Article pubs.acs.org/est
Hair Mercury Concentrations in Western Hudson Bay Polar Bear Family Groups Thea Bechshoft,*,† Andrew E. Derocher,† Evan Richardson,‡ Nicholas J. Lunn,‡ and Vincent L. St. Louis† †
Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada Wildlife Research Division, Science and Technology Branch, Environment and Climate Change Canada, University of Alberta, CW405, Biological Sciences Building, Edmonton, AB T6G 2E9, Canada
‡
ABSTRACT: Methylmercury is one of the more toxic forms of mercury (Hg), the biomagnification of which is prevalent in the Arctic where apex predators such as polar bears (Ursus maritimus) can carry high loads. The maternal transfer of contaminants to offspring is a concern, as offspring may be particularly sensitive to the effects of environmental pollutants during early development. However, few studies of polar bears report on Hg in dependent young. We examined hair total Hg (THg) concentrations in 24 polar bear family groups in western Hudson Bay: mother, cub-of-the-year (COY), yearling, and 2 year old. THg concentrations increased with bear age, with COYs having lower concentrations than other offspring groups (p ≤ 0.008). Using AICcbased regression models, we found maternal THg to be positively related to body condition and litter size, while overall offspring THg was positively related to maternal body condition in addition to being dependent on the sex and age of the offspring. COY THg concentrations were positively related to maternal THg while also depending on the sex of the offspring. Considering our results, future studies in polar bear ecotoxicology are encouraged to include offspring of different ages and sexes.
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INTRODUCTION Methylmercury (MeHg) is one of the more toxic forms of mercury (Hg) in that it biomagnifies through food chains.1−3 This biomagnification is particularly evident in the Arctic marine ecosystem, where apex predators such as polar bears (Ursus maritimus) can carry high loads of Hg,2,4 which may have neurological, histopathological, and endocrine effects.5−9 Polar bear offspring stay with their mother for up to 2.5 years.10 During early development, they are dependent on milk before gradually transitioning to solid food.11,12 Harmful contaminants, such as MeHg and persistent organic pollutants, are transferred from mothers to gestating and unweaned offspring.13,14 This may affect polar bear offspring health as well as their long-term fitness, as organisms are particularly sensitive to the effects of environmental pollutants during prenatal and early development.15−18 However, despite numerous ecotoxicological studies of Hg in polar bears,7,19,20 only four studies have examined Hg accumulation in dependent young.14,21−23 Of these, only one examined dependent offspring < 1 year old.14 Similar patterns hold true for polar bear studies focusing on other contaminants, in that only a few of these publications include offspring of < 2 years of age.24−27 Of the polar bear toxicology studies that have included dependent young, some have found this group to differ not only from adults but also within the group of dependent young according to sex or specific age, e.g., in contaminant intake or antibody and hormone concentrations.14,24,28,29 Variation in physiological © 2016 American Chemical Society
responses to contaminants is to be expected between dependent offspring life stages (e.g., when changing from milk to primarily solid food) as well as between the sexes, as male and female mammals differ in their endocrine, neurological, morphological, and physiological profile already in their early development.17,30−33 The aim of this study was to examine variation in hair total Hg (THg; all forms of Hg in a sample) concentration in polar bear family groups from western Hudson Bay, including dependent cubs-of-the-year (COYs), yearlings, 2 year olds, and their mothers. Our objectives were to (1) investigate the relationship between THg concentrations of mothers and dependent offspring and (2) describe differences in THg concentrations between offspring of different ages in relation to sex, body condition, and number of siblings.
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EXPERIMENTAL SECTION Polar Bear Hair Samples. As part of ongoing research on the ecology, population dynamics, and status of polar bears in western Hudson Bay, Canada, adult females accompanied by offspring were sampled in September 2014 and 2015 by chemical immobilization.34 Guard hairs (< 2 g) were collected Received: Revised: Accepted: Published: 5313
January 28, 2016 March 29, 2016 April 20, 2016 April 20, 2016 DOI: 10.1021/acs.est.6b00483 Environ. Sci. Technol. 2016, 50, 5313−5319
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Environmental Science & Technology
concentrations acquired from the digestion and DMA techniques (Figure 1; Pearson’s correlation test: t = 26.3, df =12, p < 0.0001, r = 0.99).
from the rump of each bear. The bear’s sex was determined in the field as was individual fatness (body condition), which was scored on a scale from 1 (emaciated) to 5 (obese).35 While the scale ranks from 1 to 5, the polar bears included in our study scored between 1 and 3. Weight was estimated from axillary girth and body-length measurements.36 The age of the adult bears was estimated by counting cementum tooth-growth-layer groups,37 and age of offspring was determined using body size and dentition. Age was missing for one adult female but substituted with the mean age of the remaining 23 individuals within that group. Assuming offspring were born in December, we classified 9 month old offspring as COYs, 21 month old offspring as yearlings, and 33 month old offspring as 2 year olds. The data set consisted of 24 family groups (2014: 13, 2015: 11) with 33 offspring: 25 COYs (2014: 12, 2015: 13), seven yearlings (2014: 4, 2015: 3), and one 2 year old (2014: 1, 2015: 0). The mean age of the mothers was 14 years (range: 8− 24 years). A total of nine families consisted of a mother with twin COYs (two male−male, seven female−male), and 15 families consisted of a mother with a single offspring (10 female [five COY, four yearling, one 2 year old] and five male [two COY, three yearling]). Mercury Analysis. Dietz et al.38 found that 97% of the THg in polar bear hair existed in its organic form, MeHg. The guardhair samples were thus analyzed for concentrations of THg according to the procedure outlined in St. Louis et al.3 Hair samples were washed before analyses to remove repellant oils and extraneous dirt. Hair was agitated using stainless steel forceps in warm Milli-Q water containing a small amount of mild dishwashing detergent and then rinsed three times with Milli-Q water and air-dried overnight in the University of Alberta Biogeochemical Analytical Service Laboratory (BASL; Edmonton, Canada) class 100 clean room. Hair samples were analyzed for THg in the BASL using standard protocols. The 2014 whole-hair samples (20 mg) were digested in 60 mL sealed Teflon digestion vessels using 7 mL of 7:3 (v/v) HNO3−H2SO4. Digestion vessels were heated in a vented oven for 2 h at 125 °C. Once cooled, 19 mL of Milli-Q water and 1 mL of BrCl were added to each digestion vessel, and vessels were reheated overnight at 60 °C. A 0.5 mL subsample of the digest was then diluted with Milli-Q water to a final volume of 50 mL, and 0.04% (v/v) hydroxylamine hydrochloride was added to neutralize excess BrCl. Sample reduction, delivery, and cold-vapor atomic fluorescence detection were accomplished using an automated Tekran 2600 THg analyzer. Spike recoveries in samples were 98.9 ± 11.6%, and duplicate analyses were within 10% of one another. Mean concentrations of THg measured in Certified Reference Materials (National Research Council Canada) Mess-3 and DORM-3 (89.0 ± 5.2 ng/g and 373.9 ± 15.3 ng/g, respectively) were within their certified ranges. The 2015 whole hair samples were analyzed using a Milestone Direct Mercury Analyzer (DMA-80). Hair samples (9−11 mg) were placed into nickel sample boats and analyzed using the DMA-80, which was calibrated using 10 liquid Hg standards (0−1000 ng; Fisher Scientific) placed in quartz sample boats. Average concentrations of THg measured in Certified Reference Materials IAEA-086 (certified range 0.534− 0.612 mg/kg) and DORM-3 (certified range 0.322−0.442 mg/ kg) were within their certified ranges. All data are given in ng/g dry weight (dw). The analytical limit of detection for both methods was 0.5 ng/g. After analyzing eight polar-bear-hair samples, as well as three DORM-3 and three Mess-3 SRM samples, we found no significant difference in THg
Figure 1. Total mercury (THg) concentrations as measured in three DORM-3 samples, three Mess-3 samples, and eight polar-bear hair samples using the two analysis techniques applied in the present study: the DMA method and the acid-digest method (see text for further details). A 1:1 reference line was added to the plot.
Statistical Analysis. THg concentrations were normalized with a log10 transformation following an assessment for normality by use of visual data inspection as well as Shapiro normality tests. To allow for easier assessment of biological relevance, however, THg concentrations were plotted as the original μg/g in Figures 1−4. A Student’s t test was applied to test whether sibling offspring should be treated as dependent or independent data points. Relation to THg concentrations of body condition variables (fatness versus weight) were tested using Pearson’s correlation tests in adults and offspring, respectively, before choosing which of these to include in further analyses. Finally, the influence of the year was assessed using a Student’s t test. Regression analyses were conducted without interactions due to low sample size. In the regression models, the final minimal adequate model was determined by comparing the corrected Akaike Information Criterion (AICc) values calculated by a backward-step model simplification function: the initial model was fitted with all variables, after which it was successively refitted by dropping the leastsignificant variable (with respect to calculated AICc value) until only those variables resulting in the lowest AICc score were left in the final minimal adequate model (defined as the best tradeoff between goodness-of-fit and model simplicity). All statistical analyses were conducted using R version 3.0.2.39 Statistical significance was set to p ≤ 0.05, with p ≤ 0.1 considered a statistically significant trend. Means are presented ± 1 standard deviation. An ANOVA followed by a Tukey’s HSD test was used to investigate differences in THg concentrations between offspring groups (COY, yearling, 2 year old), and adults. A multiple regression model was developed to examine variation in maternal THg concentration in response to litter size, offspring age, maternal age, and maternal fatness (a categorical variable). The regression analysis for mothers was run twice, once including and once excluding the single 2 year old in the data set. THg concentrations in offspring were examined as a 5314
DOI: 10.1021/acs.est.6b00483 Environ. Sci. Technol. 2016, 50, 5313−5319
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Environmental Science & Technology
trations: in adults, it was fatness (fatness: t = 1.6, df = 22, p = 0.1, r = 0.33; weight: t = 0.2, df = 22, p = 0.9, r = 0.04), while for offspring it was weight (fatness: t = 1.3, df =31, p = 0.2, r = 0.23; weight: t = 5.4, df = 31, p < 0.00, r = 0.70). The regression analysis AICc-determined minimal adequate model (r2 = 0.32, F3,20 = 3.2, p = 0.04) retained two predictors of maternal THg concentrations: fatness (score 2: p = 0.07, β = 0.57; score 3: p = 0.02, β = 0.79) and litter size (p = 0.08, β = 0.42). The same analysis, excluding the single 2 year old, retained the same two predictors: fatness (score 2: p = 0.12, β = 0.48; score 3: p = 0.04, β = 0.52; Figure 3a) and litter size (p = 0.04, β = 0.52; Figure 3b) (overall minimal model: r2 = 0.37, F3,19 = 3.7, p = 0.03). The AICc-determined minimal adequate model for THg concentrations in all offspring (r2 = 0.76, F5,14 = 9.10, p < 0.0001) retained maternal fatness, offspring age, and sex of offspring. Offspring THg significantly increased with age (yearling: p < 0.0001, β = 0.81, 2 year old: p = 0.003, β = 0.48) and with maternal fatness (score 2: p = 0.07, β = 0.35, score 3: p = 0.80, β = 0.05). In addition, male offspring had higher THg concentrations than their female counterparts (p = 0.12, β = 0.23). When the same regression analysis was run for all offspring except the single 2 year old, the retained variables were offspring age, sex of offspring, and maternal THg concentration (overall minimal model: r2 = 0.68, F3,15 = 10.5, p < 0.0001). THg concentration increased with maternal THg (p = 0.09, β = 0.26; Figure 3c) as well as with offspring age (yearling: p < 0.0001, β = 0.82; Figure 3e), in addition to which male offspring had higher THg concentrations than their female counterparts (p = 0.19, β = 0.21; Figure 3d). When COYs were analyzed on their own, the AICc-determined model retained maternal THg concentration and sex of offspring as predictors of COY THg concentrations (minimal adequate model: r2 = 0.31, F2,12 = 2.67, p = 0.11). COY THg concentrations were positively linked to maternal THg concentrations (p = 0.09, β = 0.45; Figure 3f) and higher in male COYs (p = 0.16, β = 0.36; Figure 3g). Maternal fatness, however, was not significantly different between mothers with a singleton COY and those with twin COYs (t = −0.71, df =7.29, p = 0.50).
function of maternal THg concentration and fatness, sex of offspring, offspring group, and offspring weight, using multiple regression analyses (choice of maternal variables were based on results from the previous regression model). These analyses were run including and then excluding the single 2 year old in the data set. Finally, as COY was the only offspring group with singletons as well as twins, a multiple-regression analysis was done for this group only, with COY THg concentration as the response variable and maternal THg concentrations as well as sex of the COY, number of siblings, and weight of COY as explanatory variables. To avoid overfitting the regression model and to remove the effect of maternal fatness, we included only mothers with fatness scores of 2 in this last analysis, as these made up 2/3 of the COY-related data. The relationship between number of COYs and maternal fatness was instead tested using a Student’s t test.
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RESULTS Sibling offspring were no more similar within their group than they were with their singleton peers (t = 1.6, df =23, p = 0.13) and were thus treated as independent data points. Hair THg concentrations increased with age (Figure 2) but did not differ
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Figure 2. Box-and-whiskers plot of the concentration of total mercury (THg) in hair from western Hudson Bay polar bears in September 2014 and 2015. COY (9 months old, n = 25); yearling (21 months old, n = 7); 2 year old (33 months old, n = 1); and mothers (8−24 years old, n = 24). The median data value is displayed within the box, which is defined at either end by the lower and upper (25% and 75%) quartiles of the data. The whiskers are determined by the minimum and maximum data values.
DISCUSSION Our analysis revealed an age-related increment in hair THg, with older animals having higher concentrations. As discussed below, this is partly due to differences in food intake. In addition, it may be linked to polar bears accumulating Hg with age in liver and kidney tissue,40 although Born et al.23 found no relationship between polar-bear age and hair THg. COYs and yearlings were included in a few earlier Hg hair studies14,21−23 but were not analyzed by age class with the exception of by Knott et al.14 A couple of studies reported values for offspring groups directly comparable with those of our study: a mean THg concentration of 3.33 μg/g (range: 1.5−5.1 μg/g, n = 3) was reported for COY museum specimens from the Canadian Arctic,21 while in Svalbard and Greenland, a single COY had a value of 0.34 μg/g, and yearlings had a mean of 4.12 μg/g (range: 1.04−9.51 μg/g, n = 5).23 These COY mean THg concentrations are, respectively, 1.6 times higher21 and 6 times lower23 than the COY mean we found for western Hudson Bay, while the yearling mean was similar to our values. The observed differences are likely linked to variations in time period, geographical location, and trophic level of prey.2,3,40 In our study, the mean maternal THg concentration was slightly
between years (t = 0.7, df = 46.3, p = 0.5). The lowest concentrations were found in COYs, and the highest were found in adult bears: COYs (mean: 2.1 ± 0.8 μg/g; range: 1.0− 3.9 μg/g,) < yearlings (mean: 4.6 ± 0.9 μg/g; range: 3.7−6.2 μg/g) < two-year old (4.9 μg/g), and < adult (mean: 5.4 ± 0.8 μg/g; range: 4.3−7.2 μg/g). Hg concentrations varied between age groups (F3,53 = 60.0, p < 0.001) but only significantly so between COYs and each of the other groups (Tukey’s HSD, yearling: p < 0.001; 2 year old: p = 0.008; adult: p < 0.001). There was an increase but no significant differences in THg concentrations between the three oldest groups (yearling, 2year-old, and adult; all p > 0.44). Adults and offspring differed with regards to which body condition variable was a better predictor of THg concen5315
DOI: 10.1021/acs.est.6b00483 Environ. Sci. Technol. 2016, 50, 5313−5319
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Figure 3. (a−g) Plots of the variables retained in the AICc-based minimal adequate regression analysis models (see text for details). (a) Maternal hair total mercury (THg) in relation to fatness index score, (b) maternal hair THg in relation to number of offspring, (c) offspring hair THg in relation to maternal hair THg, (d) offspring hair THg in relation to sex of offspring, (e) offspring hair THg in relation to offspring age class (COY: cub of the year), (f) COY hair THg in relation to maternal THg, and (g) COY hair THg in relation to sex of COY.
importance as the western Hudson Bay polar bear subpopulation is already under duress due to the effects of climate change.41,42 An increase in pollutants such as Hg may add to
higher than those previously reported for western Hudson Bay,2,3,9 bringing it to the neurological effects level threshold value of 5.4 μg/g suggested by Dietz et al.8 This is of particular 5316
DOI: 10.1021/acs.est.6b00483 Environ. Sci. Technol. 2016, 50, 5313−5319
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Environmental Science & Technology the cumulative adverse population-level effects experienced in this subpopulation beyond those caused by habitat loss alone.43 Polar bears are born with lanugo, a sparse hair coat that is replaced with longer guard hair and a woolly undercoat starting approximately 2 weeks after birth.44,45 THg concentrations measured in the COYs in our study are thus likely the result of gestational transfer via blood, postnatal transfer through nursing, and, after some time, through the consumption of prey killed by their mothers.12 Given our current knowledge about polar bear hair growth patterns, the THg concentration found in mothers with COYs, as well as that of the older offspring, likely represents the accumulation of Hg ingested in the autumn and winter months before the year of sampling.23,46,47 Our finding that only the THg concentrations of offspring under the age of 2 were related to maternal THg concentration supports the understanding of a shift in the uptake pathway as offspring age, from a gestational and lactational transfer directly from the mothers to offspring to a gradual increase in Hg ingested directly via the consumption of prey.12,14,48 Maternal hair THg concentrations were positively correlated with maternal fatness and litter size. Maternal energy expenditure increases with litter size, and although there was no significant difference in maternal fatness, other tissues may be mobilized to facilitate offspring development. Furthermore, higher energetic demands may lead to higher prey intake, which could lead to a higher intake also of Hg.19 St Louis et al.;3 however, found no difference in hair THg concentrations between adult females with and without offspring (of unspecified age). Furthermore, our regression models did not test for interactions between variables. Hence, relationships such as the positive interactions between polar bear maternal age and maternal body condition, litter size, and litter weight reported elsewhere42 could not be examined in our study. THg concentration in offspring overall was dependent on their age and sex as well as maternal fatness score. This result, however, appeared to be driven by the one 2 year old in the data set; when the same analysis was run on all offspring excluding this 2 year old, the THg concentration depended on offspring age and sex, as well as maternal THg concentration. That the one 2 year old could, in itself, cause a change in the results supports the division of dependent offspring into age subcategories in future polar bear family group analyses. THg concentrations in COYs were likewise related to the sex of the COY as well as the maternal THg concentration. The overall tendency found here for male offspring to have higher THg concentrations than female offspring (Figure 4) could reflect previously described differences in energy demand (food intake) associated with differences in growth of males and females.31,32,49 Our study is the first to investigate differences in THg concentration between young polar bears of different sexes. In adult polar bears, females tend to have higher hair THg concentrations than males, which is thought to be the result of underlying sex-specific patterns in diet.3,50,51 In addition, polar bears show sex-specific differences in THg sensitivity with regards to hormonal and neurological response in that adult males, despite their lower THg concentrations, appear to be the more sensitive than adult females.9,52 Further studies of male and female variation in Hg concentration in polar bear offspring might help clarify whether this sex-specific difference in sensitivity is established during early development.15−17
Figure 4. Box-and-whiskers plot of the concentration of total mercury (THg) in hair from western Hudson Bay polar bear offspring (17 females, 16 males) sampled in September 2014 and 2015. This figure excludes the one 2 year old offspring (see text for details). The median data value is displayed within the box, which is defined at either end by the lower and upper (25% and 75%) quartiles of the data. The whiskers are determined by the minimum and maximum data values.
In conclusion, our study provides insight on hair THg concentrations in western Hudson Bay polar bear family groups. Hair THg concentrations increased with offspring age. Furthermore, maternal THg concentration was positively related to her body condition as well as litter size. Litter size, however, was not related to COY THg concentration, which was instead solely dependent on maternal THg and the sex of the COY. Finally, male offspring had a tendency to have higher THg concentrations than their female counterparts. Polar bear family groups represent a demographic unit that is rarely examined in depth in ecotoxicological studies. On the basis of our results, we encourage future studies in polar bear toxicology to include family groups consisting of offspring of different ages and both sexes.
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AUTHOR INFORMATION
Corresponding Author
*Phone: +1 (780)554-6359; fax: +1 (780)492-9234; e-mail:
[email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS
The Villum Foundation is acknowledged for funding (Thea Bechshoft). Financial and logistic support was provided by Aquarium du Qúebec, ArcticNet, Canadian Association of Zoos and Aquariums, Canadian Wildlife Federation, Care for The Wild International, Churchill Northern Studies Centre, EnviroNorth, Environment and Climate Change Canada, Hauser Bears, the Isdell Family Foundation, Manitoba Conservation and Water Stewardship, Natural Sciences and Engineering Research Council of Canada, Parks Canada Agency, Pittsburgh Zoo and PPG Aquarium, Polar Bears International, Quark Expeditions, Wildlife Media Inc., and the World Wildlife Fund (Canada and international). 5317
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