florida Everglades7). However, recognition of widespread atmospheric Hg contamination of ecosystems coupled with increasing evidence of subtle neurobehavioral, endocrine, reproductive, and © 2013 American Chemical Society

immune system impairment, in a variety of vertebrate species at environmentally relevant MeHg exposures,8−10 has led to the perception that risks of atmospherically derived MeHg may be more widespread than previously thought. In response, comprehensive programs in the United States (e.g., MercNet11) and Canada (e.g., CARA12) were established to further address remaining uncertainties and provide a baseline against which to compare the effectiveness of Hg emission regulations and recent studies have sought to characterize risks of atmospherically derived MeHg exposure to piscivorous fish and wildlife at regional scales.13−15 As part of Environment Canada’s Clean Air Regulatory Agenda (CARA) program, we previously compiled Hg concentration data from over 100 species of fish from nearly 5000 locations across Canada between 1967 and 2010.16 The spatial and temporal scope of data collected provided a unique opportunity to evaluate MeHg risk on a national scale. This paper reports the results of a screening-level ecological risk assessment of dietary MeHg exposure for key aquatic piscivores in Canada. Screening-level ecological risk assessments are a component of the Ecological Risk Assessment (ERA) Received: Revised: Accepted: Published: 13093

August 26, 2013 October 21, 2013 October 24, 2013 October 24, 2013 dx.doi.org/10.1021/es403534q | Environ. Sci. Technol. 2013, 47, 13093−13103

Environmental Science & Technology

Article

framework and are generally used to evaluate the need for more rigorous study to reduce uncertainties and characterize risk.17,18 For this screening-level risk assessment, adult common loons (Gavia immer) and sexually mature female walleye (Sander vitreus) and northern pike (Esox lucius) serve as ecological receptors. These receptors were chosen on the basis of their status as top trophic piscivores in aquatic food webs,19,20 broad geographic distribution across Canada,21,22 and their tendency to accumulate high levels of Hg in their tissues.16,23 In addition, a large body of Hg-related ecotoxicological work exists in the literature for the common loon.24 The selection of female fish at the age of first reproduction follows the rationale of Sandheinrich et al.15 in order to simplify interpretation of risk at the population level. With the exception of severely Hg-polluted aquatic ecosystems, the major route of MeHg exposure for piscivorous fish and wildlife in most aquatic ecosystems is via the diet.1,25 Consequently, in this paper, we evaluate risk based on dietary MeHg exposure inferred from prey Hg concentration. Because fish Hg concentrations vary by species and size26 and it is difficult to obtain consistent species and size combinations for all sites from previously existing data sets, we used a modeling approach to estimate Hg concentrations in a standard-length, small yellow perch (Perca f lavescens) across Canada.27 This approach maximizes the value of existing historical data sets by normalizing exposure to a common prey indicator across all sites. We selected a 12 cm whole yellow perch as a common prey indicator. Yellow perch tolerate a wide range of environmental conditions,28 share a similarly broad distribution across Canada as the chosen receptors,22 and are considered a favored prey of common loons,29,30 walleye, and northern pike.31,32 Total Hg in yellow perch is strongly correlated to blood Hg concentrations of adult and juvenile loons on breeding grounds across northeastern North America and the Great Lakes region,13,33 as well as muscle Hg from walleye, northern pike, and largemouth bass (Micropterus salmoides) from the same systems.34 The 12 cm size selection was based on the size range of fish most commonly consumed by adult loons (10−15 cm29), and the optimal prey/ predator body length ratios of 0.29−0.3535,36 reported for walleye and northern pike at the age of first sexual maturity from lakes across Canada (walleye ∼34−42 cm; northern pike >34 cm22). Because our focus here is on Hg of atmospheric origin, we do not consider aquatic ecosystems impacted by current or historical point-source Hg inputs (e.g., chlor-alkali and pulp mill complexes, gold and Hg mine tailings). Furthermore, we do not consider reservoirs and downstream water bodies sampled within 30 years of impoundment because the behavior of MeHg in food webs during the early stages of reservoir flooding is well characterized and does not represent that in unimpacted systems.37

Table 1. Dietary Screening Benchmark Values Used to Calculate Risk Quotients for Dietary MeHg Exposure, Categorized by Ecological Relevancea dietary screening benchmark (μg MeHg g−1, ww) receptor

benchmark

NOAELc

LOAELd

reference

failed productivity impaired productivity impaired behavior

NA NA NA

0.4 0.18 0.1

24 24 24

mortality impaired growth impaired reproduction impaired behavior impaired health

2.8b 1.4 0.04 0.5 0.05

NA 1.97 0.05 0.96 0.14

45 45 45 45 45

common loon

fish

a

Bold values indicate screening benchmarks selected for this ecological risk assessment. Note that screening benchmarks are expressed as μg MeHg g−1 wet weight (ww). bExpressed as a threshold effect level (geometric mean of the 50th percentile of NOAELs and 15th percentile of the LOAELs). See Beckvar et al.46 for a more thorough description. cNo observed adverse effect level. dLowest observed adverse effect level.

have not yet been satisfactorily defined for wild or captive loons.30 The reproductive impairment benchmark for loons is equivalent to the geometric mean Hg concentration of prey fish estimated to be associated with a 40−50% reduction in productivity and a 50% reduction in egg hatching success. The reproductive failure benchmark is based on observed reproductive failure in wild loons in territories with prey fish Hg levels >0.4 μg g−1, wet weight.24 Screening benchmarks for individual survival or population impacts have not yet been proposed, in part because adult loons do not fare well in captivity41 and current mark−resight data inventories are not yet sufficient to detect small but potentially significant changes in survival of wild adult loons associated with mercury exposure.42 Screening benchmarks for fish (Table 1) were derived from chronic dietary exposures of between 4 and 12 different species in controlled laboratory studies and were based on ecologically relevant end points. Of the studies reviewed, only two used walleye43,44 while the remaining species were typical laboratory species (e.g., rainbow trout, zebra fish, fathead minnow).45 Screening benchmarks for fish are based on the highest NOAEL below the lowest LOAEL when ranked by magnitude.45 This approach, although conservative, does not severely underestimate protective thresholds as the 5% hazardous concentration threshold (HC5) approach does when data are limited.46 It should be stressed, however, that these screening benchmarks for fish are considered preliminary. Estimation of Dietary MeHg Exposure. We estimated Hg concentration in a 12 cm whole yellow perch (hereafter HgPREY) by applying the USGS National Descriptive Model for Mercury in Fish (NDMMF47) to a Canada wide data set of fish Hg concentrations.27 The NDMMF partitions variation in fish Hg concentrations between spatiotemporal and sample characteristic (e.g., species, tissue, size of fish) variation.47 Once calibrated, model coefficients can be used to estimate Hg concentrations in a specific fish species even if that particular species was not captured at a given site.47

■

METHODS Screening Benchmarks. Diet-based screening benchmarks representing concentrations of MeHg in prey associated with adverse effects form the basis for this ecological risk assessment (Table 1). Screening benchmarks for the common loon derive directly from field studies representing chronic exposure to MeHg on breeding territories,33,38,39 are associated with ecologically relevant end points, and are unlikely to be influenced by the presence of other contaminants.40 These benchmarks are equivalent to a lowest observed adverse effect level (LOAEL; Table 1) as the no observed adverse effect levels (NOAEL) 13094

dx.doi.org/10.1021/es403534q | Environ. Sci. Technol. 2013, 47, 13093−13103


Article

Table 2. Summary of Modeled Values of HgPREY Used for Calculation of Risk Quotients (RQs) Grouped by Ecozone/ Ecoprovincea ecozone/ecoprovince

abbreviation

number of sites (n) loon/fish

median (range) of HgPREY (ug g−1 ww)

Northern Arctic Southern Arctic Pacific Maritime Taiga Cordillera Boreal Cordillera Montane Cordillera Taiga Plain Boreal Plain Prairie Western Taiga Shield West Boreal Shield Hudson Plain Lake of the Woods Mid-Boreal Shield Southern Boreal Shield Mixedwood Plain Eastern Taiga Shield East Boreal Shield Atlantic Maritime Newfoundland Total

NA SA PM TC BC MC TP BP PR WTS WBS HP LOW MBS SBS MP ETS EBS AM NF

3/3 28/28 12/13 1/1 12/13 16/21 48/48 201/201 47/49 43/43 260/260 41/41 65/65 192/192 380/380 258/279 59/59 71/71 160/168 5/5 1902/1936

0.03 (0.02−0.05) 0.06 (0.02−0.09) 0.08 (0.02−0.75) 0.08 0.04 (0.02−0.09) 0.05 (0.03−0.13)/0.04 (0.01−0.13) 0.05 (0.02−0.19) 0.04 (0.01−0.25) 0.06 (0.02−0.09)/0.06 (0.02−0.22) 0.05 (0.01−0.18) 0.04 (0.01−0.18) 0.11 (0.05−0.27) 0.07 (0.03−0.17) 0.10 (0.01−0.34) 0.11 (0.01 − 0.53) 0.06 (0.02−0.40) 0.11 (0.03−0.47) 0.13 (0.06−0.33) 0.15 (0.02−0.43)/0.15 (0.02−0.96) 0.28 (0.16−0.47)

a Ecozone/ecoprovince abbreviations used in Supporting Information figures and material are also provided, as are the numbers of sites used to calculate RQs for loons (left of slash) and fish (right of slash), respectively, and the median and range of HgPREY (expressed as μg g−1 wet weight) for each ecozone/ecoprovince. If the median or range of HgPREY differed for loon or fish risk assessments, both sets are given. Ecozones are listed in a general west to east gradient (as in Figure 1) starting in northern regions and proceeding southward. Note that the Boreal Shield ecozone has been split into 6 member ecoprovinces owing to its large size. The Taiga Shield has also been divided into two regions, west and east of Hudson Bay (Supporting Information Figure S1).

Estimates of HgPREY were generated for 1936 locations sampled between 1990 and 2010.27 This time period maximizes geographic coverage while attempting to minimize the influence of potential increases or decreases in fish Hg levels on estimates of HgPREY. Estimates of HgPREY are not included for sites of current or historical Hg pollution, reservoirs, and downstream water-bodies because prediction errors were significantly higher at these sites.27 Risk Characterization. A risk quotient (RQ) approach (eq 1) was employed to characterize risks to adult breeding common loons and sexually mature female walleye and northern pike. RQ =

However, the types of site-level data required to assess this are only available for a handful of sites included in this assessment (A. Ethier, Atomic Energy Canada, Pers. comm.). We therefore used an ecozone approach to evaluate the coherence of spatial patterns of risk (i.e., proportion of sites within an ecozone with RQ > 1.0) and available Canada-wide data sets of hypothesized drivers of MeHg availability. The terrestrial ecozones of Canada (http://sis.agr.gc.ca/cansis/nsdb/ecostrat/index.html) represent subcontinental regions of general ecological similarity formed by the interaction of climate, human activity, vegetation, geological, and physiographic features51 and form the spatial unit of analysis. Although this approach necessarily aggregates data at a coarse scale, the purpose here is not predictive but associative. Nearly half of the 1936 sites were located in Canada’s most expansive ecozone, the Boreal Shield (Supporting Information Figure S1, Table 2). The remaining sites are unequally distributed among 14 other ecozones (e.g., the Arctic Cordillera had no sites; Table 2). Owing to the large size and numbers of sites within the Boreal Shield, we split the Boreal Shield into six member ecoprovinces (Supporting Information Figure S1, Table 2) and split the Taiga Shield into western and eastern portions separated by Hudson Bay (Supporting Information Figure S1, Table 2). Canada-wide digital data sets of net Hg deposition, land cover, and soil pH were used as described in the Supporting Information. Ecozone-level summaries for each data set were generated by overlaying ecozone boundaries and calculating summary statistics (e.g., minimum, mean, maximium, standard deviation) using SAGA-GIS (http://saga-gis.org). Ecozone-level summaries of land cover classes were generated after projection to an Albers Equal Area Projection in ArcMap v9.3.1.52 Principal components analysis (PCA) was used to ordinate ecozones

Hg PREY (μg g −1 wet weight) screening benchmark (μg g −1 wet weight)

(1)

For each location with a reliable estimate of HgPREY, HgPREY was divided by the appropriate screening benchmark (Table 1) to derive a RQ. Following USEPA17 convention, RQs are rounded to one decimal place (i.e., 1.0). RQs with a value >1.0 represent potential risk, whereas RQs < 1.0 represent negligible risk. Spatial Assessment of MeHg Risks. There are an estimated 910 400 lakes >0.1 km2 within Canada,48 so our HgPREY data set cannot be considered entirely representative nor unbiased owing to its amalgamated nature.27 Despite this limitation, the HgPREY data set offers a unique opportunity to evaluate large-scale patterns of Hg risk and compare them with patterns predicted by current conceptual models of environmental cycling of atmospherically derived Hg. Such models predict that regions receiving elevated Hg and/or sulfate deposition, having a high degree of forest and/or wetland cover, and having other characteristics conducive to the promotion of Hg methylation and bioaccumulation will have aquatic biota with high Hg levels.49,50 13095



Article

Recent reviews of Hg ecotoxicology have indicated that reproduction or productivity is the population demographic parameter most affected by environmentally relevant MeHg exposure.10,55 MeHg has been shown to negatively affect mate selection,56 embryonic development, and hatching success in a variety of avian species,57,58 including loons.59 MeHg exposure can negatively affect reproductive physiology in fishes,60 contribute to poor spawning success,61 impair larval survival,62 and alter sex ratios of offspring.63 In this assessment, up to 10% and 82% of sites exceeded screening benchmarks for reproductive impairment in common loons and piscivorous fishes, respectively. The large discrepancy in apparent risk is likely related to differences in the quality of screening benchmarks used for reproductive impairment (see below). The spatial pattern of risk at the ecozone/ecoprovince level (as inferred from the % of sites with RQs > 1.0) indicated that ecozones with a high proportion of sites with RQs >1.0 received elevated net Hg deposition, had a high proportion of forest cover, and were characterized by low soil pH and most are located in southeastern Canada. Concentrations of Hg in stream and lake sediments show a strikingly similar geographical pattern and indicate that the ecozones of southeastern Canada have likely received elevated Hg deposition for some time.64,65 In addition, these ecozones received significant acidic deposition owing to their downwind proximity to SOx and NOx emission sources.66,67 Although acid-sensitive regions exist in central and western Canada, to date, many aquatic ecosystems have yet to display the same level of acidification as observed in southeastern Canada.68 The Mixedwood Plain ecozone is perhaps the lone exception where, despite receiving elevated Hg69,70 and sulfate deposition,71 the proportion of sites with RQs > 1.0 was considerably lower than geographically adjacent econzones/ecoprovinces. Soils here are underlain by carbonate-rich Paleozoic bedrock, giving rise to productive soils characterized by a good buffering capacity, while intensive agricultural and urban land use51 may mitigate MeHg bioaccumulation in aquatic biota through eutrophication.72 Although direct extrapolation of the percentage of sites with RQs > 1.0 at the ecozone/ecoprovince level is discouraged, the overall west-to-east gradient of increasing Hg risk (increasing proportion of RQs > 1.0) observed here is in general agreement with conceptual models of Hg cycling. Independent measures of Hg in the blood, feathers, and eggs of common loons,39,73−75 and tissues of fish from the western United States76,77 and northeastern North America, are also supportive of our findings and suggest that a broad gradient of risk may exist across Canada. Uncertainty in Exposure Estimation. In any ecological risk assessment, the calculation of RQs and inference of risk is dependent on the assumptions and screening benchmarks used. Our assumption that the HgPREY data set is a reasonable surrogate of dietary MeHg exposure for the selected receptors is perhaps the most important. It requires that we assume THg can be considered equivalent to MeHg, that yellow perch have comparable Hg levels to other forage fishes, that Hg levels in fish have remained relatively stable over the 1990−2010 period, that life-history characteristics of receptors will not strongly influence their estimated dietary exposure, and that NDMMF provides reasonable predictions of Hg in forage fishes. HgPREY is modeled almost entirely on axial muscle total Hg concentrations27 and may overestimate risk if MeHg comprises only a portion of THg. On the other hand, our assumption that loon and fish diets consist entirely of 12 cm of whole yellow perch

based on their relative proportions of forest, wetland, agricultural, urban and barren land cover, mean net Hg deposition, and soil pH using the “pcaMethods” package.53 Correlations between the proportion of sites with RQs > 1.0 in each ecozone and principal component axis scores were conducted using Spearman’s ρ using the base “stats” package. All statistical calculations were conducted using R v2.11.1.54

■

RESULTS The range of HgPREY at sites used to characterize risk were nearly identical between common loons and piscivorous fish (Table 2). Most locations were classified as inland lakes (n = 1422) and rivers (n = 385), the Laurentian Great Lakes−St. Lawrence River system (n = 95), small watercourses (n = 26), or ponds, wetlands, or marshes (n = 8). Smaller watercourses, wetlands, ponds, or marshes were not considered to be suitable loon habitat but were considered suitable for piscivorous fish. Risk to Common Loons. For loons, calculated RQs exceeded 1.0 for behavioral impairment at 677 sites (36%), reproductive impairment at 195 sites (10%), and reproductive failure at 9 sites ( 1.0 (Figure 1, Table 2), while 7 and 5 ecozones had a majority of sites with RQs >1.0 greater than the Canada-wide average for behavioral and reproductive impairment, respectively (Figure 1, Supporting Information Table S1). Risk to Piscivorous Fishes. For piscivorous fishes, calculated RQs did not exceed 1.0 for mortality or growth at any site (Figure 2). RQs >1.0 for behavioral impairment were observed at 6 sites (1.0 for reproductive impairment were observed at 1582 sites (82%) across all 20 ecozones/ ecoprovinces and 12 ecozones/ecoprovinces had a majority of sites with RQs >1.0 that exceeded the overall average (Figure 2, Supporting Information Table S1). RQs >1.0 for health impairment were observed at 1407 sites (73%) in 19 ecozones/ecoprovinces, and 10 of these had overall proportions of sites with RQs >1.0, greater than the overall average (Figure 2, Supporting Information Table S1). Spatial Patterns of Risk. Principal components analysis of ecozone/ecoprovince level variables (Figure 3) indicated that the first axis (PC1) accounted for 31.6% of total variation and sorted ecozones on the basis of decreasing mean net Hg deposition and degree of continuous forest cover and on increasing soil pH and overall proportion of barren land. Axis PC2 explained an additional 26.8% of variation and sorted ecozones/ecoprovinces on the basis of decreasing proportion of agricultural and urban land cover (Figure 3). PC1 axis scores were negatively correlated to the proportion of sites with RQs > 1.0 for reproductive and behavioral impairment in loons (Figure 4) but only marginally so for reproductive and health impairment in fish (Figure 4). Correlations with PC2 axis scores were not significant.

■

DISCUSSION

Risk quotients calculated from estimates of HgPREY and ecologically relevant screening benchmarks suggest that preyfish Hg concentrations at a number of sites across Canada may be sufficiently high as to pose a risk to piscivorous fish and common loons. Similar findings have been recently indicated for the Great Lakes region13,15 and northeastern North America30 using tissue residue approaches. Our study agrees with and extends these previous findings to a much broader geographic scale. 13096



Article

Figure 1. (a) Map of freshwater locations within Canada where screening benchmarks for common loons are exceeded and (b) boxplots of HgPREY by ecozone for locations used to calculate RQs for common loons. Boxes show median (line), 25th and 75th percentiles (end of boxes), 5th and 95th percentiles (whiskers), and outliers (dots). Screening benchmarks indicated by colored lines as in map legend. Screening benchmarks are ranked from highest (failed productivity) to lowest (impaired behavior) and locations with higher benchmarks also exceed lower ranked benchmarks. Inset panel in (a) denotes area of higher resolution. Ecozone boundaries shown are those of Environment Canada.

tissues.79 Recent speciation measurements, however, suggest that MeHg constitutes >95% of total Hg in the muscle tissue and whole body of small fishes, including yellow perch.80,81 When measured, THg concentrations in yellow perch are generally similar to those of other forage species from the same waterbody.82

is undoubtedly an oversimplification and may both over- or underestimate risk. Preferred prey size increases with body size in loons29 while walleye and northern pike are unlikely to consume only a single prey species.78 For freshwater fish species, it is generally assumed that MeHg is >90% of THg in axial muscle and whole fish1 but this may not always be the case for organ 13097



Article

Figure 2. (a) Map of freshwater locations within Canada where screening benchmarks for piscivorous fish are exceeded and (b) boxplots of HgPREY by ecozone for locations used to calculate RQs for piscivorous fish. Boxes show median (line), 25th and 75th percentiles (end of boxes), 5th and 95th percentiles (whiskers), and outliers (dots). Screening benchmarks indicated by colored lines as in map legend (mortality and growth not shown for brevity). Screening benchmarks are ranked from highest (impaired behavior) to lowest (impaired reproduction) and locations with higher ranked benchmarks also exceed lower ranked benchmarks. Inset panel in (a) denotes area of higher resolution. Ecozone boundaries shown are those of Environment Canada.

The HgPREY data set is composed of averaged model estimates for the years 1990−2010; thus, we assume that Hg concentrations in fish have remained relatively stable or changed very slowly. It is difficult to directly test for temporal variation in HgPREY as only 197 of 1936 sites were sampled more than once

between 1990 and 2010, but coefficients of variation in HgPREY within sites were low and no clear relationships were observed with temporal duration or sampling frequency.27 While this assumption may not hold true for specific locations (e.g., Canadian Arctic83), it is relatively well supported on the basis of 13098



Article

Figure 3. Principal component ordination of ecozone/ecoprovince characteristics (a) and axis loadings for the first two principal components (b). Ecozone/ecoprovince abbreviations as in Table 2

Figure 4. Relationship between the proportion of sites with RQ >1.0 for (a) loon reproductive (filled circles) and behavioral (open circles) impairment and (b) fish reproductive (filled circles) and health (open circles) impairment and PC 1 axis scores. Spearman correlation coefficients are given for each on the respective panels.

comprehensive regional assessments.84,85 While this does not imply that such trends can be extrapolated into regions examined in this study, a relatively slow rate of change in fish Hg levels is consistent with the slow turnover of legacy Hg pools in the environment. Life-history characteristics of receptors may also contribute to an under- or overestimation of exposure. Common loons can establish breeding territories on fishless lakes86,87 reduce Hg exposure by consuming invertebrates or foraging in adjacent lakes which may have biota with lower Hg levels.87 However, the presence of sufficient fish biomass appears to be a requisite for successful rearing of chicks to fledgling age;86 thus, Hg exposure to breeding loons that contribute to recruitment is less likely to be underestimated. Walleye and northern pike are long-lived, iteroparous spawners exhibiting delayed maturity and spread reproductive contributions over multiple years.88 Fecundity generally increases with the size (age) of females,32,89 and larger/ older females tend to produce larger, higher quality eggs.90 Consequently, risks may be underestimated if larger females (which can ingest larger prey91) contribute proportionately more to larval survival and recruitment success.92

Lastly, although the NDMMF as applied in this study has yet to be independently validated, our initial assessment of model performance suggested that model coefficients are relatively stable and that prediction errors are comparable to those achieved using whole ecosystem Hg cycling models.27 While this approach has its limitations, it can provide comparable predictive capacity to data intensive Hg cycling models93 but over a much larger geographic scale. Uncertainty in Screening Benchmarks. Studies of common loons in captivity and the wild have clearly demonstrated that increased altered behavior and reduced productivity are associated with increased MeHg exposure. Although impaired productivity RQs exceeded 1.0 at only 10% of sites in this assessment, this may be an overly conservative estimate of impact, as the screening benchmarks for common loons are LOAEL based. Behavioral aberrations in breeding adults may contribute to reduced productivity because the care of eggs and young is biparental. For example, inadequate incubation may result in the loss of eggs to predation or chilling39 and failure to hatch if not turned properly.94 Lethargic parental behaviors and reduced chick feeding effort may contribute to reduced 13099



Article

fledgling success.39 Impaired behavior RQs > 1.0 occurred at up to 36% of sites in this assessment and may portent a greater impact on productivity than estimated here. Despite the convincing association between MeHg exposure and reduced productivity, evidence for declines in wild loon populations is presently lacking. Metapopulation dynamics may be able to mask localized population declines if exposure is spatially variable.95 Loon populations in areas of high Hg exposure may receive a larger influx of immigration from high productivity areas, although the extent of such buffering capacity is presently unknown (N. Burgess et al. unpubl. data). However, it is important to consider that many of the ecozones identified with a high proportion of impaired productivity RQs > 1.0 cover vast regions of Ontario, Quebec, and the Atlantic provinces. These regions are home to nearly 60% of breeding pairs estimated to raise chicks in Canada,21 and further increases in MeHg exposure may eventually exceed the ability of population dynamics to offset possible declines in productivity. In contrast, screening benchmarks for fish are considerably more uncertain. This is primarily a result of a limited quantity of high-quality dietary exposure data on which to derive ecologically meaningful benchmarks.45 Variation among dietary exposure studies related to experimental protocols, species used, and end points evaluated, all contribute to uncertainty surrounding these benchmarks and ultimately the inference of risk. On the other hand, many of the subclinical effects observed in laboratory studies (e.g., gonadal atrophy, depressed circulating sex steroids, cellular or organ damage) have been documented in a number of wild fish species,96,97 including those with low tissue Hg levels (and by extension, low levels of dietary MeHg exposure98,99). Moreover, the LOAELs reported for fish are, in most cases, relatively close in magnitude to the NOAELs used here. While these findings do not necessarily imply that all populations or individuals will be demonstrably affected by MeHg exposure, further research is clearly required to reduce the uncertainty around the inferences of risk and better understand potential impacts of MeHg exposure in piscivorous fishes. Overall, the results of this study indicate that Hg concentrations in prey fish may be sufficiently high as to pose a potential risk to common loons and piscivorous fishes at a number of sites across Canada. Although it is not possible to determine the full geographic scope of sites at risk within Canada, the association between greater proportions of sites with RQs >1.0 and ecozones with extensive forest cover, low soil pH, and moderate to high Hg deposition is consistent with conceptual models of environmental Hg cycling. Reductions in atmospheric Hg deposition would likely be beneficial for piscivorous fish and loons, as well as other potential at-risk wildlife not examined in this screeninglevel assessment.

■

Present Addresses ⊥

D.C.D.: Water Science and Technology Branch, Environment Canada, Burlington, ON L7R 3A6. ¶ Biology Dept. St. Mary’s University, Halifax, NS B3H 3C3. Notes

The authors declare no competing financial interest.

■

ACKNOWLEDGMENTS The authors wish to thank the many federal and provincial agencies and academic and nongovernmental research partners who provided access to fish Hg data. Ashu Dastoor provided Canada-wide Hg deposition data. Funding was provided by Environment Canada’s Clean Air Regulatory Agenda Mercury Science Program. Comments from three anonymous reviewers improved the quality of the original manuscript.

■

ASSOCIATED CONTENT

* Supporting Information S

Full details of the spatial data sets used, variable extraction, and ecozone level tabular summary of RQ data. This information is available free of charge via the Internet at http://pubs.acs.org/.

■

REFERENCES

(1) Wiener, J. G.; Krabbenhoft, D. P.; Heinz, G. H.; Scheuhammer, A. M. Ecotoxicology of mercury. In Handbook of Ecotoxicology, 2nd ed.; Hoffman, D. J., Rattner, B. A., Burton, G. A., Cairns, J., Eds.; Lewis Publishers: Boca Raton, FL., 2003; pp 409−463. (2) Fitzgerald, W. F.; Engstrom, D. R.; Mason, R. P.; Nater, E. A. The case for atmospheric mercury contamination in remote areas. Environ. Sci. Technol. 1998, 32, 1−7. (3) Gilmour, C. C.; Henry, E. A.; Mitchell, R. Sulfate stimulation of mercury methylation in freshwater sediments. Environ. Sci. Technol. 1992, 26, 2281−2287. (4) Cabana, G.; Tremblay, A.; Kalff, J.; Rasmussen, J. B. Pelagic foodchain structure in Ontario lakes−A determinant of mercury levels in lake trout (Salvelinus namaycush). Can. J. Fish. Aquat. Sci. 1994, 51, 381−389. (5) Cristol, D. A.; Brasso, R. L.; Condon, A. M.; Fovargue, R. E.; Friedman, S. L.; Hallinger, K. K.; Monroe, A. P.; White, A. E. The movement of aquatic mercury through terrestrial food webs. Science 2008, 320, 335−335. (6) Sample, B. E.; Suter, G. W. Ecological risk assessment in a large river-reservoir: 4. Piscivorous wildlife. Environ. Toxicol. Chem. 1999, 18, 610−620. (7) Duvall, S. E.; Barron, M. G. A screening level probabilistic risk assessment of mercury in Florida Everglades food webs. Ecotoxicol. Environ. Saf. 2000, 47, 298−305. (8) Wolfe, M. F.; Schwarzbach, S.; Sulaiman, R. A. Effects of mercury on wildlife: A comprehensive review. Environ. Toxicol. Chem. 1998, 17, 146−160. (9) Shore, R. F.; Pereira, G.; Walker, L. A.; Thompson, D. R. Mercury in non-marine birds and mammals. In Environmental Contaminants in Biota: Interpreting Tissue Concentrations, 2nd ed.; Beyer, W. N., Meador, J. P., Eds.; CRC Press: Boca Raton, FL, 2011; pp 609−624. (10) Sandheinrich, M. B.; Wiener, J. G. Methylmercury in freshwater fishrecent advances in assessing toxicity of environmentally relevant exposures. In Environmental Contaminants in Biota: Interpreting Tissue Concentrations, 2nd ed.; Beyer, W. N., Meador, J. P., Eds.; CRC Press: Boca Raton, FL, 2011; pp 169−190. (11) Schmeltz, D.; Evers, D. C.; Driscoll, C. T.; Artz, R.; Cohen, M.; Gay, D.; Haeuber, R.; Krabbenhoft, D. P.; Mason, R.; Morris, K.; Wiener, J. G. MercNet: A national monitoring network to assess responses to changing mercury emissions in the United States. Ecotoxicology 2011, 20, 1713−1725. (12) Morrison, H. The Canadian Clean Air Regulatory Agenda Mercury Science Program. Ecotoxicology 2011, 20, 1512−1519. (13) Evers, D. C.; Williams, K. A.; Meyer, M. W.; Scheuhammer, A. M.; Schoch, N.; Gilbert, A. T.; Siegel, L.; Taylor, R. J.; Poppenga, R.; Perkins, C. R. Spatial gradients of methylmercury for breeding common loons in the Laurentian Great Lakes region. Ecotoxicology 2011, 20, 1609−1625. (14) Wiener, J. G.; Sandheinrich, M. B.; Bhavsar, S. P.; Bohr, J. R.; Evers, D. C.; Monson, B. A.; Schrank, C. S. Toxicological significance of mercury in yellow perch in the Laurentian Great Lakes region. Environ. Pollut. 2012, 161, 350−357.

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]; phone: 1-905-336-4790; fax: 1-905-336-4699. 13100



Article

(15) Sandheinrich, M. B.; Bhavsar, S. P.; Bodaly, R. A.; Drevnick, P. E.; Paul, E. A. Ecological risk of methylmercury to piscivorous fish of the Great Lakes region. Ecotoxicology 2011, 20, 1577−1587. (16) Depew, D. C.; Burgess, N. M.; Anderson, M. R.; Baker, R.; Bhavsar, S. P.; Bodaly, D. A.; Eckley, C. S.; Evans, M. S.; Gantner, N.; Graydon, J. A.; Jacobs, K.; LeBlanc, J. E.; St. Louis, V. L.; Campbell, L. M. An overview of mercury concentrations in freshwater fish species: A national fish mercury dataset for Canada. Can. J. Fish. Aquat. Sci. 2013, 70, 436−451. (17) USEPA. Guidelines for ecological risk assessment, EPA/630/R 5/ 002F; US Environmental Protection Agency, Washington, DC, 1998. (18) CCME. A framework for ecological risk assessment: General guidance; Canadian Council for Ministers of the Environment: Winnipeg, MB, 1996. (19) Evers, D. C. Loons as biosentinels of aquatic integrity. Environ. Bioindic. 2006, 1, 18−21. (20) Vander Zanden, M. J.; Cabana, G.; Rasmussen, J. B. Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (δ15N) and literature dietary data. Can. J. Fish. Aquat. Sci. 1997, 54, 1142−1158. (21) Status assessment and conservation plan for the common loon (Gavia immer) in North America; U.S. Fish and Wildlife Service: Hadley, MA, 2004. (22) Scott, W. B.; Crossman, E. J. Freshwater fishes of Canada. Bull. Fish. Res. Bd. Can. 1973, 184, 1−996. (23) Evers, D. C.; Clair, T. A. Mercury in northeastern North America: A synthesis of existing databases. Ecotoxicology 2005, 14, 7−14. (24) Depew, D. C.; Basu, N.; Burgess, N. M.; Campbell, L. M.; Evers, D. C.; Grasman, K. A.; Scheuhammer, A. M. Derivation of screening benchmarks for dietary methylmercury exposure for the common loon (Gavia immer): Rationale for use in ecological risk assessment. Environ. Toxicol. Chem. 2012, 31, 2399−2407. (25) Hall, B. D.; Bodaly, R. A.; Fudge, R. J. P.; Rudd, J. W. M.; Rosenberg, D. M. Food as the dominant pathway of methylmercury uptake by fish. Water Air Soil Poll. 1997, 100, 13−24. (26) MacCrimmon, H. R.; Wren, C. D.; Gots, B. L. Mercury uptake by lake trout, Salvelinus namaycush, relative to age, growth, and diet in Tadenac lake with comparative data from other pre-Cambrian shield lakes. Can. J. Fish. Aquat. Sci. 1983, 40, 114−120. (27) Depew, D. C.; Burgess, N. M.; Campbell, L. M. Modeling mercury concentrations in prey fish: Derivation of a national-scale common indicator of dietary mercury exposure for piscivorous fish and wildlife. Environ. Pollut. 2013, 176, 234−243. (28) Craig, J. The biology of perch and related fishes; Timber Press: Portland, OR, 1987. (29) Barr, J. F. Aspects of common loon (Gavia immer) feeding biology on its breeding ground. Hydrobiology 1996, 321, 119−144. (30) Asessing the impacts on piscivorous wildlife using a wildlife criterion value based on the common loon, 1998−2003. Report No 2004-05; BioDiversity Research Institute: Gorham, ME, 2004. (31) Chapman, L. J.; Mackay, W. C. Ecological correlates of feeding flexibility in northern pike (Esox lucius). J. Freshwater Ecol. 1990, 5, 313− 322. (32) Synopsis of biological data on the walleye (Stizostedion vitreum) Mitchill 1818. FAO Fisheries Synopsis, No 119; Food and Agriculture Organization of the United Nations: Rome, Italy, 1979; 148 pp. (33) Burgess, N. M.; Meyer, M. W. Methylmercury exposure associated with reduced productivity in common loons. Ecotoxicology 2008, 17, 83−91. (34) Metal accumulations in fishes from Muskoka - Haliburton lakes in Ontario (1978−1984). Ontario Ministry of Environment: Rexdale, Ontario, 1987; 47 pp. (35) Neilson, L. A. Effect of walleye (Stizostedion vitreum) predation on juvenile mortality and recruitment of yellow perch (Perca f lavescens) in Oneida Lake, NY. Can. J. Fish. Aquat. Sci. 1980, 37, 11−19. (36) Nursall, J. R. Some behavioral interactions of spottail shiners (Notropis hudsonius), yellow perch (Perca f lavenscens) and northern pike (Esox lucius). J. Fish. Res. Bd. Can. 1973, 30, 1161−1178.

(37) Bodaly, R. A. D.; Jansen, W. A.; Majewski, A. R.; Fudge, R. J. P.; Strange, N. E.; Derksen, A. J.; Green, D. J. Post-impoundment time course of increased mercury concentrations in fish in hydroelectric reservoirs of northern Manitoba, Canada. Arch. Environ. Contam. Toxicol. 2007, 53, 379−389. (38) Population dynamics of the common loon (Gavia immer) associated with mercury-contaminated waters in northwestern Ontario. Occasional Paper No 56; Canadian Wildlife Service: Ottawa, Ontario, 1986. (39) Evers, D. C.; Savoy, L. J.; DeSorbo, C. R.; Yates, D. E.; Hanson, W.; Taylor, K. M.; Siegel, L. S.; Cooley, J.H., Jr.; Bank, M. S.; Major, A.; Munney, K.; Mower, B. F.; Vogel, H. S.; Schoch, N.; Pokras, M.; Goodale, M. W.; Fair, J. Adverse effects from environmental mercury loads on breeding common loons. Ecotoxicology 2008, 17, 69−81. (40) Burgess, N. M.; Evers, D. C.; Kaplan, J. D. Mercury and other contaminants in common loons breeding in Atlantic Canada. Ecotoxicology 2005, 14, 241−252. (41) Common Loon (Gavia immer), The birds of North America Online. The Birds of North America, 2010; http://bna.birds.cornell.edu/ bna/species/313/articles/introduction. (42) Mitro, M. G.; Evers, D. C.; Meyer, M. W.; Piper, W. H. Common loon survival rates and mercury in New England and Wisconsin. J. Wildl. Manage. 2008, 72, 665−673. (43) Friedmann, A. S.; Watzin, M. C.; BrinckJohnsen, T.; Leiter, J. C. Low levels of dietary methylmercury inhibit growth and gonadal development in juvenile walleye (Stizostedion vitreum). Aquat. Toxicol. 1996, 35, 265−278. (44) Effects of mercury contaminated diet upon walleyes, Stizostedion vitreum vitreum (Mitchill). Fisheries and Marine Service Technical Report No 597, Department of Fisheries and Oceans Canada: Winnipeg, MB, 1975; 21 pp. (45) Depew, D. C.; Basu, N.; Burgess, N. M.; Campbell, L. M.; Devlin, E. W.; Drevnick, P. E.; Hammerschmidt, C. R.; Murphy, C. A.; Sandheinrich, M. B.; Wiener, J. G. Toxicity of dietary methylmercury to fish: Derivation of ecologically meaningful threshold concentrations. Environ. Toxicol. Chem. 2012, 31, 1536−1547. (46) Beckvar, N.; Dillon, T. M.; Read, L. B. Approaches for linking whole-body fish tissue residues of mercury or DDT to biological effects thresholds. Environ. Toxicol. Chem. 2005, 24, 2094−2105. (47) A Statistical Model and National Dataset for Partitioning Fish-Tissue Mercury concentration between Spatio-temporal and Sample Characteristic Effects. United States Geological Survey Scientific Investigation Report 2004-5199; United States Geological Survey: Reston, VA, 2004; 21 pp. (48) Minns, C. K.; Moore, J. E.; Shuter, B. J.; Mandrak, N. E. A preliminary national analysis of some key characteristics of Canadian lakes. Can. J. Fish. Aquat. Sci. 2008, 65, 1763−1778. (49) Driscoll, C. T.; Han, Y.; Chen, C. Y.; Evers, D. C.; Lambert, K. F.; Holsen, T. M.; Kamman, N. C.; Munson, R. K. Mercury contamination in forest and freshwater ecosystems in the northeastern United States. Biosci. 2007, 57, 17−28. (50) Evers, D. C.; Han, Y.; Driscoll, C. T.; Kamman, N. C.; Goodale, M. W.; Lambert, K. F.; Holsen, T. M.; Chen, C. Y.; Clair, T. A.; Butler, T. Biological mercury hotspots in the northeastern United States and southeastern Canada. Bioscience 2007, 57, 29−43. (51) Ecological Stratification Working Group. A National Ecological Framework for Canada; Agriculture and Agrifood Canada and Environment Canada: Ottawa, ON, 1995. (52) Environmental Systems Research Institute, Redlands, CA. ArcMap 9.3.1; 2009. (53) Stacklies, W.; Redestig, H.; Scholz, M.; Walther, D.; Selbig, J. pcaMethodsa bioconductor package providing PCA methods for incomplete data. Bioinformatics 2007, 23, 1164−1167. (54) R Core Development Team R: A language and environment for statistical computing; Vienna, Austria, 2010. (55) 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, 12−19. (56) Frederick, P.; Jayasena, N. Altered pairing behaviour and reproductive success in white ibises exposed to environmentally relevant concentrations of methylmercury. Proc. R. Soc. B 2011, 278, 1851−1857. 13101



Article

(76) Peterson, S. A.; Van Sickle, J.; Herlihy, A. T.; Hughes, R. M. Mercury concentration in fish from streams and rivers throughout the western United States. Environ. Sci. Technol. 2007, 41, 58−65. (77) Kamman, N. C.; Burgess, N. M.; Driscoll, C. T.; Simonin, H. A.; Goodale, W.; Linehan, J.; Estabrook, R.; Hutcheson, M.; Major, A.; Scheuhammer, A. M.; Scruton, D. A. Mercury in freshwater fish of northeast North America–a geographic perspective based on fish tissue monitoring databases. Ecotoxicology 2005, 14, 163−180. (78) Mathers, R. A.; Johansen, P. H. The effects of feeding ecology on mercury accumulation in walleye (Stizostedion vitreum) and pike (Esox lucius) in Lake Simcoe. Can. J. Zool. 1985, 63, 2006−2012. (79) Barst, B. D.; Hammerschmidt, C. R.; Chumchal, M. M.; Muir, D. C.; Smith, J. D.; Roberts, A. P.; Rainwater, T. R.; Drevnick, P. E. Determination of mercury speciation in fish tissue with a direct mercury analyzer. Environ. Toxicol. Chem. 2013, 32, 1237−1241. (80) Wyn, B.; Kidd, K. A.; Burgess, N. M.; Curry, R. A.; Munkittrick, K. R. Increasing mercury in yellow perch at a hotspot in Atlantic Canada, Kejimkujik National Park. Environ. Sci. Technol. 2010, 44, 9176−9181. (81) Chumchal, M. M.; Rainwater, T. R.; Osborn, S. C.; Roberts, A. P.; Abel, M. T.; Cobb, G. P.; Smith, P. N.; Bailey, F. C. Mercury speciation and biomagnification in the food web of Caddo Lake, Texas and Louisiana, USA, a subtropical freshwater ecosystem. Environ. Toxicol. Chem. 2011, 30, 1153−1162. (82) Swanson, H. K.; Johnston, T. A.; Leggett, W. C.; Bodaly, R. A.; Doucett, R. R.; Cunjak, R. A. Trophic positions and mercury bioaccumulation in rainbow smelt (Osmerus mordax) and native forage fishes in northwestern Ontario lakes. Ecosystems 2003, 6, 289−299. (83) Carrie, J.; Wang, F.; Sanei, H.; Macdonald, R. W.; Outridge, P. M.; Stern, G. A. Increasing contaminant burdens in an Arctic fish, burbot (Lota lota), in a warming climate. Environ. Sci. Technol. 2010, 44, 316− 322. (84) Monson, B. A.; Staples, D. F.; Bhavsar, S. P.; Holsen, T. M.; Schrank, C. S.; Moses, S. K.; McGoldrick, D. J.; Backus, S. M.; Williams, K. A. Spatiotemporal trends of mercury in walleye and largemouth bass from the Laurentian Great Lakes region. Ecotoxicology 2011, 20, 1555− 1567. (85) Rasmussen, P. W.; Schrank, C. S.; Campfield, P. A. Temporal trends of mercury concentrations in Wisconsin walleye (Sander vitreus), 1982−2005. Ecotoxicology 2007, 16, 541−550. (86) Gingras, B. A.; Paszkowski, C. A. Feeding behavior and modeled energetic intake of common loon (Gavia immer) adults and chicks on small lakes with and without fish. Hydrobiology 2006, 567, 247−261. (87) Merrill, E. H.; Hartigan, J. J.; Meyer, M. W. Does prey biomass or mercury exposure affect loon chick survival in Wisconsin? J. Wildl. Manage. 2005, 69, 57−67. (88) Winemiller, K. O.; Rose, K. A. Patterns of life-history diversification in North American fishes: Implications for population regulation. Can. J. Fish. Aquat. Sci. 1992, 49, 2196−2218. (89) Carbine, W. F. Egg production of the northern pike Esox lucius L., and the percentage survival of eggs and young on the spawining grounds. Pap. Mich. Acad. Sci. 1943, 29, 123−138. (90) Roff, D. A. The Evolution of Life Histories: Theory and Analysis; Chapman-Hall: New York, NY, 1992. (91) Henderson, B. A.; Collins, N.; Morgan, G. E.; Vaillancourt, A. Sexual size dimorphism of walleye (Stizostedion vitreum vitreum). Can. J. Fish. Aquat. Sci. 2003, 60, 1345−1352. (92) Venturelli, P. A.; Murphy, C. A.; Shuter, B. J.; Johnston, T. A.; van Coeverden de Groot, P. J.; Boag, P. T.; Casselman, J. M.; Montgomerie, R.; Wiegand, M. D.; Leggett, W. C. Maternal influences on population dynamics: Evidence from an exploited freshwater fish. Ecology 2010, 91, 2003−2012. (93) Knightes, C. D.; Ambrose, R. B. Evaluating regional predictive capacity of a process-based mercury exposure model, regional-mercury cycling model, applied to 91 Vermont and New Hampshire lakes and ponds, USA. Environ. Toxicol. Chem. 2007, 26, 807−815. (94) Herring, G.; Ackerman, J. T.; Eagles-Smith, C. A. Embryo malposition as a potential mechanism for mercury-induced hatching failure in bird eggs. Environ. Toxicol. Chem. 2010, 29, 1788−1794.

(57) Heinz, G. H. Methylmercury - Reproductive and behavioraleffects on 3 generations of Mallard ducks. J. Wildl. Manage. 1979, 43, 394−401. (58) Heinz, G. H.; Hoffman, D. J.; Klimstra, J. D.; Stebbins, K. R.; Kondrad, S. L.; Erwin, C. A. Teratogenic effects of injected methylmercury on avian embryos. Environ. Toxicol. Chem. 2011, 30, 1593−1598. (59) Kenow, K. P.; Meyer, M. W.; Rossmann, R.; Gendron-Fitzpatrick, A.; Gray, B. R. Effects of injected methylmercury on the hatching of common loon (Gavia immer) eggs. Ecotoxicology 2011, 20, 1684−1693. (60) Crump, K. L.; Trudeau, V. L. Mercury-induced reproductive impairment in fish. Environ. Toxicol. Chem. 2009, 28, 895−907. (61) Hammerschmidt, C. R.; Sandheinrich, M. B.; Wiener, J. G.; Rada, R. G. Effects of dietary methylmercury on reproduction of fathead minnows. Environ. Sci. Technol. 2002, 36, 877−883. (62) Alvarez, M. D.; Murphy, C. A.; Rose, K. A.; McCarthy, I. D.; Fuiman, L. A. Maternal body burdens of methylmercury impair survival skills of offspring in Atlantic croaker (Micropogonias undulatus). Aquat. Toxicol. 2006, 80, 329−337. (63) Matta, M. B.; Linse, J.; Cairncross, C.; Francendese, L.; Kocan, R. M. Reproductive and transgenerational effects of methylmercury or Aroclor 1268 on Fundulus heteroclitus. Environ. Toxicol. Chem. 2001, 20, 327−335. (64) Muir, D. C. G.; Wang, X.; Yang, F.; Nguyen, N.; Jackson, T. A.; Evans, M. S.; Douglas, M.; Koeck, G.; Lamoureux, S.; Pienitz, R.; Smol, J. P.; Vincent, W. F.; Dastoor, A. Spatial trends and historical deposition of mercury in eastern and northern Canada inferred from lake sediment cores. Environ. Sci. Technol. 2009, 43, 4802−4809. (65) Nasr, M.; Ogilvie, J.; Castonguay, M.; Rencz, A.; Arp, P. A. Total Hg concentrations in stream and lake sediments: Discerning geospatial patterns and controls across Canada. Appl. Geochem. 2011, 26, 1818− 1831. (66) Jeffries, D. S.; Brydges, T. G.; Dillon, P. J.; Keller, W. Monitoring the results of Canada/U.S.A acid rain control programs: Some lake responses. Environ. Monit. Assess. 2003, 88, 3−19. (67) Dupont, J.; Clair, T.; Gagnon, C.; Jeffries, D.; Kahl, J.; Nelson, S.; Peckenham, J. Estimation of critical loads of acidity for lakes in northeastern United States and eastern Canada. Environ. Monit. Assess. 2005, 109, 275−292. (68) Jeffries, D. S.; Semkin, R. S.; Gibson, J. J.; Wong, I. Recently surveyed lakes in northern Manitoba and Saskatchewan, Canada: Characteristics and critical loads of acidity. J. Limnol. 2010, 69, 45−55. (69) Prestbo, E. M.; Gay, D. A. Wet deposition of mercury in the US and Canada, 1996−2005: Results and analysis of the NADP mercury deposition network (MDN). Atmos. Environ. 2009, 43, 4223−4233. (70) Drevnick, P. E.; Engstrom, D. R.; Driscoll, C. T.; Swain, E. B.; Balogh, S. J.; Kamman, N. C.; Long, D. T.; Muir, D. G. C.; Parsons, M. J.; Rolfhus, K. R.; Rossmann, R. Spatial and temporal patterns of mercury accumulation in lacustrine sediments across the Laurentian Great Lakes region. Environ. Pollut. 2012, 161, 252−260. (71) Jeffries, D. S.; Clair, T. A.; Couture, S.; Dillon, P. J.; Dupont, J.; Keller, W.; McNicol, D. K.; Turner, M. A.; Vet, R.; Weeber, R. Assessing the recovery of lakes in southeastern Canada from the effects of acidic deposition. Ambio 2003, 32, 176−182. (72) Chen, C. Y.; Stemberger, R. S.; Kamman, N. C.; Mayes, B. M.; Folt, C. L. Patterns of Hg bioaccumulation and transfer in aquatic food webs across multi-lake studies in the northeast US. Ecotoxicology 2005, 14, 135−147. (73) Evers, D. C.; Taylor, K. M.; Major, A.; Taylor, R. J.; Poppenga, R. H.; Scheuhammer, A. M. Common loon eggs as indicators of methylmercury availability in North America. Ecotoxicology 2003, 12, 69−81. (74) Evers, D. C.; Kaplan, J. D.; Meyer, M. W.; Reaman, P. S.; Braselton, W. E.; Major, A.; Burgess, N.; Scheuhammer, A. M. Geographic trend in mercury measured in common loon feathers and blood. Environ. Toxicol. Chem. 1998, 17, 173−183. (75) Scheuhammer, A. M.; Perrault, J. A.; Bond, D. E. Mercury, methylmercury, and selenium concentrations in eggs of common loons (Gavia immer) from Canada. Environ. Monit. Assess. 2001, 72, 79−94. 13102



Article

(95) Raimondo, S.; Barron, M. G. Population-level modeling of mercury stress in the Florida panther (Puma concolor coryi) metapopulation. In Demographic toxicity: Methods in Ecological Risk Assessment; Akcakaya, H. R., Ed.; Oxford University Press: New York, NY, 2008; pp 40−53. (96) Barst, B. D.; Gevertz, A. K.; Chumchal, M. M.; Smith, J. D.; Rainwater, T. R.; Drevnick, P. E.; Hudelson, K. E.; Hart, A.; Verbeck, G. F.; Roberts, A. P. Laser ablation ICP-MS co-localization of mercury and immune response in fish. Environ. Sci. Technol. 2011, 45, 8982−8988. (97) Batchelar, K. L.; Kidd, K. A.; Munkittrick, K. R.; Drevnick, P. E.; Burgess, N. M. Reproductive health of yellow perch (Perca f lavescens) from a biological mercury hotspot in Nova Scotia, Canada. Sci. Total Environ. 2013, 454−455C, 319−327. (98) Friedmann, A. S.; Costain, E. K.; MacLatchy, D. L.; Stansley, W.; Washuta, E. J. Effect of mercury on general and reproductive health of largemouth bass (Micropterus salmoides) from three lakes in New Jersey. Ecotoxicol. Environ. Saf. 2002, 52, 117−122. (99) Webb, M.; Feist, G.; Fitzpatrick, M.; Foster, E.; Schreck, C.; Plumlee, M.; Wong, C.; Gundersen, D. Mercury concentrations in gonad, liver, and muscle of white sturgeon Acipenser transmontanus in the lower Columbia River. Arch. Environ. Contam. Toxicol. 2006, 50, 443−451.

13103


Spatial Patterns of Methylmercury Risks to Common Loons

Recommend Documents