Environ. Sci. Technol. 2009, 43, 3646–3651
Mercury Trends in Ringed Seals (Phoca hispida) from the Western Canadian Arctic since 1973: Associations with Length of Ice-Free Season A . G A D E N , † S . H . F E R G U S O N , †,‡ L. HARWOOD,§ H. MELLING,| AND G . A . S T E R N * ,†,‡ Department of Environment and Geography, University of Manitoba, 500 University Crescent, Winnipeg MB, R3T 2N2, Canada, Fisheries and Oceans Canada, 501 University Crescent, Winnipeg MB, R3T 2N6, Canada, Fisheries and Oceans Canada, Yellowknife, Northwest Territories, X1A 1E2, Canada, and Fisheries and Oceans Canada, Sidney, British Columbia, V8K 4B2, Canada
Received November 20, 2008. Revised manuscript received February 9, 2009. Accepted February 16, 2009.
We examined a unique time series of ringed seal (Phoca hispida) samples collected from a single location in the western Canadian Arctic between 1973 and 2007 to test for changes in total mercury (THg) in muscle tissue associated with (1) year and (2) length of ice-free season. We found no temporal trend with muscle THg whereas a curvilinear relationship existed with the length of ice-free season: seals attained higher THg in short (2 months) and long (5 months) ice-free seasons. δ15N and δ13C in muscle tissue did not illustrate significant trends with ice-free days. We estimated that the turnover time of THg in muscle was about twice as long as stable isotope turnover in muscle, possibly explaining the lack of trend with stable isotopes in association with ice-free duration. Our discussion explains how summer environmental conditions may influence the composition of prey (mercury exposure) available to ringed seals. Results offer insight into how marine mammals may respond to directional changes in the Arctic ice-free season.
over the 20 year period from 1981-2001 (3). Western Canadian Arctic ringed seals (Phoca hispida) also have relatively high hepatic THg levels compared to other Arctic regions (4); however, unlike the beluga and Arctic birds no clear trend over time was observed (5). Outridge et al. (6) reported mercury inputs and losses from the Arctic Ocean were near equilibrium and concluded that recent variations in mercury concentrations in marine biota were therefore unlikely due to changes in ambient seawater mercury concentrations but may be affected by dynamic ecological and geochemical processes. Similarly, Kirk et al. (7) found springtime atmospheric mercury depletion events also do not appear to significantly affect mercury concentrations in marine environments. Thus, while monitoring mercury in the Arctic provides a history of “what” the concentrations are and have been, an equally important question to examine is “why” the concentrations fluctuate. Studying fundamental ecosystem and physical dynamics could potentially explain variation observed in mercury levels in biota, particularly ringed seals for which there are no clear temporal trends. Seals accumulate Hg through their fish-based diet (8), so any shifts in prey stocks as a result of climate change will alter their contaminant exposure (9, 10). One of the most important physical variables affected by climate change is the sea ice regime; many ecosystem functions in the Arctic depend, to some extent, on the timing, duration and extent of sea ice including processes resulting in the availability of prey (i.e., see ref 11). Adult ringed seals from Prince Albert Sound (Figure 1) feed mostly on Arctic cod (Boreogadus saida) in fall and winter and a mix of fish and invertebrates (crustaceans, squid and benthic invertebrates) in summer (12, 13). Higher trophic level prey such as Arctic cod have relatively high concentrations of mercury compared to lower trophic level organisms (i.e., zooplankton 14, 15). A longer ice-free season could result in longer periods of access to Arctic cod (16), the higher contaminated prey. Shifts in trophic level of ringed seals can be determined with stable isotope ratios of nitrogen (17). The changing sea ice regime may also influence seals’ foraging areas (i.e., benthic/inshore vs pelagic/offshore), and this information can be assessed with stable isotope ratios of carbon (17). Here we relate mercury, which is linked to the carbon cycle and consumed in the foodweb (9), to one of the most important physical parameters influencing biological pro-
Introduction Contaminant levels have been monitored throughout the Arctic in response to global transport and human food safety. Temporal trends of increasing mercury concentrations have been observed for many biological samples. For example, mercury concentrations in Greenland seabird feathers showed a significant increase over 100 years beginning in the 1860s (1). In the Canadian Arctic, total mercury (THg) significantly increased over the 28 year period from 1975-2003 by ∼2% and ∼3% annually in the eggs of northern fulmar (Fulmarus glacialis) and thick-billed murre (Uria Iomvia), respectively (2). THg concentrations in beluga (Delphinapterus leucas) liver adjusted for age from the Mackenzie Delta increased * Corresponding author phone: 204 984 6761; fax: 204 984 2403; e-mail:
[email protected]. † University of Manitoba. ‡ Fisheries and Oceans Canada, Winnipeg. § Fisheries and Oceans Canada, Yellowknife. | Fisheries and Oceans Canada, Sidney. 3646
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FIGURE 1. Sampling region in the western Canadian Arctic. Ringed seals were sampled near Ulukhaktok (formerly Holman) along the northwest coast of Prince Albert Sound. 10.1021/es803293z CCC: $40.75
2009 American Chemical Society
Published on Web 03/23/2009
TABLE 1. Mean ± Standard Error for δ15N, δ13C, and THg Concentrations in Male and Female Adult Ringed Seal Muscle from Ulukhaktok, NT (1973-2007), and from Ringed Seals across Alaska and the Canadian Arctic location Holman/ Ulukhaktok, CAN
year
muscle THg (µg/g ww)
16.87 (0.60) 15.57 (0.32) 16.19 (0.25) 15.85 (0.27) 15.85 (0.18) 15.22 (0.09) 15.73 (0.24) 15.67 (0.26) 15.17 (0.17) 14.73 (0.35) 15.30 (0.16) 14.86 (0.12) 15.48 (0.20) 15.41 (0.16)
-20.85 (0.28) -21.21 (0.14) -20.64 (0.12) -20.97 (0.04) -20.63 (0.13) -20.81 (0.32) -20.82 (0.14) -20.93 (0.09) -20.31 (0.12) -20.61 (0.19) -20.52 (0.13) -20.81 (0.10) -20.69 (0.13) -20.80 (0.10)
16.9 ( 0.6
-18.5 ( 0.8
0.61 (0.07) 0.46 (0.07) 0.62 (0.07) 0.41 (0.12) 0.50 (0.05) 0.29 (0.03) 0.56 (0.07) 0.44 (0.07) 0.52 (0.04) 0.44 (0.10) 0.34 (0.04) 0.32 (0.03) 0.54 (0.09) 0.61 (0.08) 0.36 (0.05) 0.21 (0.08) 0.47 (0.04) 0.46 (0.03) 1.13 (0.15) 0.81 (0.06) 0.10 ( 0.16 0.22 ( 0.33
this this this this this this this this this this this this this this this this 22 22 21 21 32 33
133
0.41 ( 0.29
34
61
0.39 ( 0.17
34
0.68 ( 0.29
35
M F M F M F M F M F M F M F M F M F M F
1996-2001 1995-1997
11 6 14 3 15 2 11 7 13 4 8 8 6 9 10 3 26 28 10 20 59-78a 11
1987-1993 1989-1993
2007
2004 2003 2002 1996 1995 1993 1977 1973
1998
15.8 (8-26) 17.0 (8-26) 15.6 (8-21) 14.7 (7-21) 16.5 (7-26) 9.5 (7-12) 19.2 (11-25) 16.4 (11-26) 15.2 (7-26) 19.3 (11-26) 13.5 (9-21) 16.4 (11-21) 12.5 (7-17) 13.4 (7-21) 17.2 (7-36) 12.0 (7-17) 9.3 (7-16) 8.5 (7-17) 15.7 (8-26) 14.0 (8-26)
17.43 ( 0.28
9
-18.04 ( 0.38
reference study study study study study study study study study study study study study study study study
n ) 59 for THg; n ) 78 for δ N and δ C. Samples from Sachs Harbour, Holman, Shingle Point, and Paulatuk. Samples from Salluit, Wakeham Bay, George River, Inukjuaq, Resolute Bay, Sanikiluak, and Eureka. a
c
δ13C (‰ in muscle)
N
2005
Barrow, AK Barrow, AK Western Canadian Arcticb Eastern Canadian Arcticc Northwater Polynya, CAN
δ15N (‰ in muscle)
age average (range)
sex
15
13
b
ductivity in the Arctic Ocean: length of the annual ice-free season. Biological (age and sex) and ecological (δ15N and δ13C) variables are also reviewed in our THg analysis of adult ringed seals. We use THg and stable isotope half-lives in muscle (18, 19) to estimate initial timelines of THg, δ15N, and δ13C incorporation into ringed seal muscle and relate these to seasonal diet. Seals were sampled from the western Canadian Arctic, most commonly in the Prince Albert Sound area of the eastern Amundsen Gulf (Figure 1) from 1973-2007.
Methods Field Sampling. As part of a harvest-based monitoring program, ringed seal samples were obtained from hunters from Ulukhaktok (formerly Holman; 70°43′N, 117°45′W), NT, located along the northwest shore of Prince Albert Sound (Figure 1). Approximately 13-20 seals were sampled annually for mercury in 1993, 1995, 1996, 2002-2005, and 2007, which represented approximately 4% of all the seals harvested in each year (20). Additional samples from 1973 and 1977 were included in our analysis (21, 22). We used samples from adult ringed seals (7+ years) in this study. All samples were taken in the subsistence harvests primarily during the month of June and prior to break-up of the sea ice, and they were analyzed for trace elements with the same methods as described below. Sex and standard length (cm) were recorded from harvested seals, and lower jaws were collected to extract for later age estimation. Muscle tissue was taken from the lower back (dorsal to the kidneys), frozen within 24 h of collection, and shipped to the Freshwater Institute, Fisheries and Oceans Canada, Winnipeg, MB, for mercury analyses. Mercury in muscle was chosen for the analysis because it appears to be a better indicator of recent dietary exposure to contaminants
(23) and is significantly related to THg in other tissues (24), whereas mercury in liver tends to accumulate over time (i.e., ref 25). Age estimates were provided by counting growth layer groups (GLG) in the dentine layer of lower canines (26). Recent studies have indicated that counts of dentinal GLG tend to underestimate ages of older seals (>10 years) compared to the reading of cementum layers (27). However, we used the same aging method (dentinal) that was used for the 1970s samples to ensure the data sets were comparable. The duration of the ice-free season in the Eastern Amundsen Gulf, beginning as early as mid-May and lasting until as late as mid-November, was determined for each year using ice charts from the Canadian Ice Service. For a given year, total ice-free days were summed from the first day of ice clearing (the earliest day showing a lead approximately 10 km wide near the mouth of Prince Albert Sound) to the first day of ice freeze-up (the first day showing a continuous cover of new, unbroken ice 20, 28). In our analyses we used the number of ice-free days for the year previous to sampling. Chemical Analysis. Tissue subsamples were taken from the core of the frozen sample tissue, eliminating outside contamination. We used approximately 0.2 g muscle for the analyses. After the subsample was heated and digested in sulfuric and nitric acids, mercury levels were determined using Cold Vapour Atomic Absorption Spectroscopy (CVAAS (29)).Total mercury was measured in wet weight. Replicates, blanks, and standard reference material (SRM; LUTS-1, TORT-2, CRM 2976) were all used as measures of quality control. The limit of detection was 0.005 µg/g wet weight, and 85% of the standard reference material was recovered. Before analysis for stable isotope ratios (δ15N and δ13C), lipids were extracted from muscle tissue because they tend VOL. 43, NO. 10, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 2. Regression Coefficients of Muscle THg, δ15N, δ13C and Age in Ulukhaktok Male and Female Adult Ringed Seals from 1973-2007 (note: δ15N and δ13C were only available 1995-2007) δ15N
THg
δ13C
age
1 -0.06
1
1 0.21
1
Male Adults THg δ15N δ13C age
1 0.33a 0.17 0.34b
1 0.03 0.14 Female Adults
THg δ15N δ13C age a
FIGURE 2. Box and whisker plot of wet weight (ww) mercury concentrations in muscle of adult ringed seals at Ulukhaktok, Northwest Territories, Canada, and a bar graph of the previous years’ ice-free days. There are no significant temporal trends in either plot. to bias δ13C values (30). Lipids were extracted from 0.2 g muscle using methods based on ref 31. Briefly, the tissue was submerged in 5 mL of a 2:1 mixture of chloroform and methanol for 18 h. After centrifugation and removal of the extract, another 5 mL was added and mixed for 2 h. The process was repeated twice more with the solution mixed for 1 h each time for a total of four extractions to sufficiently remove all lipids from the material (unpublished data, Chambellant et al.). After being freeze-dried, the samples were analyzed for δ15N and δ13C by Continuous Flow Ion Ratio Mass Spectroscopy (CFIR-MS) at the University of Winnipeg Stable Isotope Laboratory. Isotopic data are presented in units per milliliter (‰) with δ (delta) notation. Here δ15N and δ13C are derived from δsample‰ ) [(Rsample/Rstandard) - 1] × 1000
(1)
where R is the ratio of heavy to light isotope (15N/14N or 13 C/12C) in the sample and standard. The nitrogen stable isotope standard was atmospheric nitrogen; Pee Dee belemnite limestone formation was the standard for carbon stable isotopes. Error was (0.19‰ and (0.21‰ for δ15N and δ13C, respectively, from the laboratory analysis. Statistical Analysis. We first did a linear regression analysis of both seal muscle THg and ice-free days against year to determine any temporal trends. No significant trends were observed for 1993-2007 data. For all other statistical analyses, we log-transformed the THg (and age and length) data to produce uniform residuals. δ15N and δ13C were not logtransformed because they were normally distributed. For comparative purposes, the nonlogged data (means and SE) are listed in text and tables. 3648
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