Inter-Annual Variation of Persistent Organic ... - ACS Publications

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Inter-Annual Variation of Persistent Organic Pollutants (POPS) in an Antarctic Top Predator Arctocephalus gazella Emily K. Brault,†,* Michael E. Goebel,‡ Heidi N. Geisz,§ Elizabeth A. Canuel,§ and Rebecca M. Dickhut§,∥ †

University of California, Santa Cruz, Ocean Sciences Department, 1156 High Street, Santa Cruz, California 95064 Antarctic Ecosystem Research Division, NOAA Fisheries, Southwest Fisheries Science Center, 8901 La Jolla Shores Dr., La Jolla, California, 92037 § Virginia Institute of Marine Science, College of William & Mary, P.O. Box 1346, Gloucester Point, Virginia 23062 ‡

S Supporting Information *

ABSTRACT: Persistent organic pollutants (POPs), contaminants that may bioaccumulate in upper trophic level organisms, were detected in the milk of a top predator, the Antarctic fur seal (Arctocephalus gazella). Multiparous females had significantly lower concentrations of certain POPs (transnonachlor, p,p′-DDE, and several PCBs) in their milk than primiparous females, likely due to the annual lactational transfer of the POP burden from mother to pup. Furthermore, there were significant interannual differences in POP concentrations in multiparous females’ milk from five breeding seasons between 2000 and 2011. Decreasing trends in concentrations of certain POPs over the recent decade coincide with declining global emissions, yet atmospheric concentrations in the Antarctic are not always consistent with global trends, suggesting that additional factors may contribute to temporal trends of POPs in fur seals. Climate shifts and corresponding availability of krill over the past decade were not consistent with trends observed in POP concentrations in fur seal milk, suggesting that climate may not be a key factor. Additional mechanisms, such as variability in the geographic ranges of individual seals during overwintering migrations are discussed and should be explored further.

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both anthropogenic and natural.7 Changes in sea ice and temperatures due to climate change may worsen the biological effects of POPs by exacerbating harmful stressors such as food shortage, disease, or competition with invasive species.7 Because POPs in polar biota can cause adverse health effects that may be exacerbated by climate change, it is important to measure POP levels in Antarctic predators.1 Antarctic fur seals (Arctocephalus gazella) are abundant top predators in the Antarctic food web and have a circumpolar distribution. In the early austral summer, adult female fur seals return to natal breeding beaches to give birth to a single pup, leaving after 4.5 months of rearing.8 In the nonbreeding season, these seals forage pelagically and are broadly distributed in the Southern Ocean. Individuals in the South Shetland population show highly variable migrations that can extend up the eastern coast of South America in the Atlantic or range widely in the South Pacific.9 As predators, these seals may accumulate high levels of POPs.10 To date, few measurements of POP

INTRODUCTION In the Antarctic, persistent organic pollutants (POPs), such as organochlorine pesticides (OCPs) and polychlorinated biphenyls (PCBs), are ubiquitous.1 Reaching the Antarctic via longdistance atmospheric transport, POPs are deposited to surface waters, as well as the snowpack. POPs may become concentrated in ice layers and may enter surface waters due to glacial melting, possibly contributing to unchanging levels of ∑DDT (p,p′-DDT + p,p′-DDE) in Adélie penguins over the last 30 years.2,3 From surface waters, POPs are accumulated by phytoplankton, and subsequently may bioaccumulate in zooplankton and higher trophic levels of the marine food web.1 Although these contaminants have been banned in several countries for decades, they are still used in some countries.4 Considering their continued use in some regions, as well as their current introduction to the Antarctic food web via glacial melting, understanding the distribution of these contaminants remains important. Studies have yet to be performed to determine whether current levels of POPs in Antarctic biota cause adverse effects, though an array of harmful impacts, including immunosuppression,5,6 has been documented in analogous species in the Arctic. The health effects of POPs on polar biota may change due to environmental, ecological, and physiological stressors, © 2013 American Chemical Society

Received: Revised: Accepted: Published: 12744

August 12, 2013 October 14, 2013 October 18, 2013 October 18, 2013 dx.doi.org/10.1021/es403577f | Environ. Sci. Technol. 2013, 47, 12744−12752

Environmental Science & Technology

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POP Analysis. The POP analysis method is described in Geisz et al.3 In brief, seal milk was freeze-dried, manually homogenized, and subsampled. A surrogate standard was added to all milk samples prior to extraction using high-purity organic solvents. Bulk lipid analysis was performed gravimetrically on a subsample of the total extract. Samples were further purified using acid extraction and column chromatography; fractions isolated by column chromatography were reduced in volume and analyzed using gas chromatography-negative chemical ionization mass spectrometry (GC-MS). Control procedures included analysis of field and laboratory blanks and intercalibration by analysis of standard reference materials (SRMs) from the U.S. National Institute of Standard Testing (NIST). Surrogate standard recoveries ranged from ∼65 to 100%. POPs in the seal milk samples were quantified relative to surrogate standards. Peak areas were determined for targeted POPs and surrogate standards for each sample, and relative response factors were determined by analysis of standards. δ13C and δ15N Analysis. δ13C and δ15N values for Antarctic fur seal milk were determined using an elemental analyzerisotope ratio mass spectrometer (EA-IRMS) at the Virginia Institute of Marine Science (VIMS). The elemental analyzer was a Costech ECS 4010 CHNSO Analyzer (Costech Analytical Technologies, Inc.) and the isotope ratio mass spectrometer was a Delta V Advantage Isotope Ratio Mass Spectrometer with a Conflo IV Interface (Thermo Electron North America, LLC). A small number of seal milk samples (from the 2005/06 breeding season) were analyzed at the University of CaliforniaDavis Stable Isotope Facility, using a PDZ Europa ANCA-GSL elemental analyzer interfaced to a PDZ Europa 20−20 isotope ratio mass spectrometer (Sercon Ltd., Cheshire, UK). δ15N values were not significantly different between samples analyzed on both instruments. δ13C values were significantly different (p < 0.001), but this may be a consequence of variable foraging locations across years. Prior to isotope analysis, lipids were removed from subsamples using an Accelerated Solvent Extractor (ASE). After the POP extraction method, an extraction with a chloroform:methanol solution (1:2; v:v) was performed.24 Samples, contained in precleaned (72 h Soxhlet extraction with 1:2 chloroform/methanol solution) filter papers (Whatman, 55 mm, hardened ashless), were removed from the ASE cells, transferred to precleaned glass jars where solvent was evaporated, and frozen until isotope analysis (−20 °C). Approximately 1 mg dry weight of sample was placed into tin cups (Costech, 5 × 9 mm, pressed tin capsules). Blanks and international standards (USGS 40 and USGS 41) were analyzed on the EA-IRMS after every ten samples. Samples were analyzed for 13C/12C and 15N /14N and expressed as δ13C and δ15N based on the Vienna PeeDee Belemite and atmospheric nitrogen (AIR) standards, respectively. Data Analysis. Prior to statistical analyses, the data were blank corrected using routine blanks. Only contaminants that were detected in the majority of samples were reported. For a small number of samples (n = 2) in which concentrations of a few POPs were below the detection limit of the GC-MS and thus not quantifiable, the lowest quantified concentration of the contaminant for the group (primiparous vs multiparous, or breeding year) was determined and divided by three,25,26 and this value was included in the data set. Concentrations of POPs were compared between primiparous and multiparous Antarctic fur seals for those samples collected during the austral summer of 2005/06 since seal milk

concentrations in the milk of Antarctic fur seals have been made.11 Concentrations of POPs in marine mammals are influenced by diverse factors, including trophic level, breeding status, migration, and diet.10,12,13 Breeding status may be a particularly important determinant of POP concentrations in marine mammals; for example, body burdens of POPs in female seals may decrease due to lactational transfer of POPs to their young.10,12−14 Polar animals with long-distance migrations to source regions of POPs, like the Antarctic fur seal, have some of the highest concentrations of POPs among polar biota.15,16 As upper trophic level predators, these seals are also subjected to biomagnification of POPs in their diets. Stable isotope values (δ13C and δ15N) have been used to evaluate the diets of marine predators and may help explain patterns seen in POP concentrations.17 Since the lighter isotope of N (14N) is preferentially excreted during amino acid metabolism and egestion,18 δ15N is indicative of trophic position. δ13C aids in identifying food sources or location of the prey due to variations across different primary producers, source water masses, or geographic location in the Antarctic.19,20 δ13C and δ15N are used in combination with contaminants to elucidate uptake mechanisms, diet, and food web structure17 and have the potential to explain patterns seen in the POP concentrations of animals, such as seals, feeding at multiple trophic levels. In this study, we quantified POPs and stable isotope values in Antarctic fur seal milk, examining variation in contaminant concentrations in Antarctic fur seal milk over time (2000 to 2011), and we discuss factors contributing to the trends.

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METHODS Study Site. Antarctic fur seal milk samples were collected during six austral summers (December to February) between 2000 and 2011 at Cape Shirreff, Livingston Island (62°28′S, 60°46′W). The Antarctic fur seal breeding season begins in November and lactation extends into April. Throughout this work, we use the start of the breeding season followed by a twodigit designation for the year of weaning (e.g., 2000/01). Milk samples were collected during the following breeding seasons: 2000/01, 2001/02, 2004/05, 2005/06, 2009/10, and 2010/11. Cape Shirreff is an ASPA (Antarctic Specially Protected Area) and is the site of the U.S. Antarctic Marine Living Resources (US AMLR) Program’s long-term study of the breeding biology and population dynamics of Antarctic fur seals, established in 1997. Sample Collection. Seal milk samples were collected as described in Polito and Goebel.21 In brief, female Antarctic fur seals were captured with hoop nets, sedated (5 mg Midazolam), and anesthetized (isoflurane; see Gales and Mattlin22). Almost all milk samples were collected from females during their perinatal period, the time between parturition and a female’s first foraging trip, via manual expression. Some nonperinatal milk samples were collected during the 2005/06 breeding season. Milk samples were collected in precleaned vials and stored at −20 °C until analysis. The US AMLR Program conducts longitudinal studies on marked Antarctic fur seals. Thus, most seals in this study were of known-age (with known reproductive histories); either by being tagged as a pup or through tooth cementum-aging.23 Primiparous seals (females pupping for the first-time) were all originally tagged as pups. Multiparous seals are females who have bred prior to the year of sample collection. 12745

dx.doi.org/10.1021/es403577f | Environ. Sci. Technol. 2013, 47, 12744−12752


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was only collected from multiparous seals during the other breeding seasons. In addition, for only 2005/06, both perinatal and nonperinatal milk was collected. Only perinatal milk was available for all other years. Comparisons between POP concentrations of primiparous and multiparous seals were not performed separately for perinatal and nonperinatal milk. For three seals, nonperinatal and perinatal milk samples were collected during 2005/06. Differences between the perinatal and nonperinatal milk of these seals were assessed by paired t tests for all POPs and were not significant. Since the sensitivity of the GC-MS at the time 2005/06 samples were analyzed was lower than when the other samples were analyzed fewer compounds are reported for 2005/06 than for other years (2000/01, 2001/02, 2004/05, 2009/10, and 2010/11). Data were tested for normality and heterogeneity of variance prior to analysis. Since most POP concentrations failed the normality tests, a Box-Cox transformation was performed on all data. A student’s t test was conducted for each compound to test for significant differences in the concentrations of each contaminant between primiparous and multiparous seal milk. Paired t tests were used to compare the perinatal and nonperinatal milk of the three seals, mentioned previously, for δ13C and δ15N. The difference between perinatal δ13C and nonperinatal δ13C was significant (p = 0.024). Polito and Goebel21 noted significant change in δ13C and δ15N of Antarctic fur seal milk across perinatal and nonperinatal periods. Therefore, comparisons of primiparous isotopic values to those of multiparous were performed separately for nonperinatal and perinatal milk.21 A one-way ANOVA was used to determine significant differences between isotopic values of milk from all breeding seasons (2000/01, 2001/02, 2004/05, 2005/06, 2009/10, and 2010/11). Only 2005/06 perinatal milk samples were included in this analysis due to the significant variation between isotopic data of perinatal and nonperinatal milk. Linear regression analysis was used to evaluate relationships between (1) POP concentrations and δ13C or δ15N values, (2) POP concentrations and age of seal, and (3) POP concentrations and breeding season. Age data were included in the analyses when available, while POPs, δ13C and δ15N, and breeding season data were available for all analyses. All analyses were performed using R statistical software27 and differences were identified as significant when p < 0.05.

Figure 1. Pesticides in primiparous and multiparous seals. Concentrations of pesticides (A) and p,p′-DDE (B) in milk from primiparous and multiparous Antarctic fur seals. Significant differences are indicated with asterisks.

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RESULTS AND DISCUSSION POP Concentrations in Primiparous vs Multiparous Seals. POP concentrations were significantly higher in primiparous milk than in multiparous milk for all PCBs, except PCB 101 (p = 0.012 for PCB 105; p < 0.01 for PCBs 118, 128, 138, 153, 167, 170, and 180), as well as trans-nonachlor and p,p′-DDE (p = 0.036 and 0.032, respectively), (Figures 1 and 2, Table S1 of the Supporting Information, SI). Other pesticides also showed a trend of higher concentrations in primiparous milk although the differences were not statistically significant, possibly due to the small sample size for primiparous seals (n = 5). Interestingly, the difference in POP concentrations between primiparous and multiparous seal milk is strong for PCBs and less so for OCPs, such as HCHs and chlordanes. PCBs may be more persistent in the environment than some OCPs, like HCHs. Half-lives, the time for the concentration to reach half of the initial concentration, for ∑PCB (101, 136, 151, 118, 153, and 138) in Antarctic seawater (∼ 5.7 years) appear to be longer than those of ∑HCH (α- and γ-HCH) (∼3.4 years).28

Previous studies have documented a decrease in the contaminant load of POPs in female marine mammals via lactation and subsequent exposure of POPs to their pups.10,12−14 After birth, lactation is a major exposure route of POPs for young seals and may even exceed the contribution of transplacental transfer to the POP burden of young.29 While these results are consistent with previous studies looking at maternal depuration of POPs in mammals,10,12−14 this is the first time this phenomenon has been documented in Antarctic fur seals. Although POP concentrations in fur seal milk are significantly different between primiparous and multiparous fur seals, age alone does not appear to be a factor contributing to variation in POP concentrations. Consistent and frequent significant correlations were not found between POP concentrations and age of seals (p > 0.05). For all 25 compounds, only one significant relationship was discovered the concentration of p,p′-DDT was negatively correlated with 12746



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quantify POPs in Antarctic fur seal pup tissues, exploring potential physiological and behavioral effects from POP exposure, and consider the breeding status of their mothers since this research indicates that POP concentrations are higher in primiparous Antarctic fur seal milk than multiparous seal milk. Temporal Trends in POP Concentrations. Concentrations of 16 out of 25 total contaminants in the seal milk samples decreased significantly over the time period of this study (p ≤ 0.001 for α-HCH, γ-chlordane, trans-nonachlor, p,p′-DDT, o,p′-DDT, oxychlordane, mirex, PCB 195, and PCB 206; p = 0.002, 0.04, 0.02, 0.02, 0.01, 0.03, and 0.005 for cisnonachlor, and PCBs 128, 138, 156, 170, 180, and 187, correspondingly) with the most marked changes generally observed between 2000/01, 2001/02 and 2009/10 vs 2004/05, 2005/06 and 2010/11 (Figures 3−5, Tables S3a,b of the SI). For several compounds with significant trends (cis- and transnonachlors, oxychlordane, and PCBs 138, 128, 156, 170, 180, 187, 195, and 206) there was a pattern of highest contaminant concentrations in 2000/01, 2001/02, and 2009/10 and lowest concentrations in 2004/05, 2005/06, and 2010/11. Higher concentrations of o,p′-DDT and p,p′-DDT occurred early in the decade (2000/01 and 2001/02) and lower concentrations in subsequent years. In contrast, two contaminantsα-HCH and γ-chlordanehad unique patterns where the highest concentrations were measured in 2009/10 for α-HCH and 2005/06 for γ-chlordane. Trends of some contaminant, such as p,p′-DDE and p,p′-DDD, exhibited no declines in the past decade. The lack of decline of the compounds may result from continued introduction. Approximately 14 countries still use DDT for disease control and many have plans to reintroduce the insecticide.4,38 Furthermore, other countries have begun using dicofol, an insecticide that may contain DDT as an impurity.4,38 Overall, these results indicate that POP concentrations in fur seal milk varied temporally across breeding seasons spanning a decade, with some compounds exhibiting a declining trend. Bacon et al.11 reported measurements of POPs in three Antarctic fur seal milk samples collected in 1984 and 1985 on the South Shetland Islands (Table S4 of the SI). Despite the small sample size, to our knowledge this is the only previous study to measure contaminants in Antarctic fur seal milk, allowing us to examine longer-term trends in POPs. The trends from the mid-1980s to recent years vary across contaminants: concentrations of DDT compounds, trans-nonachlor, and some PCBs (118, 153, and 138) may be increasing, while concentrations of some chlordanes (γ- and α-chlordane) and PCB 187 may be decreasing. For PCB 101, concentrations in fur seal milk from the mid-1980s was less than milk collected from modern primiparous seals, but greater than milk from recent multiparous seals. Several factors may contribute to the observed interannual variation in POP concentrations in fur seal milk, including global usage of the contaminants, shifts in diet over the past decade (2001−2011), climatic or oceanographic changes, and migration patterns. Because only female, multiparous Antarctic fur seals were analyzed across the five different breeding seasons, the role of gender and breeding status in interannual variation of POP concentrations could not be evaluated in this study. The POPs analyzed in this study have been banned for decades in many regions, including North America and Europe, but are still used in some parts of the world. Accordingly, global

Figure 2. PCBs in primiparous and multiparous seals. PCB concentrations in milk from primiparous and multiparous Antarctic fur seals. Significant differences are indicated with asterisks.

age of the seal (p = 0.034). Since POP concentrations varied significantly across the six breeding seasons; correlations between contaminant concentrations and age were also assessed separately by year. Similarly, significant correlations were not frequent or consistent (Table S2 of the SI). The lack of a correlation is likely due to POPs accumulating for a longer period of time (∼4 years) in the mother’s tissues prior to the first lactation. Antarctic fur seals first reproduce at age four and have high probabilities of giving birth each year.8 Thus, a primiparous female bioaccumulates POPs for four years before maturing, while multiparous animals transfer contaminant loads to their offspring annually. In accordance with this conclusion, earlier studies have found that first born offspring may have higher exposure to POPs than subsequent offspring due to higher loads of POPs during the first lactation than in subsequent lactation periods.29−31 The amounts of milk consumed by pups of mothers in this study were not measured. Additionally, since measurements of percent contribution of blubber weight to body weight, birth mass, lipid content of blubber, and the pollutant concentrations in the blubber of pups were not made, it is not possible to determine the POP load in pups and the respective contributions from gestational and lactational exposure in this study. However, Borrell et al.29 calculated the transfer of contaminants to young long-finned pilot whales (Globicephala melas) from the Faroe Islands from their mothers via gestation and lactation. Transfer rates for lactation (from the POP body load of mothers to calves) of 67.6 to 100% and 92.5 to 99.9% were calculated for total DDTs (all compounds) and PCBs, respectively.29 In contrast, transfer rates were much lower for gestation (6.95 to 9.58% and 4.14 and 9.73% for total DDTs and PCBs, respectively). For both lactation and gestation transfer rates, variation was related to the age of the female whale. 29 Nursing mammals are at a critical stage of development, such that even low concentrations of POPs have been found to cause adverse health effects, making POP exposure in pups via suckling particularly concerning.32−36 Sørmo et al.37 indicated that exposure to PCBs, especially dioxin-like PCBs such as PCB 118, which was detected in Antarctic fur seal milk in this study, had immunosuppressive effects on free-ranging gray seal pups. The effects of exposure of Antarctic fur seal pups to POPs via lactation are unknown at this time. Future research should 12747



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Figure 4. Temporal variation of PCBs. PCB concentrations in milk from Antarctic fur seals collected over six breeding seasons (2000/01, 2001/02, 2004/05, 2005/06, 2009/10, and 2010/11). Significant negative trends in contaminant concentrations are indicated with asterisks. Figure 3. Temporal variation of pesticides. Pesticide concentrations in milk from Antarctic fur seals collected over six breeding seasons (2000/01, 2001/02, 2004/05, 2005/06, 2009/10, and 2010/11). Significant negative trends in contaminant concentrations are indicated with asterisks.

of HCHs and PCBs since the 1980s. However, declines were not clearly evident in phytoplankton samples.28 Other factors, such as phytoplankton biomass, influence contaminant concentrations, and demonstrate the array of variables that may contribute to POP loads with increasing trophic level. This study shows significant declines in the concentration of some POPs in fur seal milk over the past decade, suggesting that decreased global emissions of POPs may have influenced the temporal variation. Yet, this trend was not observed for all POPs and atmospheric concentrations of some POPs (e.g., heptachlor) are not decreasing due to continued use in the southern hemisphere.44 Additionally, concentrations of some PCBs (118, 153, and 138), DDT compounds and transnonachlor have increased from the mid-1980s to the present when compared to Bacon et al.11 Therefore, trends in POP concentrations in fur seal milk may be driven by other factors (e.g., shifting migration patterns). As mentioned above, δ15N and δ13C values for fur seal milk indicate the trophic level and source region of the prey for these individuals. Mean δ15N and δ13C values for all multiparous perinatal seal milk samples from six breeding seasons (2000/01,

emissions of POPs (PCBs, HCHs, and DDTs) have declined in recent decades.39−42 However, POPs may still be emitted to the environment via continued legal or illegal use as well as their release from stocks of unused POPs.43 In polar regions, glacial melting, releasing POPs that have accumulated over decades of atmospheric deposition, may also be a continued source of POPs to the marine environment.2 Dickhut et al.44 evaluated atmospheric concentrations of some POPs along the Western Antarctic Peninsula (WAP). Over the preceding 20 years, α- and γ-HCH declined in concentration. 44 However, the concentrations of a contaminant known to still be in use in areas of the world, heptachlor, did not decline.4 Additionally, Galbán-Malagón et al.28 assessed trends in HCHs and PCBs by comparing recent measurements in Antarctic seawater and phytoplankton to historic data. The authors found considerable declines in seawater concentrations 12748



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between the concentrations of any of the measured POPs and the corresponding δ15N signatures of the seal milk samples. Only one contaminantp,p′-DDDhad concentrations negatively correlated with δ15N (p = 0.035). Furthermore, most contaminant concentrations did not have significant relationships with δ13C. Concentrations of p,p′-DDD and PCB 167 were negatively correlated with δ13C (p = < 0.001 and 0.026, respectively), while cis-nonachlor and PCB 101 were positively correlated with δ13C (p = 0.023 and 0.001, correspondingly). Since variations in POP concentrations across years were found, relationships between contaminant concentrations and isotopic values were also assessed separately by year. However, the significant relationships remained inconsistent and uncommon (Table S6a,b of the SI). Biomagnification of POPs renders diet an important factor in determining the POP concentrations in organism tissues with an increase in contaminant concentrations typically being observed with increasing δ15N.43,45 The lack of consistent and frequent relationships between POP concentrations and δ15N may result from of different turnover times for the contaminants versus isotopes. The contaminant signature represents a longer time frame (several months to years), while the δ 15 N signature represents a shorter period (weeks).10,21 Changes in fur seal diets between the recent weeks prior to sample collection and several months beforehand would result in the contaminant concentrations not being significantly correlated with δ15N. The lack of consistent correlations between POP concentrations and δ15N suggest other factors, such as migration, influence seal milk contaminant loads more than their Antarctic diet. Differences found between the δ13C values in primiparous vs multiparous milk suggest that regional differences in foraging and migration patterns may be a more important determinant of contaminant loads. Migration is an additional factor that can affect interannual variability in the concentrations of POPs in the tissues of animals. Among Antarctic biota, the highest concentrations of POPs have been measured in highly migratory seabird species, such as the south polar skua.1,15,26 Like seabirds, some marine mammals are resident to Antarctica, while others, such as Antarctic fur seals, only breed and forage in the Antarctic region in the summer. In the nonbreeding season, they migrate northwards to more human-influenced areas for the remainder of the year, ingesting POPs from these other food webs. Similarly, the migrations of marine mammals have been shown to influence their POP concentrations.46 Hinke et al.9 studied the migrations of Antarctic fur seals during the nonbreeding season and found that migrations of individual animals were highly variable both across seasons and geographic range. Some individuals ventured into the open ocean of the Pacific or Atlantic, while others migrated close to the shores of South America. The highly variable migratory habits of individuals and across years may contribute to the variability in POP concentrations observed in the Antarctic seal milk samples from 2001 to 2011. Seals that migrate nearer to the coast of South America, including the shores of Argentina, Chile, and Brazil, for example, are likely exposed to higher concentrations of POPs than seals whose migrations remained in the open ocean.4 Further research comparing the POP concentrations in the tissues of Antarctic fur seals of known migratory routes will verify the role of migration in the POP body burden of these seals.

Figure 5. Additional PCBs. PCB concentrations in milk from Antarctic fur seals collected over five breeding seasons (2000/01, 2001/02, 2004/05, 2009/10, and 2010/11). Significant negative trends in contaminant concentrations are indicated with asterisks. Note that 2005/06 data are not included because these PCBs were not detected for that year.

2001/02, 2004/05, 2005/06, 2009/10, and 2010/11) were 10.67 ± 0.11 and −22.41 ± 0.13 ‰, respectively (Table S5 of the SI). δ15N and δ13C values for multiparous perinatal seal milk across these six breeding seasons ranged from 10.16 ± 0.33 to 11.13 ± 0.19 and “−21.82 ± 0.28 to −24.18 ± 0.21 ‰, respectively. There was one significant difference between δ13C values for different breeding season. The δ13C values for 2005/ 06 multiparous seals were significantly lower than those for all other seasons (p < 0.001). This result could indicate that multiparous female seals during the 2005/06 breeding season were foraging in different areas than multiparous females during the other five breeding seasons. Considering the findings of latitudinal δ13C variation by Quillfeldt et al.,20 multiparous seals sampled in 2005/06 may be foraging at higher latitudes, farther south along the Antarctic Peninsula. Interestingly, the δ13C of perinatal primiparous milk from 2005/06 is not significantly different from that of multiparous seals for other years, suggesting primiparous seals are foraging in the same region as multiparous seals during all years except 2005/06. δ15N values of multiparous seals from all breeding seasons, as well as the δ15N of primiparous 2005/06 seals, are not significantly different. Therefore, these seals appear to be consuming prey at the same trophic level during all six breeding seasons. δ15N values for nonperinatal milk samples from primiparous and multiparous seals (2005/06) are similar (8.67 ± 0.58 and 8.65 ± 0.15 ‰, respectively). Likewise, δ15N values for perinatal milk samples from primiparous and multiparous seals are similar (11.2 ± 0.11 and 10.2 ± 0.33 ‰, respectively). The δ15N results indicate that primiparous and multiparous seals consume prey at a similar trophic level. However, δ13C values for nonperinatal primiparous seals differed from values for nonperinatal multiparous seals (p < 0.001, −24.2 ± 0.052 and −25.1 ± 0.11 ‰, correspondingly). δ13C of perinatal primiparous milk (−22.5 ± 0.23 ‰) was also significantly different from perinatal multiparous milk (−24.2 ± 0.21 ‰, p = 0.002). Thus, the δ13C findings suggest primiparous and multiparous seals may be foraging in different regions. There were no common and consistent significant correlations 12749



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in seal milk (Table S4); δ13C and δ15N for Antarctic fur seal perinatal milk protein (Table S5); and significance of correlations of POP concentrations with δ15N/δ13C for each breeding season (Table S6a,b). This material is available free of charge via the Internet at http://pubs.acs.org.

Environmental changes influence prey abundances and, consequently, cause shifts in diet, which may alter the loads of POPs that predators like fur seals ingest. Many prey species have life history strategies intimately tied to the sea ice, including Antarctic krill. Recruitment of krill depends on sea ice since it provides foodsuch as ice algaeduring the austral spring and winter. Several studies have demonstrated a strong link between ENSO and sea ice conditions.47−49 For instance, Quetin and Ross50 found their recruitment index (the portion of age-class 1 krill of the total) to be positively correlated with the absolute value of a seasonal El Niño/Southern Oscillation (ENSO) index. The authors found the highest recruitments of krill occurred during times of neutral or moderate periods of ENSO.50 When the availability of a prey type declines in response to climate variation, predators, like Antarctic fur seals, may rely more heavily on other prey sources. Diet shifts can affect POP concentrations in their tissues, such that consuming higher trophic level prey sources, like fish, will result in higher predator POP body burdens.1 Over the past decade, 2000, 2008, and 2011 had strong La Niña conditions, while 2003, 2005, 2007, and 2010 had strong El Niño conditions.51 In this study, the highest concentrations of POPs generally occurred in 2000/01a time of a strong La Niña eventand 2001/02 and 2009/10times with weaker La Niña conditions. In contrast, this study found generally lower POP concentrations in 2004/05, 2005/06, and 2010/11. During 2005 and 2010 strong El Niño events occurred, while 2004 experienced weaker El Niño conditions. Considering the overlapping trends of contaminants and climatic patterns, future research should explore the effects of global climate events and POP loads in polar animals. POP concentrations in fur seal milk show considerable interannual variability. The significant declines in concentrations of some POPs in fur seal milk over the past decade may reflect declines in global usage of POPs. A comparison with limited data from the 1980s, however, suggests that concentrations of certain compounds may actually have increased over the longer term. Other possible contributors to the interannual variability we observed include breeding season diet, which may be affected by climate cycles such as El Niño; however, a lack of variability in δ15N of fur seal milk suggests that diets are not highly variable. Thus, it is possible that the largest contributor to interannual variability in the POP burden of fur seals is their winter foraging and migration patterns. Migration has the potential to bring adult fur seals into regions heavily or minimally affected by pesticide use, influencing their POP accumulations and transfers to their pups within the Antarctic environment. Furthermore, our comparisons of POP concentrations in primiparous and multiparous seals suggest that female Antarctic fur seals lower their body burdens of POPs via lactation transfer to their young, explaining the lack of bioaccumulation of pesticides among adult female fur seals. This study demonstrates substantial interannual variation in POP concentrations in fur seal milk between 2000 and 2011, and indicates that migration may contribute greatly to this variability.

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AUTHOR INFORMATION

Corresponding Author

*Phone: 651-295-1644; fax: 831-459-4882; e-mail: ebrault@ ucsc.edu. Notes

The authors declare no competing financial interest. ∥ Author is deceased.

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ACKNOWLEDGMENTS We would like to acknowledge the National Science Foundation (NSF) for the funding to conduct this research (Award No. 0838932). Additionally, we would like to thank Elizabeth MacDonald and Michele Cochran for contributions to the chemical analyses, as well as Zachary Brown, Catarina Wor, and Dr. Andrew Wozniak for valuable insights in data analyses and presentation. We are grateful to the many field assistants that helped in capture and sample collection especially G.I. McDonald, Y. Tremblay, J.J. Lyons, R. Burner, R. Buchheit, N. Pussini, C. Bonin, and K. Pietrzak. We are also grateful for the support of Drs. Rennie S. Holt and George Watters, directors of the US-AMLR program and to Dr. D.P. Costa, UCSC for their support of Pinniped research at Cape Shirreff. All Antarctic fur seal research and sample collection was conducted under Marine Mammal Protection Act Permit Nos. 1024, 774-1649, 774-1847, and 16472-01 granted by the Office of Protected Resources, National Marine Fisheries Service. This paper is Contribution No. 3325 of the Virginia Institute of Marine Science, College of William & Mary.

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REFERENCES

(1) Corsolini, S. Industrial contaminants in Antarctic biota. J. Chromatogr. A. 2009, 1216 (3), 598−612. (2) Chiuchiolo, A. L.; Dickhut, R. M.; Cochran, M. A.; Ducklow, H. W. Persistent organic pollutants at the base of the Antarctic marine food web. Environ. Sci. Technol. 2004, 38 (13), 3551−3557. (3) Geisz, H. N.; Dickhut, R. M.; Cochran, M. A.; Fraser, W. R.; Ducklow, H. W. Melting glaciers: A probable source of DDT to the Antarctic marine ecosystem. Environ. Sci. Technol. 2008, 42 (11), 3958−3962. (4) Barra, R.; Colombo, J. C.; Eguren, G.; Gamboa, N.; Jardim, W. F.; Mendoza, G. Persistent organic pollutants (POPs) in eastern and western South American countries. Rev. Environ. Contam. T. 2006, 185, 1−33. (5) Fisk, A. T.; de Wit, C. A.; Wayland, M.; Kuzyk, Z. Z.; Burgess, N.; Letcher, R.; Braune, B.; Norstrom, R.; Polischuk Blum, S.; Sandau, C.; Lie, E.; Jørgen, H.; Larsen, S.; Skaare, J. U.; Muir, D. C. G. An assessment of the toxicological significance of anthropogenic contaminants in Canadian Arctic wildlife. Sci. Total Environ. 2005, 351−352, 57−93. (6) Letcher, R. J.; Ove Bustnes, J.; Dietz, R.; Jenssen, B. M.; Jørgensen, E. H.; Sonne, C.; Verreault, J.; Vijayan, M. M.; Gabrielsen, G. W. Exposure and effects assessment of persistent organohalogen contaminants in Arctic wildlife and fish. Sci. Total Environ. 2010, 408 (15), 2995−3043. (7) Muir, D. C. G.; de Wit, C. A. Trends of legacy and new persistent organic pollutants in the circumpolar Arctic: Overview, conclusions, and recommendations. Sci. Total Environ. 2010, 408 (15), 3044−3051. (8) Lunn, N. J.; Boyd, I. L.; Croxall, J. P. Reproductive performance of female Antarctic fur seals: The influence of age, breeding

ASSOCIATED CONTENT

* Supporting Information S

POP concentrations in primparous and multiparous seals (Table S1); significance of correlations of POP concentrations with age for each breeding season (Table S2); POP concentrations over time (Table S3a,b); POP concentrations 12750



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experience, environmental variation and individual quality. J. Anim. Ecol. 1994, 63 (4), 827−840. (9) Hinke, J.; Watters, G.; Trivelpiece, W.; Goebel, M. 2012. Synopsis of Data from Satellite Telemetry of Foraging Trips and Migration Routes of Penguins and Pinnipeds from the South Shetland Islands, 1997/98 to present [Abstract]. In Working Group on Ecosystem Monitoring and Management; Santa Cruz de Tenerife, Spain, 2−13 July 2012. Document: WG-EMM-12/37. (10) Tanabe, S.; Sung, J. K.; Choi, D. Y.; Baba, N.; Kiyota, M.; Yoshida, K.; Tatsukawa, R. Persistent organochlorine residues in northern fur seal from the Pacific coast of Japan since 1971. Environ. Pollut. 1994, 85 (3), 305−314. (11) Bacon, C. E.; Jarman, W. M.; Costa, D. P. Organochlorine and polychlorinated biphenyl levels in pinniped milk from the Arctic, the Antarctic, California, and Australia. Chemosphere. 1992, 24 (6), 779− 791. (12) Ross, P. S.; Ellis, G. M.; Ikonomou, M. G.; Barrett-Lennard, L. G.; Addison, R. F.; High, P. C. B. concentrations in free-ranging Pacific Killer Whales, Orcinus orca: effects of age, sex, and dietary preference. Mar. Pollut. Bull. 2000, 40 (6), 504−515. (13) Ylitalo, G. M.; Matkin, C. O.; Buzitis, J.; Krahn, M. M.; Jones, L. L.; Rowles, T.; Stein, J. E. Influence of life-history parameters on organochlorine concentrations in free-ranging killer whales (Orcinus orca) from Prince William Sound, AK. Sci. Total Environ. 2001, 281 (1−3), 183−203. (14) Beckmen, K. B.; Ylitalo, G. M.; Towell, R. G.; Krahn, M. M.; O’Hara, T. M.; Blake, J. E. Factors affecting organochlorine contaminant concentrations in milk and blood of northern fur seal (Callorhinus ursinus) dams and pups from St. George Island, Alaska. Sci. Total Environ. 1999, 231 (2−3), 183−200. (15) Focardi, S.; Bargagli, R.; Corsolini, S. Isomer-specific analysis and toxic potential evaluation of polychlorinated biphenyls in Antarctic fish, seabirds and Weddell seals form Terra Nova Bay (Ross Sea). Antarct. Sci. 1995, 7 (1), 31−35. (16) Corsolini, S.; Kannan, K.; Imagawa, T.; Focardi, S.; Giesy, J. P. Polychloronaphthalenes and other dioxin-like compounds in Arctic and Antarctic marine food webs. Environ. Sci. Technol. 2002, 36 (16), 3490−3496. (17) Ramos, R.; González-Solís, J. Trace me if you can: The use of intrinsic biogeochemical markers in marine top predators. Front. Ecol. Environ. 2012, 10 (5), 258−266. (18) Minagawa, M.; Wada, E. Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim. Cosmochim. Acta 1984, 48 (5), 1135−1140. (19) Hobson, K. A.; Piatt, J. F.; Pitocchelli, J. Using stable isotopes to determine seabird trophic relationships. J. Anim. Ecol. 1994, 63 (4), 786−798. (20) Quillfeldt, P.; McGill, R.; Furness, R. Diet and foraging areas of southern ocean seabirds and their prey inferred from stable isotopes: Review and case study of Wilson’s storm-petrel. Mar. Ecol.: Prog. Ser. 2005, 295, 295−304. (21) Polito, M. J.; Goebel, M. E. Investigating the use of stable isotope analysis of milk to infer seasonal trends in the diets and foraging habitats of female Antarctic fur seals. J. Exp. Mar. Biol. Ecol. 2010, 395 (1−2), 1−9. (22) Gales, N. J.; Mattlin, R. H. Fast, safe, field-portable gas anesthesia for Otariids. Mar. Mammal Sci. 1998, 14 (2), 361−372. (23) Goebel, M. E.; Costa, D. P.; Crocker, D. E.; Sterling, J. T.; Demer, D. A. Foraging ranges and dive patterns in relation to bathymetry and time-of-day of Antarctic fur seals, Cape Shirreff, Livingston Island. In Antarctic Ecosystems: Models for Wider Ecological Understanding; Davidson, W., Howard-Williams, C., Broady, P., Eds.; New Zealand Natural Sciences: Christchurch, 2000; pp 47−50. (24) Bligh, E. G.; Dyer, W. J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 1959, 37 (8), 911−917. (25) Dickhut, R. M.; Deshpande, A. D.; Cincinelli, A.; Cochran, M. A.; Corsolini, S.; Brill, R. W.; Secor, D. H.; Graves, J. E. Atlantic bluefin tuna (Thunnus thynnus) population dynamics delineated by organochlorine tracers. Environ. Sci. Technol. 2009, 43 (22), 8522−8527.

(26) Geisz, H. Persistent organic pollutants (POPs) as tracers of environmental change and Antarctic seabird ecology. Ph.D. Dissertation, Virginia Institute of Marine Science: Gloucester Point, VA, 2010. (27) R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2012. ISBN 3-900051-07-0, URL http://www.R-project.org/. (28) Galbán-Malagón, C. J.; del Vento, S.; Berrojalbiz, N.; Ojeda, M. J.; Dachs, J. Polychlorinated biphenyls, hexachlorocyclohexanes and hexachlorobenzene in seawater and phytoplankton from the Southern Ocean (Weddell, South Scotia, and Bellingshausen Seas). Environ. Sci. Technol. 2013, 47 (11), 5578−5587. (29) Borrell, A.; Bloch, D.; Desportes, G. Age trends and reproductive transfer of organochlorine compounds in long-finned pilot whales from the Faroe Islands. Environ. Pollut. 1995, 88 (3), 283−292. (30) Rogan, W. J.; Gladen, B. C.; McKinney, J. D.; Carreras, N.; Hardy, P.; Thullen, J.; Tingelstad, J.; Tully, M. Polychlorinated biphenyls (PCBs) and dichlorodiphenyl dichloroethene (DDE) in human milk: Effects of maternal factors and previous lactation. Am. J. Public Health 1986, 76 (2), 172−177. (31) Aguilar, A.; Borrell, A. Reproductive transfer and variation of body load of organochlorine pollutants with age in fin whales (Balaenoptera physalus). Arch. Environ. Contam. Toxicol. 1994, 27 (4), 546−554. (32) Thomas, P. T.; Hinsdill, R. D. Perinatal PCB exposure and its effect on the immune system of young rabbits. Drug Chem. Toxicol. 1980, 3 (2), 173−184. (33) Huisman, M.; Koopman-Esseboom, C.; Fidler, V.; HaddersAlgra, M.; van der Paauw, C. G.; Tuinstra, L. G. M. TH.; WeisglasKuperus, N.; Sauer, P. J. J.; Touwen, B. C. L.; Boersma, E. R. Perinatal exposure to polychlorinated biphenyls and dioxins and its effect on neonatal neurological development. Early Hum. Dev. 1995, 41 (2), 111−127. (34) Pluim, H. J.; van der Goot, M.; Olie, K.; van der Slikke, J. W.; Koppe, J. G. Missing effects of background dioxin exposure on development of breast-fed infants during the first half year of life. Chemosphere. 1996, 33 (7), 1307−1315. (35) Faroon, O. M.; Keith, S.; Jones, D.; De Rosa, C. Effects of polychlorinated biphenyls on development and reproduction. Toxicol. Ind. Health 2001, 17 (3), 63−93. (36) Tanabe, S. Contamination and toxic effects of persistent endocrine disrupters in marine mammals and birds. Mar. Pollut. Bull. 2002, 45 (1−12), 69−77. (37) Sørmo, E. G.; Larsen, H. J. S.; Johansen, G. M.; Skaare, J. U.; Jenssen, B. M. Immunotoxicity of polychlorinated biphenyls (PCB) in free-ranging gray seal pups with special emphasis on dioxin-like congeners. J. Toxicol. Environ. Health A. 2009, 72 (3−4), 266−276. (38) van den Berg, H. Global status of DDT and its alternatives for use in vector control to prevent disease. Environ. Health Perspect. 2009, 117 (11), 1656−1663. (39) Li, Y. F.; Scholtz, M. T.; van Heyst, B. J. Global gridded emission inventory of α-hexachlorocyclohexane. J. Geophys. Res. 2000, 105 (D5), 6621−6632. (40) Breivik, K.; Sweetman, A.; Pacyna, J. M.; Jones, K. C. Towards a global historical emission inventory for selected PCB congenersa mass balance approach 1. Global production and consumption. Sci. Total Environ. 2002, 290 (1−3), 181−198. (41) Li, Y. F.; Bidleman, T. Usage and emissions of organochlorine pesticides. In Canadian Arctic Contaminants Assessment Report II, Sources, Occurrence, Trends and Pathways in the Physical Environment; Bidleman, T., Macdonald, R., Stow, J., Eds.; Indian and Northern Affairs Canada: Ottawa, 2003; pp 49−70. (42) Li, Y. F.; Li, D. C. Global emission inventories for selected organochlorine pesticides. Meteorological Service of Canada. Internal Report; Environment Canada: Toronto, Canada, 2004. (43) Schwarzenbach, R. P.; Egli, T.; Hofsetter, T. B.; von Gunten, U.; Wehrli, B. Global water pollution and human health. Annu. Rev. Env. Resour. 2010, 35, 109−136. 12751



Article

(44) Dickhut, R. M.; Cincinelli, A.; Cochran, M.; Ducklow, H. W. Atmospheric concentrations and air-water flux of organochlorine pesticides along the Western Antarctic Peninsula. Environ. Sci. Technol. 2005, 39 (2), 465−470. (45) Jones, K. C.; de Voogt, P. Persistent organic pollutants (POPs): State of science. Environ. Pollut. 1999, 100 (1−3), 209−221. (46) Vetter, W.; Luckas, B.; Heidemann, G.; Skirnisson, K. Organochlorine residues in marine mammals from the Northern hemispherea consideration of the composition of organochlorine residues in the blubber of marine mammals. Sci. Total Environ. 1996, 186 (1−2), 29−39. (47) Loeb, V. J.; Hofmann, E. E.; Klink, J. M.; Holm-Hansen, O.; White, W. B. ENSO and variability of the Antarctic Peninsula pelagic marine ecosystem. Antarct. Sci. 2009, 21 (2), 135−148. (48) Stammerjohn, S.; Massom, R.; Rind, D.; Martinson, D. Regions of rapid sea ice change: An inter-hemispheric seasonal comparison. Geophys. Res. Lett. 2012, 39 (6), L06501. (49) Kwok, R.; Comiso, J. C. Southern ocean climate and sea ice anomalies associated with the Southern Oscillation. J. Climate. 2002, 15, 487−501. (50) Quetin, L. B.; Ross, R. M. Episodic recruitment in Antarctic krill Euphausia superba in the Palmer LTER study region. Mar. Ecol.: Prog. Ser. 2003, 259, 185−2000. (51) Climate Prediction Center Internet Team. Cold and warm episodes by season. NOAA Center for Weather and Climate Prediction. 7 Oct. 2013. Web. 7 Oct. 2013, http://www.cpc.ncep. noaa.gov/products/analysis_monitoring/ensostuff/ensoyears.shtml.

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