Regulated and Unregulated Halogenated Flame Retardants in

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Regulated and unregulated halogenated flame retardants in peregrine falcon eggs from Greenland Katrin Vorkamp, Knud Falk, Soren Moller, Frank Rigét, and Peter Borgen Sørensen Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b04866 • Publication Date (Web): 01 Dec 2017 Downloaded from http://pubs.acs.org on December 5, 2017

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Environmental Science & Technology

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Regulated and unregulated halogenated flame retardants

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in peregrine falcon eggs from Greenland

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Katrin Vorkamp1*, Knud Falk1, Søren Møller2, Frank F. Rigét3,4, Peter B. Sørensen5 1

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Aarhus University, Department of Environmental Science, Arctic Research Centre, Roskilde, Denmark; 2

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Aarhus University, Department of Bioscience, Arctic Research Centre, Roskilde, Denmark; 4

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Roskilde University Library, Roskilde, Denmark;

Greenland Institute of Natural Resources, Nuuk Greenland;

Aarhus University, Department of Bioscience, Silkeborg, Denmark.

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Abstract

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Median levels of regulated flame retardants, i.e. polybrominated diphenyl ethers (PBDEs), brominated

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biphenyl (BB) 153 and hexabromocyclododecane (HBCD) in 33-48 eggs of peregrine falcons (Falco

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peregrinus) from Greenland were 1900, 359 and 5.98 ng/g lipid weight (lw) and generally intermediate to

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levels in North America and Europe. Unregulated flame retardants had lower median concentrations of 1.06

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(2-ethylhexyl-2,3,4,5-tetrabromobenzoate, EH-TBB), 2.42 (1,2-bis(2,4,6-tribromophenoxy)-ethane,

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BTBPE), 0.52 (2,4,6-tribromophenyl 2,3-dibromopropyl ether, DPTE) and 4.78 (dechlorane plus) ng/g lw.

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Although these compounds are often considered recent replacements for PBDEs, they were also present in

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eggs from the 1980s. BDE-209 was the only compound with a significant increase (+7.2% annual change)

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between 1986 and 2014, while BB-153 and DPTE decreased significantly (-8.0 and -2.8% annual change,

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respectively). Dechlorane plus showed a non-significant increase. Individual birds equipped with light-

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logging geolocators, confirmed the contaminant exposure over a large geographical area as the birds spend

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nearly equal time periods in their breeding and wintering grounds in Greenland and Central/South America,

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respectively, interrupted by 5-6 weeks of migration through North America.

*

Corresponding author. E-mail: [email protected]

1 ACS Paragon Plus Environment


TOC art

BDE-209 ng/g lw 5 10 50 200

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1985

1995

2005

2015

Year

Br Br

Br Br Br

Cl Br

Cl Cl O

Br Br

Br

Cl

Cl

Cl

Cl Cl

Cl

Cl

Br

Cl

Cl

25 26

27

Introduction

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Added to flammable polymers for fire safety purposes, some flame retardants (FRs) have been shown to

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enter the environment and to be taken up by animals and humans both near and distant from emission

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sources.1,2 Several studies have detected brominated FRs, i.e. polybrominated diphenyl ethers (PBDEs), the

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hexabrominated biphenyl BB-153 and hexabromocyclododecane (HBCD), in eggs of peregrine falcon

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(Falco peregrinus) at high concentrations for terrestrial wildlife.3–6 In samples from cities in the USA,

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ΣPBDE reached concentrations at the µg/g lipid weight level.5

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PBDEs and HBCD have been associated with adverse effects in humans and animals, in particular on the

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(developing) nervous system, thyroid function and reproduction.7,8 Polybrominated biphenyls have also been

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associated with endocrine disruption and were classified as probably carcinogenic in humans.9 In birds,

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behavioral changes were frequently observed effects following the exposure to FRs in the laboratory and the

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field.10 Raptors appeared more sensitive to FR exposure than other birds and showed effects on thyroid

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system, steroids, retinol, behavior, growth/development and reproduction at environmentally relevant

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concentrations.10,11

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The commercial Penta- and OctaBDE mixtures have been phased out in the USA and the European Union

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(EU) for over ten years 12,13. The fully brominated BDE-209, the main component of the commercial


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DecaBDE product, is banned in electric and electronic equipment in the EU and was phased out in the USA

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by 2013. 14,15 Penta- and DecaBDE were produced in quantities of about 100,000 and 1.25 million tons,

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respectively, of which 95 and 45%, respectively, were used in the USA.16

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The production of polybrominated biphenyls (PBBs) was discontinued in the USA in the 1970s, following

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the Michigan incident.17 The majority of HBCD was used in Europe, estimated at 11,000 tons in 2006, of

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which about 96% were used in expanded and extruded polystyrene.18,19 The three PBDE mixtures, hexa-BB

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and HBCD are included in the Stockholm Convention on Persistent Organic Pollutants (POPs), with

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DecaBDE being the most recent addition.20

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Potential alternative FRs include, but are not limited to, 2-ethylhexyl-2,3,4,5-tetrabromobenzoate (EH-TBB),

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bis(2-ethylhexyl)tetrabromophthalate (BEH-TEBP), 1,2-bis(2,4,6-tribromophenoxy)-ethane (BTBPE),

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decabromodiphenyl ethane (DBDPE), 2,4,6-tribromophenyl 2,3-dibromopropyl ether (DPTE or TBP-DBPE)

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and dechlorane plus (DDC-CO or DP), which were recently detected in marine wildlife from Greenland.21

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BEH-TEBP, BTBPE, and DDC-CO have previously been reported for peregrine falcon eggs from Canada

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and Spain, while DPTE was recently detected in peregrine falcon eggs from Germany, 22-24 indicating the

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bioaccumulation potential of these compounds in birds of prey. Mixtures of EH-TBB and BEH-TEBP have

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been used in the commercial products Firemaster 550® and Firemaster BZ-54® to replace PentaBDE, but

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BEH-TEBP has also been used individually.25,26 BTBPE is marketed as FF-680® and was announced to

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replace OctaBDE,27 while DBDPE was introduced in the 1990s as Saytex 810® for the same commercial

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applications as BDE-209.28,29 Little is known about DPTE, except for recent information on DPTE being

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used in Germany. 24 DDC-CO is a high production volume chemical in the USA originally introduced as a

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FR in the 1960s.30,31

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The peregrine falcon population in Greenland consists of 500-1000 pairs. It belongs to the subspecies F. p.

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tundrius, which also breeds in the Arctic parts of Canada and Alaska32 and has been monitored in South

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Greenland since the 1980s.33 Unlike the European populations of the subspecies F. p. peregrinus, the

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peregrine falcons from Greenland migrate to the Caribbean and South America during the northern



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hemisphere winter.3,34 During the breeding season in Greenland the falcons mainly feed on small terrestrial

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passerines, but they have a wider diet during migration and in their winter grounds.3,34 Contaminant

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concentrations were first determined for this population in 2003: Although still presenting high

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concentrations in wildlife, most legacy POPs had decreased by 2003, while PBDEs had increased in the

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peregrine falcon eggs from South Greenland.3,34 No time trend has yet been published on the alternative FRs

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in peregrine falcons. The previous studies attributed the exposure to FRs mainly to the falcon’s winter

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migration to the American continent.3 Recent developments in animal tracking methods now allow the

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mapping of migratory routes for individual birds and thus a more precise assessment of their contaminant

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exposure in time and space. This study therefore has the objectives i) to determine the migration route of the

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peregrine falcons from South Greenland as well as the duration of each stage in their annual migration cycle,

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ii) to extend previously established time series of PBDEs, BB-153 and HBCD to a time period of nearly 30

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years, iii) to address the concentrations and trends of the alternative FRs in the peregrine falcon eggs and iv)

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to revisit the hypothesis of main FR exposure during winter migration to the American continent.

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Experimental section

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Geolocators

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The study area is low Arctic, in the municipality of Kujalleq in South Greenland (60-61°N, 45-46°W)

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(Figure S1 of the Supporting Information). The area has been visited every year since 1981 (except in 1993

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and 2004) for population monitoring and sampling. Between 2012 and 2015, ten individual birds were

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equipped with geolocators in addition to conventional ringing.35 We used a miniature MK-4 device

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(Biotrack, London, UK), approximately 1.5 g, which can be attached to a standard leg ring. It logs light

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intensity, which was read out when the birds returned to Greenland and converted to midnight and midday

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latitude and longitude. Details on the conversion and data processing are given in the Supporting

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Information. According to the manufacturer, the accuracy is ± 150 km and mainly influenced by shading,

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interferences from artificial light and proximity to equinox or the equator.


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Egg samples

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Addled peregrine falcon eggs have been collected for chemical analysis since 1986. All eggs were infertile,

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i.e. with liquid contents and no embryo development, except for four eggs with partly developed embryos.

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Several studies have concluded that persistent compounds are not likely to be affected in their concentration

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by in ovo metabolisation.36,37 The eggs were weighed and measured upon collection in the field and kept at

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roughly 10°C until transported to the laboratory in Denmark. Here they were immediately stored at -20°C

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until they were opened and their content transferred to amber glasses. These were also stored at -20°C until

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analysis.

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A total of 48 whole eggs were available to study PBDEs, of which 37 eggs originated from the period 1986-

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2003 and had been analyzed previously.3 The eleven new eggs were from 2004-2014. BB-153 and HBCD

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were analysed in 22 and 33 eggs, respectively. The alternative flame retardants were analysed in 41 whole

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eggs also covering the period 1986-2014. Of these, 39 eggs were identical with those for PBDE analysis. A

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full match was not possible because of insufficient sample material for the remaining samples. Table S1

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gives an overview of all samples and analyses.

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Chemical analysis

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The analysis of PBDEs and BB-153 in the eleven new samples followed previous methods and ensured

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separation of BB-153 and BDE-154.3 The PBDE analysis included the congeners 17, 28, 47, 49, 66, 85, 99,

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100, 153, 154, 183 and 209 and was performed by the same staff in the same laboratory as the previous

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analyses. The determination of HBCD had changed from the gas chromatography-mass spectrometry (GC-

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MS) method in the previous study, only yielding ΣHBCD, to the isomer-specific determination by high

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performance liquid chromatography-mass spectrometry (LC-MS/MS).

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Briefly, the samples were spiked with recovery standards (13C-polychlorinated naphthalenes 27 and 64), 13C-

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BDE-209 and 13C-HBCD isomers, Soxhlet extracted with hexane:acetone (4:1) and cleaned on a column

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packed with aluminium oxide, silica (with and without H2SO4) and Na2SO4. The first fraction, eluted with

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hexane, contained the PBDEs and BB-153, while HBCD isomers eluted in the second fraction with



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hexane:dichloromethane (1:1). The extracts of the first fraction were analyzed by GC-MS in electron capture

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negative ionization mode (ECNI) using a 60 m DB-1701 column and an extended oven temperature

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program.3 The HBCD extracts were evaporated to dryness, re-dissolved in 500 µl methanol and analyzed as

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described previously.38

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For the analysis of the alternative FRs, the samples were spiked with the same recovery standards and 13C-

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BEH-TEBP. The extracts were split in half for separate clean-up of the BEH-TEBP fraction, which is not

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stable to acid treatment, using gel permeation chromatography. Details of the method were described

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previously.21 Different from this description, the column clean-up was only performed once, due to the lower

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lipid content of the peregrine falcon eggs, and both DBDPE and BEH-TEBP were analysed on a 15 m DB-1

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column.

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The laboratory is accredited for the analysis of PBDEs in biota, and quality assurance/quality control

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measures followed accredited procedures. Duplicate samples showed good agreement (Table S2). Recovery

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rates were > 80% with the exception of three samples analyzed for the alternative FRs, for which a loss of

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some extract droplets had been documented. These were corrected for recovery. PBDEs and HBCDs were

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analyzed in the laboratory’s reference material and compared with control charts (Table S3). Since most of

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the alternative FRs were below detection limits in the laboratory reference material (Table S4), spiked

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control samples were analyzed, showing good agreement with target values for most compounds, but some

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deviation for BEH-TEBP, BTBPE and DBDPE (Table S5). Long-term accuracy is monitored through

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participation in external proficiency testing schemes for PBDEs and HBCD in biota (Figure S2). Limits of

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quantification ranged from 0.045 ng/g lw (anti-DDC-CO) to 66.4 ng/g lw (DBDPE) for the alternative FRs.

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The lipid content was determined according to 39.

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Statistical analysis

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For the time trend analysis, concentrations were first averaged for eggs of the same bird and the same year.

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Eggs of the same bird and different years (Table S1) were averaged as well and appointed to the average

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year. This reduced the degrees of freedom, but accounted for potential autocorrelation in the dataset. The


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time trend analysis is based on annual mean concentrations and followed previously described methods.40,41

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The variation over time is divided into a log-linear and a non-linear component. The linear component is

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tested by log-linear regression, while a 3-point running smoother is used for the non-linear component and

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tested by analysis of variance (ANOVA). A power analysis of the time trend analysis is included in the

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Supporting Information (Table S6).

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Results and discussion

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Migratory behavior

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Geolocator data could be retrieved for three individual birds upon their recapture in Greenland. Two birds

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provided data for one migration cycle each and one bird provided data for three cycles (i.e. five bird years in

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total). The results are shown together with conventional ring recovery data in Figure 1. Despite a small

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sample size, the geolocator data verified results from other studies in North America and Greenland using the

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same technique or satellite telemetry.42-44 The peregrines from South Greenland showed site fidelity to the

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same winter territory in Latin America where they spent about 5 months every year. Every spring and fall,

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they spent 5-6 weeks on migration each way either through North America or along the Atlantic coast, while

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the breeding season in Greenland was about 4.5 months. Our geolocator data support ring recoveries from

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the last four decades showing that Greenland female peregrines winter in the Caribbean region and northern

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South America to 30°S although some females may winter as far north in the USA as 39°N.42,45,46

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The tracking and ring recovery data confirm that the contaminant exposure of the peregrines integrates a

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large area, mainly determined by emissions in the eastern part of the USA, Central America and the

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Caribbean and the northern part of South America (Figure 1). The exposure to contaminants might further

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gain complexity by two additional factors: Firstly, some prey species such as the small terrestrial passerines

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the falcons feed on in Greenland, are migratory birds themselves. Secondly, studies on peregrine falcons in

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the USA have shown that the peregrines can receive some contaminants from anthropogenic sources in urban

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areas.47 This might also apply to the peregrine falcons from Greenland on their migration and in their



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wintering grounds. In North and Latin America, peregrines often winter in urban or semi-urban areas 42,44 as

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also confirmed by at least one of the tracked birds from South Greenland overwintering in the area of

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Caracas, Venezuela (Figure 1).

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As the technology for miniaturization of tracking devices develops fast, and costs decrease, studies into

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mapping migration routes and winter grounds of birds of prey will become more feasible. Global Positioning

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System (GPS) devices are also used increasingly for wildlife tracking48 and might offer higher precision than

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achievable here. Our geolocator tracking relies on the recapture of the birds, which has been the limiting step

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in extending our geolocator data to a sample size that would allow quantitative exposure analyses. As more

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geolocator data are obtained, it will be possible to combine these time- and place-specific data on the bird’s

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movements with emission inventory data, which for example are available for organochlorines49, and

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environmental and avian half-lives of these contaminants. This could result in a quantitative approach to

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explain contaminant concentrations and patterns in individual peregrine falcons and thus the inter-individual

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variation in the overall dataset. We have shown now that the individual bird has preferred winter grounds to

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which it returns in several migration cycles. For persistent compounds with ongoing emissions, this might

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indicate a larger variation in exposure within than between annual migration cycles.

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PBDEs, BB-153 and HBCD

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The median concentrations of ΣPBDE, BB-153 and ΣHBCD in the 48 eggs were 1900, 359 and 5.98 ng/g lw,

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respectively, with ranges over several orders of magnitude (Table 1). The concentrations of all compounds

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are also shown in Figure S3.

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The median ΣPBDE concentration is generally similar to or higher than those in eggs of peregrine falcons

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that breed and overwinter in Europe,6,23 but lower than levels observed in the peregrine populations breeding

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in non-Arctic parts of Canada and the USA.4,5,47,50 Higher PBDE levels in peregrine falcon eggs in North

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America than in Europe are in line with the historical PBDE use pattern,16 with the Greenland peregrine

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falcons taking an intermediate position. This is consistent with their migratory behavior including 4-5

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months of reduced exposure in Greenland, compared to birds breeding in North America. However, the


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variation among birds is large. This can be expected, given the high inter-individual variability in their

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wintering grounds (Figure 1) as well as potential contributions from local sources in urban centers, as

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discussed above.11,47 A summary of published brominated FR data in peregrine falcon eggs is given in Table

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S7.

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BDE-153 was the main PBDE congener, accounting on average for 42% of ΣPBDE (range 19-91%) (Figure

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2). This was also found in other studies on peregrine falcons 4,5 and has been attributed to the longer half-life

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of BDE-153 and/or the debromination of BDE-209.51-53 Although BDE-153 is the predominant PBDE

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congener, the percentage of BDE-99 increased significantly over time (p

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γ, but a higher percentage of γ-HBCD compared with the Greenland samples.22 In both cases, the proximity

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of emission sources might play a role, but has not been studied further. In peregrine nestlings, HBCD was

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only detected in individuals from urban locations.54

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BDE-209 and BB-153 were the only congeners with a significant time trend, showing opposite trends

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(Figure 3). Most of the other PBDEs and ΣHBCD showed increases as well, but these were not statistically

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significant (Table 2). Several studies have documented a recent decrease in lower brominated PBDE

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concentrations in wild birds, including peregrine falcon eggs from Sweden,6,60 but a similar decrease was not

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yet apparent in our study. The trends are probably influenced by the large inter-individual variation in the

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concentrations of the peregrine falcons from Greenland, as opposed to the Swedish peregrines that

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overwinter in Europe. Furthermore, the ongoing exposure to BDE-209 can maintain a high level of lower

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brominated PBDEs via debromination.52,53 The decrease of BB-153 was indicated in the previous time trend

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analysis in 2003,3 but has only become statistically significant in this extension of the time series.

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An increase of BDE-209 was also found in peregrine falcon nestlings from Canada and in peregrine falcon

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eggs from Sweden and the USA,4,6,11 with indications of a recent maximum in the Swedish study. As those

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birds overwinter in Europe, the earlier regulation of BDE-209 in Europe compared with the USA might play


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into this finding. The occurrence and significant increase of BDE-209 in the Greenland peregrine falcon eggs

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confirms its recent classification as a POP and inclusion in the Stockholm Convention.20

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Alternative flame retardants

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The concentrations of the alternative FRs were considerably lower than those of PBDE congeners, and a

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detection frequency of 100% was only reached for DPTE and syn- and anti-DDC-CO (Table 1; Figure S3).

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Interestingly, the majority of the alternative FRs studied here was also detectable in the oldest eggs from the

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1980s (Table S1), documenting that the use of these compounds and their occurrence in the environment is

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not an emerging phenomenon.

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Although DPTE was detectable in all samples, its mean concentration of 1.0 ng/g lw is lower than the mean

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concentration of 33 ng/g lw in peregrine falcon eggs collected in Germany in 2014.24 Apparently DPTE was

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still being used in Germany, which might suggest local sources.24 Little information is available on potential

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or actual DPTE use in other countries. DPTE median concentrations were below detection limits in peregrine

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falcon nestlings from Canada.11 Our time trend analyses showed a significant decrease of DPTE (Figure 3),

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with an annual rate of -2.8% (p=0.04). This trend does not support the assumption of DPTE being a

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significant replacement product of PBDEs.

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DDC-CO had previously been analyzed in eggs of peregrine falcons from Spain and Canada, with rather

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different median concentrations of 0.6 and 43 ng/g lw, respectively.22 Our results are intermediate, similarly

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to PBDEs and BB-153. The time trend analysis resulted in a positive, but not significant trend for both

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isomers of DDC-CO in the peregrine falcon egg samples since 1986 (Table 2; Figure 3). Other time trend

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studies on DDC-CO have been inconclusive: ΣDDC-CO increased in the atmosphere of the Great Lakes with

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doubling times of 3-6 years at three stations, while it remained unchanged at two other stations in the same

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region.61 On the other hand, decreases of DDC-CO were observed in suspended sediments, a sediment core

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and lake trout samples of Lake Ontario, following peaks in the 1980s.62 Reasons for this apparent difference

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are not clear, but it is possible that the matrices studied reflected different emission sources. In belugas

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(Delphinapterus leucas) from the St. Lawrence Estuary, DDC-CO increased from 1997 to about 2000 and



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decreased subsequently, possibly with a second peak around 2010.63 No significant change in DDC-CO

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concentrations was found in eggs of white stork (Ciconia ciconia) and black kite (Milvus migrans) from

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Spain between 1999 and 2011, however, the authors highlighted a large intra-species variation in

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concentrations.64

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The fraction of anti-DDC-CO to ΣDDC-CO (fanti) was 0.70 on average (range 0.61-0.80). While the relative

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standard deviation of lipid-normalised ΣDDC-CO concentrations was 129%, it was only 5.2% for fanti. This

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reflects the strong correlation of the two isomers (R2=0.96; p

Regulated and Unregulated Halogenated Flame Retardants in

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