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Emission changes dwarf the influence of feeding habits on temporal trends of per- and polyfluoroalkyl substances in two Arctic top predators Heli Routti, Jon Aars, Eva Fuglei, Linda Hanssen, Karen Lone, Anuschka Polder, Åshild Ø. Pedersen, Sabrina Tartu, Jeffrey M. Welker, and Nigel G. Yoccoz Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b03585 • Publication Date (Web): 18 Sep 2017 Downloaded from http://pubs.acs.org on September 19, 2017
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Emission changes dwarf the influence of feeding
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habits on temporal trends of per- and polyfluoroalkyl
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substances in two Arctic top predators
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Heli Routti,†* Jon Aars,† Eva Fuglei,† Linda Hanssen,‡ Karen Lone,† Anuschka Polder,§
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Åshild Ø. Pedersen,† Sabrina Tartu,† Jeffrey M. Welker,∥ and Nigel G. Yoccoz,⊥
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† Norwegian Polar Institute, Fram Centre, Tromsø, Norway
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‡ Norwegian Institute for Air Research, Fram Centre, Tromsø, Norway
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§ Norwegian University of Life Science, Campus Adamstua, Oslo, Norway
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∥ University of Alaska Anchorage, Department of Biological Sciences, Anchorage, AK, USA
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⊥ UiT-The Arctic University of Norway, Department of Arctic and Marine Biology, Tromsø,
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Norway
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ABSTRACT
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We monitored concentrations of per- and polyfluoroalkyl substances (PFASs) in relation to
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climate-associated changes in feeding habits and food availability in polar bears (Ursus
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maritimus) and arctic foxes (Vulpes lagopus) (192 plasma and 113 liver samples, respectively)
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sampled from Svalbard, Norway, during 1997-2014. PFASs concentrations became greater with
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increasing dietary trophic level, as bears and foxes consumed more marine as opposed to
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terrestrial food, and as the availability of sea ice habitat increased. Long-chained perfluoroalkyl
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carboxylates (PFCAs) in arctic foxes decreased with availability of reindeer carcasses. The ~9-
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14% yearly decline of C6-8 perfluoroalkyl sulfonates (PFSAs) following the cease in C6-8 PFSA
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precursor production in 2001 indicates that the peak exposure was mainly a result of atmospheric
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transport of the volatile precursors. However, the stable PFSA concentrations since 2009-2010
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suggest that Svalbard biota is still exposed to ocean-transported PFSAs. Long-chain ocean-
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transported PFCAs increased 2-4% per year and the increase in C12-14 PFCAs in polar bears
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tended to level off since ~2009. Emerging short-chain PFASs showed no temporal changes.
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Climate-related changes in feeding habits and food availability moderately affected PFAS trends.
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Our results indicate that PFAS concentrations in polar bears and arctic foxes are mainly affected
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by emissions.
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INTRODUCTION
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Per- and polyfluoroalkyl substances (PFASs) have been produced at large quantities for a wide
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variety of purposes.1,2 In particular perfluoroalkyl carboxylates (PFCAs) and perfluoroalkyl
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sulfonates (PFSAs) (and their precursors) are recognized as global pollutants of emerging
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concern because they are persistent, bioaccumulative and toxic.3-5 PFASs have complex emission
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history.6,7 Production of perfluorooctane sulfonyl fluoride (POSF) based products, including
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perfluorooctane sulfonate (PFOS), grew rapidly in Europe and North-America from the 1970s
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until the major producer, 3M, voluntarily phased-out the production in 2001-2002.8,9 After the
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production ceased in Western countries, China started to produce POSF-based products in the
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early 2000s.6 However, the estimated yearly production volumes in China have been less than a
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tenth compared to the yearly production volumes in the 1990s.6 China has exported large
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quantities of POSF to Brazil where it is used to synthetize N-ethyl perfluorooctane sulfonamide
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(N-EtFOSA), used as a pesticide.10 An amendment of the Stockholm Convention listing PFOS,
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its salts and POSF was ratified by most countries in 2010 and, in 2014 by China (chm.pops.int).
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They are included in Annex B of the Convention, which means that they are restricted, but not
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completely banned.11
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Large quantities of C9-13 PFCAs were emitted from Western countries and Japan until 2002,
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but since 2003, the emissions have increased from continental Asia.7 Furthermore, the release of
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fluorotelomer-based precursors, including fluorotelomer alcohols (FTOHs) and –sulfonates
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(FTSAs), increasingly contributes to global PFCA emissions.7
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(PFOA), its salts and PFOA-related compounds are proposed for listing under the Stockholm
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Convention.12 C8-14 PFCAs including their salts and precursors are currently proposed or
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intended for restrictions by European Union (www.echa.europa.eu).
Today, perfluorooctanoate
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PFSAs and PFCAs, that are released directly into the aquatic system, may slowly reach the
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Arctic via ocean currents,13-15 whereas, their volatile precursors, for example FTOHs and
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perfluoroalkane sulfonamides (FASAs), undergo rapid transport via air currents. These
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precursors can be degraded to PFSAs and PFCAs in the atmosphere.16-19 The transport of PFCAs
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via ocean currents is expected to be major compared to atmospheric transport13,20 whereas the
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contribution of oceanic vs atmospheric transport of PFSAs and PFCAs may vary locally.21 The
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European Arctic, including Svalbard, is exposed to high input of both oceanic and atmospheric
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contaminants as the area is largely affected by winds and ocean currents from Europe and North-
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America.22,23
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Arctic mammalian predators are exposed to high concentrations of PFAS because PFASs
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biomagnify in high latitude food webs.3,24,25 PFAS exposure in Arctic biota, in particularly in
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polar bears (Ursus maritimus), is alarming. Concentrations of PFOS in polar bear plasma are
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similar to those reported in humans living at the proximity of a PFAS manufacturing plant in
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China.26-28 Documented adverse health effects of PFASs in experimental animals and humans are
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numerous.5,29,30 Modelling studies suggest that current PFAS concentrations in polar bears are
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high enough to contribute to reproductive, immunotoxic and genotoxic effects31 and correlative
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studies have linked PFAS concentrations in polar bears to changes in steroid and thyroid
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hormone concentrations.32,33 Furthermore, PFAS concentrations in Arctic mammals may
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increase during seasonal food deprivation periods.28,34
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Temporal trends of PFASs are highly variable in Arctic predators,35-38 which is likely related to
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the complex emission sources and variance in transport mechanisms of these compounds. It is
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thus essential to quantify the temporal trends (year to year) of PFAS concentrations in Arctic
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wildlife that may reflect source changes toward Asia and South America from traditional sources
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of Western countries.7,10 However, emission history is not the only factor that may influence
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temporal changes in contaminant exposure in Arctic predators. Climate-driven changes in ocean
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circulation patterns may affect long-range transport of PFAS15and, furthermore food web
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structures and predator-prey interactions are changing in the Arctic ecosystems.39 This likely
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influences contaminant exposure in Arctic biota as documented recently for polar bears.40-42
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Polar bears and arctic foxes (Vulpes lagopus) are among the highest contaminated Arctic apex
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predators.43 Polar bears and arctic foxes from Svalbard are species that can provide information
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about temporal trends of PFASs in the Arctic environment as well as how PFAS accumulation
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may be related to diet choices. For instance, both species feed on variable food items from both
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the marine and terrestrial ecosystem,44-46 which may affect their exposure to contaminants. Polar
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bears feed preferably on ringed seals (Pusa hispida), but they also ingest other marine food items
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such as whale carcasses, seabirds and terrestrial prey like geese and reindeer, particularly in the
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absence of sea ice.44,47-49 The arctic fox in Svalbard is a predator and scavenger foraging on both
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marine and terrestrial food items including reindeer, ptarmigans, geese, seabirds and seals.45,46,50
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However, feeding habits of polar bears and arctic foxes in Svalbard have likely changed over
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time because climate warming is especially pronounced in the Svalbard area compared to other
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Arctic areas.51 For instance, the maximum extent of sea ice in the Barents Sea, including
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Svalbard, has decreased by ~ 50% since the late 1990s,52 the length of the summer season (i.e.
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time with reduced ice) has increased by over 20 weeks between 1979 and 201353 and winter sea
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ice is retreating.54 Furthermore, duration of snow cover on land has decreased 0.5 day per year
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since 1976 whereas rain-on-snow events are predicted to increase by 40 % at the end of this
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century.51,55
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The aim of the study was to investigate temporal trends of PFASs in relation to climate-
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associated changes in feeding habits and food availability in two Arctic top predators from
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Svalbard, namely the polar bear and the arctic fox during the period 1997-2014. Furthermore, we
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discussed about the role of emission history and long-range transport mechanisms on PFAS
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trends in polar bears and arctic foxes. We also analyzed several emerging PFASs.
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MATERIALS AND METHODS
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Field sampling
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Adult female polar bears from the Barents Sea subpopulation were captured annually between
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25th March and 5th May in the period 2000-2014. The 192 samples collected opportunistically
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throughout Svalbard represented 137 individual females. Twenty-eight females were captured 2-
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8 times. Details of immobilization, determination of age, body condition, breeding status and
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blood sampling are given in supporting information. Breeding status, age and body condition for
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each sampling year are given in Table S1.
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Arctic foxes (n=113) were trapped by local trappers on western Spitsbergen, Svalbard, around
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the Isfjorden area and Nordenskiöld Land during the annual harvest between 1st November and
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15th March in the period 1997-2014. All trapped individuals were less than two years old and
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none of the females had given birth. Among the sampled foxes, number of individuals, as well as
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sex, age and body condition were balanced over the eleven trapping seasons (Table S2). Details
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of sampling as well as determination of body condition (ranging from 1-barely measurable fat to
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4-extensive fat) have been described previously.56,57 Samples of skeletal muscle and liver were
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packed in aluminium foil and stored at -20°C until analysed.
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Proxies for feeding habits
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Stable isotope values of nitrogen and carbon (δ15N and δ13C, respectively) were used as
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proxies for feeding habits of polar bears and arctic foxes. Due to the availability of different
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body compartments for the two species, δ15N and δ13C were measured in polar bear red blood
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cells and arctic fox muscle tissue. Half-lives for δ15N and δ13C in polar bear red blood cells are
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over 3 months and ~1.5 months, respectively,58 whereas half-lives for δ15N and δ13C for muscle
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tissue of a small mammal is approximately a month.59 As polar bears were captured in April and
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arctic foxes collected in November-March, stable isotope values for both species thus reflect
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mostly their winter diet. Analytical procedures are described in supporting information.
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Proxies for food availability
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Polar bear habitat preference likely reflects the occurrence and availability of seals to polar
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bears.60 We thus used sea ice habitat quality available for individual polar bears as a proxy for
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availability of seals to polar bears. First, we categorized surrounding areas of Svalbard according
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to the abundance of preferred sea ice habitat. The yearly (2000-2014) distribution and duration of
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preferred sea ice habitat was based on resource selection function (RSF) models as described in
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detail in supporting information. According to the maps produced by RSF models, preferred
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habitat was consistently available for more days of the year on the east side of Svalbard than in
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the west side of Svalbard over the whole study period (Figure S1). Among the 137 individual
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polar bears studied, we used telemetry data (n=83) or capture position (n=54) to assign them to
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the better habitat on the eastern side or the poorer habitat on the western side as detailed in
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supporting information.
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We used reindeer mortality and sea ice cover as proxies for availability of Svalbard reindeer
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carcasses and seals, respectively, to arctic foxes.57 Reindeer mortality was derived from the
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ongoing annual long-term summer monitoring of structural composition and mortality of
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Svalbard reindeer in Adventdalen, Nordenskiöld, and expressed as number of reindeer that died
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during the past 12 months in Advendtdalen.57,61,62 As reindeer mainly die in late winter and
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spring63 they are available as food items for foxes mainly in the late winter and spring.
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Therefore, we used the number of reindeer carcasses observed during the summer preceding the
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arctic fox trapping season as a proxy.
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To determine availability of sea ice cover for individual foxes, we calculated an index for each foxes based on daily sea ice maps of Isfjorden as described in supporting information.
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Analyses of PFAS
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Due to the availability of different body compartments for the two species, we monitored
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PFASs in plasma of polar bears and liver of arctic foxes. The 17 PFASs monitored in polar bear
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plasma and arctic fox liver are listed in Table 1. Methods for clean-up, separation, quantification
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and quality assurance are explained in supporting information.
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Data analyses
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We used the statistical program R version 3.3.1. for data analyses.64 We used additive mixed
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models (GAMM) on R-package mgcv65 to analyse the effects of year, feeding habits and food
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availability, in addition to biological variables, on PFAS concentrations in polar bears and arctic
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foxes. To study PFAS concentrations in polar bears, we defined 26 candidate models with year,
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δ15N and δ13C values in red blood cells, habitat quality (high vs. low), breeding status, age and
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body condition as fixed predictor variables, and individual ID as random variable to account for
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repeated measurements (Table S6). As perfluoroundecanoate (PFUnDA) concentration was
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considerably higher in samples analysed in 2012 compared to those analysed in 2014-15 (median
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49 and 20 ng/g, respectively) for unknown reasons, we included batch (2012 vs. 2014-15) as a
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random variable in the polar bear PFUnDA model. A smaller set of candidate models (n=5) were
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applied
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perfluorobutane
sulfonate
(PFBS),
perfluoroheptanoate
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perfluorotetradecanoate (PFTeDA) due to the limited number of polar bear samples (n=70)
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analysed for these compounds. To study liver PFAS concentrations in arctic foxes, we defined 18
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candidate models including the effects of year, muscle δ15N and δ13C, reindeer carcasses, sea ice
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cover and body condition (Table S7). As we hypothesize non-linear PFAS trends due to their
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complex emission history, we entered year as a smoothed term using penalized regression splines
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and Gaussian distribution.65 The other predictor variables were applied as linear numerical or
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categorical variables. The models were fitted using the restricted maximum likelihood (REML)
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method. Highly correlated predictor variables (e.g. δ15N and δ13C) were not included in the same
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model as recommended.66 To make inference from all candidate models and subsequently from
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all predictor variables, we used model averaging based on Akaike’s Information Criterion
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(AIC)67 using the R-package MuMIn.68 More specifically, we ranked the models according to
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AIC, which was further used to calculate AIC weight (e(0.5(AICmin
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divided by the sum of all relative likelihoods). Further, we calculated model averaged estimates
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for all the predictor variables in the candidate model list weighted using AIC weights. We used
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95% confidence intervals of the model-averaged estimates to determine whether the parameters
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were significantly different from 0 at the 5% confidence level. We used diagnostic plots (Figure
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S2-S3) to identify that the distribution of model residuals met the model assumptions.69 The
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residual plots revealed an outlier in models explaining perfluorohexane sulfonate (PFHxS)
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concentrations in arctic foxes. We excluded this outlier, which did not lead to significant changes
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in parameter estimates.
– AICi))
(PFHpA)
and
); relative likelihood
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We used plots from the highest ranked GAMMs to evaluate during which period PFAS
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concentrations linearly changed in polar bear and arctic fox food web. Estimates for yearly
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changes in PFAS concentrations were derived from linear mixed effects models (LMEM) (R
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package lme470) and linear models (LM) for polar bears and arctic foxes, respectively. Polar bear
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individual ID was included in LMEMs as random variable. To obtain yearly changes in polar
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bear/arctic fox food web, we adjusted the changes for biological and environmental variables i.e.
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we included the same covariates in the LMEMs and LMs as in the top GAMM for the given
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compound in the given species. The non-adjusted trends were derived from models that excluded
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the continuous predictors reflecting feeding habits and food availability from the top GAMMs
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(δ13C, δ15N in both species, and sea ice cover and reindeer mortality in arctic foxes). The annual
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changes (%) in the median concentrations were calculated from 100 * (eestimate
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Temporal changes in feeding habits were investigated by GAMMs, and the yearly linear changes
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were obtained using LMEMs or LMs.
for year
– 1).
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RESULTS AND DISCUSSION
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Concentrations of PFASs in polar bears and arctic foxes
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PFOS was quantitatively the most abundant PFAS detected in both polar bears and arctic foxes
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(Table 1). The contribution of PFOS to ΣPFAS decreased from over 80% to ~60% during the
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study period. Linear and branched PFOS, investigated only in arctic fox liver samples, were
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highly correlated (r=0.94, 95% CI [0.91, 0.96], pLOD Fluorotelomer sulfonates (FTSA) 6:2 FTSA C8 n.a. 8:2 FTSA C10 n.a. Perfluoroalkane sulfonamido substances FOSA C8 0.02
