Halogenated Flame Retardants in Predator and Prey Fish From the

Jun 21, 2017 - The doubling age (T2) was defined as the rate that FR concentrations doubled annually as a function of growth year of the fish. ... Lak...
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Halogenated Flame Retardants in Predator and Prey Fish From the Laurentian Great Lakes: Age-Dependent Accumulation and Trophic Transfer Guanyong Su,†,‡,§ Robert J. Letcher,*,†,§ Daryl J. McGoldrick,∥ and Sean M. Backus∥ †

Ecotoxicology and Wildlife Health Division, Environment and Climate Change Canada, National Wildlife Research Centre, Carleton University, Ottawa, Ontario K1A 0H3, Canada ‡ Jiangsu Key Laboratory of Chemical Pollution Control and Resources Reuse, School of Environmental and Biological Engineering, Nanjing University of Science and Technology, Nanjing 210094, P. R. China § Department of Chemistry, Carleton University, Ottawa, Ontario K1S 5B6, Canada ∥ Water Science & Technology Directorate, Science and Technology Branch, Environment and Climate Change Canada, Canada Centre for Inland Waters, Burlington, Ontario L7S 1A1, Canada S Supporting Information *

ABSTRACT: The identification, persistence, accumulation and trophic transfer of 25 polybrominated diphenyl ether (PBDE) congeners, 23 non-PBDE halogenated flame retardants (NPHFRs), 4 polybrominated-diphenoxybenzenes (PB-DiPhOBzs) and 6 methoxylated (MeO−) PB-DiPhOBzs were investigated in predator and prey fish collected in 2010 from sites in the North American Great Lakes of Ontario (n = 26) and Erie (n = 39). Regardless of locations or species, 20 PBDEs and 12 NPHFRs were quantifiable in at least one of the 65 analyzed samples, and polybrominated-1,4diphenoxybenzenes (PB-DiPhOBzs) and MeO-PB-DiPhOBzs were not detectable in any of analyzed samples. Among the FRs, the greatest concentrations were the ∑PBDE, ranging from 1.06 (Rainbow Smelt, Lake Erie) to 162 (Lake Trout, Lake Ontario) ng/g wet weight (ww), which was followed by mean HBCDD concentrations ranging ND to 17.3 (Lake Trout, Lake Ontario) ng/g ww. The remaining FRs were generally not detectable or at sub-ppb levels. In most of cases, FR concentrations in samples from Lake Ontario were greater than those from Lake Erie. Strong and significant positive linear relationships occurred between log-normalized FR concentrations (ww or lipid weight (lw)) and ages of the top predator Lake Trout (n = 16, from Lake Ontario), and the estimated FR doubling ages (T2) were 2.9−6.4 years. For Walleye from Lake Erie, significantly positive linear relationships were also observed for some FRs, but the linear relationships generally became negative after FR concentrations were normalized with lipid weight. This study provides novel information on FR accumulation in aquatic organisms, and for the first time, significant positive linear relationships are reported between log-normalized FR concentrations (lw or ww) and ages of Lake Trout from the Great Lakes.

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INTRODUCTION Flame retardants (FRs) are a grouping of chemicals that are used to hinder the ignition and spread of fire, and thus are added to manufactured materials such as plastics, electronic product, textiles, surface finishes, and coatings.1,2 Going back several decades, legacy FRs include commercial mixtures of penta/ octa bromodiphenyl ethers (penta/octa-BDEs), hexabromobiphenyls (PBBs) and hexabromocyclododecane (HBCDD). Between 2009 and 2014 these FRs were listed as persistent organic pollutants (POPs; Annex A) under the Stockholm Convention due to their proven bioaccumulation, long-range transport, and adverse biological effect activity.3 Environmental persistence and impacts of these legacy FRs are likely to continue since they remain in the products that contain them.4−6 Increasing restrictions on legacy FRs has led to the increasing demand for “novel” FRs as replacements, and are thus emerging FRs of environmental concern, for example, Dechlorane Plus © XXXX American Chemical Society

(DDC−COs), decabromodiphenyl ethane (DBDPE), 1,2-bis(2,4,6-tribromophenoxy)ethane (BTBPE), 2-ethylhexyl-2,3,4,5tetrabromobenzoate (EHTBB), tetrabromobisphenol A-bis(2,3dibromopropylether) (TBBPA-DBPE).7,8 Environmental monitoring studies have demonstrated that both legacy and emerging FRs are pervasive in the environment samples (i.e., bird eggs, water, fish, atmospheric dust) from the Laurentian Great Lakes of North America, which are an important part of North America’s ecosystem and the largest surface freshwater system on Earth.9,10 Su et al. recently investigated 14 PBDEs and 23 non-PBDEs halogenated FRs (NPHFRs) in 115 herring gull egg samples collected in 2012 or Received: Revised: Accepted: Published: A

May 5, 2017 June 15, 2017 June 21, 2017 June 21, 2017 DOI: 10.1021/acs.est.7b02338 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Article

Environmental Science & Technology

fish (i.e., Lake Trout in Lake Ontario, Walleye in Lake Erie) is related with biological characteristics (i.e., sex, age); and (3) to examine the relationships between FR concentrations and trophic levels in aquatic biota from the Laurentian Great Lakes.

2013 from 20 colonies spanning the Great Lakes basin, and found that PBDEs, HBCDD, syn- and anti-DDC−CO, BB-153, BB-101, 2,4,6-tribromophenyl allyl (TBP-AE), pentabromomoethylbenzene (PBEB), BTBPE, α-1,2-dibromo-4-(1,2-dibromoethyl)-cyclohexane (TBECH), β-TBECH, pentabromo-pxylene (pTBX), octabromo-1,3,3-trimethyl-1-phenyl indane (OBTMPI) and hexabromobenzene (HBB) were quantifiable in at least one of these analyzed samples.5 Most importantly, concentrations of some FRs (i.e., decabromodiphenyl ether (BDE-209), HBCDD and DDC−COs) were significantly greater than measured in earlier egg samples, emphasizing the importance continued monitoring of these FRs in the Laurentian Great Lakes.5 The occurrence of FRs has been frequently reported in Laurentian Great Lakes fish samples. Zhu et al. showed concentrations of these FRs in Great Lakes Lake Trout increased exponentially between 1980 and 2000.11 Similarly, PBDEs, DDC−COs, PBEB, EHTBB, is(2-ethylhexyl)-tetrabromophthalate (BEHTBP), and TBBPA-BDBPE were reported in atmospheric particle phase samples from the same areas in the Great Lakes.12,13 Environmental assessments evaluate the risks of chemical exposure and bioaccumulation in humans and biota.14 Trophic transfer in Great Lakes aquatic biota has been well-examined for some FRs from some specific locations. In a recent study, PBDE concentrations were determined in a mixed food web of native and non-native aquatic species in Lake Erie, and non-native prey species (e.g., rainbow smelt) were found to significantly contribute to PBDE biomagnification.15 Trophic transfer of DDC−COs was also reported in a marine food web from Liaodong Bay, China, where lipid equivalent concentrations of anti-DDC−CO were positively correlated with trophic level and with a trophic magnification factor (TMF) of 5.6, suggesting the trophic magnification potential of anti-DDC−CO.16 In Lake Winnipeg (MB, Canada), in the examination of PBDEs, HBCDD, DBDPE, and BTBPE, strong positive linear relationships were found for BDE-47, BDE-209, and DBDPE concentrations in relation to trophic level, also suggesting these FRs biomagnify in the Lake Winnipeg food web.17 The present study has the following objectives: (1) to investigate the contamination levels of 48 legacy and replacement FRs (25 PBDEs and 23 non-PBDE halogenated flame retardants (NPHFRs)) in Lake Ontario and Lake Erie, the Laurentian Great Lakes; (2) to evaluate whether bioaccumulation of FRs in

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MATERIALS AND METHODS Standards and Chemicals. The 48 target FRs (25 PBDEs and 23 other flame retardants (NPHFRs)), along with their full chemical names and chemical structures are shown in Figure 1. All chemicals and standards were purchased from Wellington Laboratories Inc. (Guelph, ON, Canada), with the exception of octabromo-1,3,3-trimethyl-1-phenylindane (OBTMI) which was provided by Dr. Åke Bergman (Stockholm University, Sweden). The standards of 3 polybrominated-1,4-diphenoxybenzenes (PB-DiPhOBzs) and 5 methoxylated (MeO−) PB-DiPhOBzs were synthesized and kindly provided by AccuStandard Inc. (New Haven, CT), and the specific chemical structures are provided in Supporting Information (SI) Figure S1. Sample Collection. Collections made by Environment and Climate Change Canada (ECCC) as part of ongoing contaminant monitoring and surveillance activities in the Great Lakes, were the source of all aquatic samples in the present study. Detailed information on sampling, sample preparation, and storage methods have been described previously,18 and we have also reported in detail elsewhere all biological information on 65 aquatic samples.19 In brief, a total for the 65 aquatic biotic samples were collected in 2010 from Lake Ontario (n = 26) and Lake Erie (n = 39) (SI Figure S2). The aquatic samples from Lake Ontario were comprised of six species, including Alewife (Alosa pseudoharengus; n = 2), Deepwater Sculpin (Myoxocephalus thompsonii; n = 2), Lake Trout (Salvelinus namaycush; n = 15), Rainbow Smelt (Osmerus mordax; n = 2), Round Goby (Neogobius melanostomus; n = 2) and Slimy Sculpin (Cottus cognatus; n = 2). The aquatic samples from Lake Erie were comprised of nine species, including Emerald Shiner (Notropis atherinoides; n = 3), Freshwater Drum (Aplodinotus grunniens; n = 3), Lake Trout (Salvelinus namaycush; n = 7), Rainbow Smelt (Osmerus mordax; n = 3), Round Goby (Neogobius melanostomus; n = 3), Trout Perch (Percopsis omiscomaycus; n = 3); Walleye (Sander vitreus; n = 10), Whiter Perch (Morone americana; n = 3) and Yellow Perch (Perca f lavescens; n = 3). After capture, the fish were immediately frozen on dry ice and transported to the laboratory

Figure 1. Chemical structures of the target flame retardant compounds in this study. The hydrogen atoms are omitted for clarity. B

DOI: 10.1021/acs.est.7b02338 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Article

Environmental Science & Technology

FR Concentration As a Function of Fish Growth. The doubling age (T2) was defined as the rate that FR concentrations doubled annually as a function of growth year of the fish. T2 was derived from the slope of the plots of natural log FR concentrations (wet or lipid weight) versus fish age (in years) as follows:

where they are partially thawed, weighed, measured, and sexed by visual assessment of their gonadal tissues. Ages of Lake Trout and Walleye were determined using coded wire tags when present. For fish not containing tags, ages were estimated using scale samples. All remaining portions of the fish, including internal organs, are then homogenized for FR analysis. Flame Retardant (FR) Analysis. Determination of these target 48 brominated FRs in biotic samples was carried out in the Letcher Laboratories at the NWRC (ECCC, Ottawa, Canada), and details on sample extraction and instrumental analysis have been described in detail in our previous publications.5,6,20,21 In brief, approximately 2.0 g of the biotic homogenate (wet weight, ww) was accurately weighed and homogenized with precleaned diatomaceous earth (DE). The mixture was spiked with BDE-30 and -156 and 13C12−BDE-209 as internal standards, and subjected to accelerated solvent extraction (ASE) using dichloromethane (DCM). ASE extracts were evaporated down to 2 mL following by residual moisture removed by filtering through sodium sulfate. A 10% volume was taken and lipid content was determined gravimetrically. The remaining extract volume was concentrated under gentle nitrogen, and subject to high performance-gel permeation chromatography (HP-GPC) (Waters, Milford, MA) that was operated using DCM at a flow rate of 5 mL/min. The collected fraction was re-evaporated to approximately 0.5 mL, and further cleaned-up on a silica LC-Si SPE cartridge (500 mg X 6 mL; 6 g; J.T. Baker) with 8 mL of 5% DCM/hexane (v/v) solvent.22 The collected fraction was evaporated under gentle nitrogen flow down to 1 mL, solvent exchanged into 2,2,4-trimethylpentane (TMP) and re-evaporated under nitrogen to around 250 μL. After quantitative transfer to a preweighed brown glass GC vial with insert and cap, the final sample fraction was then ready for analysis by gas chromatography (6890 GC) -single quadrupole mass spectrometry (5973N MS) (GC-MS; (Agilent Technologies, Mississauga, ON, Canada)) operated in the electron capture negative ion (ECNI) mode. A 15 m DB-5 HT GC column (0.25 mm i.d., 0.1 mm, J&W Scientific, Agilent) was used. The sample injector was operated at 240 °C and in the pulsed-splitless mode. The initial GC oven temperature was 100 °C and held for 2 min, then to 250 °C at a rate of 25 °C/min, then to 260 °C at 1.5 °C/min, and finally to 325 °C at 25 °C/min. This final temperature was held for 7 min. Brominated FR quantification was achieved via selected ion monitoring (SIM) for m/z 79Br− and 81Br−. However, the SIMs for BDE-209 (m/z 487), 13C12−BDE-209 (m/z 495), and the syn- and anti-DDC−CO isomers (m/z 652) were different. For quality assurance and quality control, for each batch of biotic samples, one fish (from Ottawa market) tissue sample fortified with target chemicals (Figure 1 and SI Figure S1) was also analyzed to ensure good recoveries of the target analytes. During the analysis, some background contamination was observed for BDE-47, BDE-100, BDE-99, and BDE-209. Thus, for each batch of extractions, one blank sample was also included to investigate the possible background contamination during the analysis. FRs in the samples were background subtracted if FR contamination was present and the background peak response was >5% of that in a given fish sample fraction (i.e., BDE-209). The method limits of detection (MLODs) were based on a signal-to-noise ratio (S/N) of 3 and ranged from 0.001 to 0.1 ng/g ww depending on the specific FR. Recoveries of the internal standard FRs were generally >80% and 80% of the ∑PBDE concentrations of all of the 65 analyzed biotic samples. The pattern of BDE congeners was generally comparable with previous studies in the same area.5,25 Similar to previous reports,17 in the present study different species exhibited large differences in PBDE concentrations. For example, the mean ∑PBDE concentrations in top predator Lake Trout from Lake Ontario was as great as 94.8 ng/g ww (522 ng/g lw), as compared to Deepwater Sculpin from the same area were as low as 4.58 ng/g ww (84.3 ng/g lw). Lake Trout from Lake Ontario contained significantly greater ∑PBDE concentrations than those from Lake Erie. Greater concentrations in Lake Ontario fish as compared to those in Lake Erie were consistent with a previous study that reported ∑PBDE in edible portions of Great Lakes fish and the spatial trend was Lake Ontario ≫ Erie ≈ Huron ≈ Superior.25 This was also consistent with ∑PBDE levels in whole fish from basin-wide sampling where the order was Lake Ontario > Superior > Michigan > Huron > Erie. As shown from the PCA, for the different fish species there were contrasting BDE congener patterns (Figure 2A and SI Figure S3). Greater than 95% of the combined overall data variability accounted for by PC 1 and PC 2 (93.6% and 3.1% for Lake Erie, 89.6% and 8.0% for Lake Ontario). As indicated by PCA biplot of Lake Erie or Ontario fish, there are clear differences with the proportion of BDE-99 and BDE-47 to ∑PBDE concentrations, whereas there were no clear differences for the proportion of the other BDE congeners (i.e., BDE-28, BDE-49, BDE-66, BDE-100, BDE-119, BDE-85/155, BDE-154, BDE-153, and BDE-209) among fish species. Especially for fish from Lake Erie, the proportion of BDE-47 appeared to be differentiated along PC1 with greater proportions of fish occupying higher trophic levels, whereas BDE-99 appears to differentiate along PC1 with higher proportions in fish occupying

Figure 2. Biplot from the principal component analysis (principal component (PC) 1:93.6%, PC2:3.1%) of polybrominated diphenyl ether (PBDE) congener composition patterns in different fish species (A), correlation analysis between trophic level and proportion of BDE-47 (B) or BDE-99 (C) to ∑PBDEs in n = 39 individual fish samples, from Lake Erie, the Laurentian Great Lakes. In Figure 2A, ES, WP, LT, RS, TP, FD, RG, YP, and W represented Emerald Shiner, White Perch, Lake Trout, Rainbow Smelt, Trout Perch, Freshwater Drum, Round Goby, Yellow Perch, and Walleye, respectively. The number behind the fish species is the calculated trophic level (Figure 2A). D

DOI: 10.1021/acs.est.7b02338 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

common name

E

11.4

3.57 NA (3.10−4.43)

0.77 NA (0.60−0.99)

0.94 NA (0.75−1.16)

Rainbow Smelt

Round Goby

Trout Perch

4.58 NA (4.44−4.76)

0.96 NA (0.88−1.09)

White Perch

Yellow Perch

16.5

15.0

9.58 3.4 (2−6) 47.3 (3.23−14.0)

Walleye

9.07

7.73

54.0

4.38 Lake Trout 14.5 (3−10) (12.3−17.6)

2.19

22.8

2.19 NA (1.78−2.75)

9

10.2

Freshwater 2.18 NA Drum (0.91−3.53)

Emerald Shiner

Slimy Scul- 3.85 NA pin (2.46−5.25)

0.55 NA (0.27−0.83)

Round Goby

45.4

47.2

1420

6.9

8.05

9.4

2290

127

2.19

10.5

16.8

7.9

18.1

4.29 NA (2.50−6.07)

Rainbow Smelt

7.9

58.3

Wc

4310

8.5

18.3

Lb

Lake Trout 18.1 6.6 (3−10) 64.8 (7.23−26.4)

e

Aa

3

3

5F5M

3

3

3

4F/3M

3

3

2

2

2

9F/6M

2

2

Nd 38.5%g

TBPAE

0.013 (0.008− 0.019)

0.0054 (0.0054− 0.0054)

72.3%

pTBX

ND

ND

10.7 ND (9.52−11.8)

9.43 ND (8.39−10.0)

9.11 ND (2.49−12.6)

10.9 ND (10.6−11.5)

11.0 ND (10.6−11.2)

10.3 ND (10.3−10.3)

6.13 ND (4.05−8.91)

9.67 ND (9.21−10.3)

2.19 ND (1.78−2.75)

17.1 0.017 (17.0−17.2) (0.016− 0.019)

14.3 0.0054 (14.3−14.3) (0.0018− 0.0090)

15.5 0.025 (15.0−15.9) (0.016− 0.034)

ND

0.023 (0.015− 0.029)

0.013 (0.005− 0.027)

ND

0.005 (0.004− 0.007)

0.003 (0.002− 0.005)

0.009 (0.004− 0.022)

0.026 (0.011− 0.049)

ND

0.049 (0.038− 0.060)

0.030 (0.002− 0.059)

ND

0.051 (0.051− 0.052)

0.10 (0.097− 0.11)

100.0%

BB-153

1.59 (0.99− 2.19)

2.52 (2.28− 2.75)

83.1%

HBCDD

0.46 (0.34− 0.57)

2.44 (1.93− 2.94)

0.23 (0.20− 0.27)

0.011 (ND-0.020) 0.088 0.21 0.19 (ND(0.073−0.104) (0.15−0.32) 0.58)

0.24 (ND0.010 0.062 0.08 (0.009−0.010) (0.050−0.081) (0.06−0.10) 0.42)

0.055 0.20 (0.11−0.29) 0.19 1.19 (ND(0.040−0.074) (0.13−0.25) 2.57)

0.006 0.028 0.18 0.23 (ND(0.006−0.007) (0.023−0.032) (0.16−0.22) 0.35)

0.005 (ND-0.008) 0.031 0.13 ND (0.025−0.040) (0.08−0.18)

0.003 0.019 0.015 (0.002−0.004) (0.017−0.022) (0.012− 0.018)

0.029 0.14 (0.09−0.33) 0.18 2.76 (0.014−0.091) (0.13−0.42) (1.20− 6.26)

0.007 0.037 0.13 ND (0.006−0.008) (0.033−0.040) (0.13−0.15)

0.45 (0.34− 0.53)

0.31 5.97 (0.29−0.34) (1.95− 10.0)

0.041 (0.039− 0.043)

0.084 (0.036− 0.133)

0.023 0.064 0.057 (0.019−0.027) (0.055−0.070) (0.046− 0.072)

ND

ND

0.019 (ND− 0.039)

89.2%

anti-DDC-CO

100%

∑PBDEs

94.8 (19.1−162)

0.11 (0.10−0.11) 16.1 (12.6−19.6)

0.001 (ND0.003)

0.005 (ND0.011)

1.15 (1.06−1.32)

11.8 (7.21−33.7)

0.007 (ND0.015)

11.0 (6.50−17.3)

0.008 0.010 5.45 (0.005−0.011) (0.008−0.012) (4.37−6.24)

0.010 0.011 3.27 (0.009−0.012) (0.011−0.011) (2.52−4.58)

0.006 (ND0.011)

0.008 0.10 4.16 (0.006−0.009) (0.009−0.012) (3.90−4.64)

3.71 0.006 0.006 (0.004−0.007) (0.005−0.006) (2.60−5.17)

ND

0.004 (ND0.011)

0.010 0.010 3.14 (0.006−0.014) (0.008−0.012) (3.04−3.21)

0.005 0.005 3.60 (0.003−0.007) (0.004−0.006) (3.35−3.72)

0.11 (0.11−0.11)

0.016 0.034 5.53 (0.013−0.019) (0.028−0.040) (5.01−6.06)

0.009 0.010 15.5 (0.008−0.010) (0.007−0.012) (7.50−23.5)

0.036 (ND0.086)

0.017 0.021 4.58 (0.016−0.018) (0.020−0.022) (4.13−5.03)

0.010 0.012 11.7 (0.010−0.010) (0.011−0.013) (9.28−11.7)

87.7%

syn-DDC-CO

0.034 (ND0.31 (ND−0.74) 0.80 17.3 (0.17−1.40) (2.7−32.5) 0.079)

ND

0.029 (ND− 0.058)

83.1%

BB-101

0.020 (ND− 0.040)

56.9%

PBEB

ND

ND

16.8 0.091 (ND− 0.010 (ND− ND (15.7−18.5) 0.173) 0.028)

15.2 0.0053 (15.1−15.3) (0.0048− 0.0059)

11.9 0.046 (11.7−12.2) (0.040− 0.046)

δ15N

“A” means age (unit: year). b“L” means length (unit: cm). c“W” means weight (unit: g). d“N” means number, sample size. “9F/6M” means that the sample size is 15 with 9 female and 6 male fishes. e“NA” means not available. f“ND” means not detectable. gdetection frequency.

a

Erie

12.1 NA (10.1−14.1)

Deepwater 5.43 NA Sculpin (4.92−5.95)

Ontario Alewife

lakes

lipid/%

Table 1. Arithmetic Means and Ranges (ng/g wet Weight) Of Individual Non-PBDE Halogenated Flame Retardants (NPHFRs) and ∑PBDE concentrations in Fish from Lakes of Ontario and Erie, the Laurentian Great Lakes

Environmental Science & Technology Article

DOI: 10.1021/acs.est.7b02338 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Article

Environmental Science & Technology

fish samples.29 1,2-dibromo-4-(1,2-dibromoethyl)cyclohexane (TBECH) is an additive FR and contains equal amounts of two major diastereomers, α- and β-TBECH.7,37 α-/β-TBECH were detected in 5 of 65 present fish samples. The greatest wet concentration was 0.86 ng/g ww in one Lake Trout sample from Lake Erie. In a recent herring gull egg monitoring study, TBECH isomers were generally not detectable or at concentrations not exceeding 0.48 ng/g ww.5 None of the target PB-DiPhOBz and MeO-PB-DiPhOBz congeners were detectable in any of the 65 fish samples. Chen et al. first reported MeO-PB-DiPhOBzs in the eggs of herring gulls from colony sites in the Laurentian Great Lakes, and hypothesized that the MeO-PB-DiPhOBzs are degradation/ metabolism products and sourced from the FR tetradecabromo-1,4-diphenoxybenzene (TeDB-DiPhOBz).38,39 More recent studies have reported that TeDB-DiPhOBz has a short photolytic half-life in the order of minutes in organic solvents and when exposed to sunlight, and that enzymatic hydroxylation can occur to the photolytic and lower brominated PB-DiPhOBzs products of TeDB-DiPhOBz as demonstrated in in vitro biotransformation assays using harvested wild herring gull and adult male Wister-Han rat liver.40−43 In the present study, the lack of detection of PB-DiPhOBzs and MeO-PBDiPhOBzs in Great Lake forage and predatory fish suggests that aquatic derived dietary items are also not a source of PB-DiPhOBz congeners to herring gulls.38,39 Age- and Sex-Dependent Accumulation of Flame Retardants. Relationships between individual characteristics of fish (i.e., sex, age, length, and weight) and FR concentrations were examined for the Lake Trout from Lake Ontario (n = 15; nine female and six male), and the Walleye from Lake Erie (n = 10; five female and five male). The remaining species in our food web study were not included due to their small sample sizes. For most of detected FRs, significant differences were observed on their concentrations between male and female Walleye from Lake Erie. It should be emphasized that significant differences were also observed for physiological characteristics (i.e., ages, length, and weight) between male and female Walleye fishes. Among the FR concentrations for Lake Trout from Lake Ontario, a significant difference (t test, p < 0.05) between male and female fishes was only observed for BB-101 (female > male). These results suggested that sex did not influence FR concentrations in both Lake Trout and Walleye. This finding is consistent with a study on the influence of fish sex on mercury/total-PCB concentrations in which significant differences between sexes were detected in less than 25% of the tests conducted.44 FR concentrations (wet weight) increased as a function of increasing age of the Lake Trout or Walleye. Significantly positive linear correlative relationships were observed for 16 FRs (BDE-28, BDE-49, BDE-47, BDE-66, BDE-100, BDE-119, BDE-99, BDE-95/155, BDE-154, BDE-153, BDE-183, ∑PBDEs, BB-101, BB-153, and HBCDD) in Lake Trout from Lake Ontario between log-normalized concentration (wet weight) versus fish age, and T2 values ranged from 2.9 (BDE-47) to 3.9 (BDE-49) years (Table 2 and Figure 3). For FR concentrations (wet weight) in Walleye from Lake Erie, significant positive linear correlative relationships were found for BDE-66, BDE-119, BDE-99, BDE-85/155, BDE-154, BDE-153, pTBX, BB-153, and HBCDD, and T2 ranged from 2.0 (HBCDD) to 5.5 (BB-153) years (Table 2 and Figure 4). For ∑PBDE wet weight concentrations in Walleye, there was a

centrations (wet weight) were for Lake Trout (2.76 ng/g ww). HBCDD was not detectable in any of Freshwater Drum and Round Goby samples. Commercial production of polybrominated biphenyls (PBBs), an additive FR, began in the 1970s, and its manufacture was discontinued in the United States in 1976 due to the agriculture contamination episode in Michigan in 1973−1974.30 Despite the short period of production and usage, in the present study the detection frequencies of BB-101 and -153 were as high as 83.1% and 100%, respectively, and indicating their persistence in Lake Ontario and Erie fish. The high detection frequencies of BB-101 and BB-153 are consistent with those reported in Great Lakes herring gull eggs.5 The greatest mean BB-101 and −153 concentrations (wet weight) were 0.31 and 0.80 ng/g ww, respectively, both of which were determined in Lake Trout samples of Lake Ontario. Like BB-101 and BB-153 in herring gull eggs,5 there was a significant linear correlation relationship (p < 0.0001; r2 = 0.8786) between BB-101 and BB-153 concentrations in fishes from Lake Ontario and Lake Erie. DDC−COs isomers are used as polychlorinated FRs and produced by Oxychem. Initial reports of these DDC−CO isomers in the Great Lakes environment was in 2006, where syn- and anti-DDC−CO were found in air samples.31 In the present study, syn- and anti-DDC−CO were quantifiable in 87.7% and 89.2% of the 65 analyzed fish samples from the Lake Ontario and Lake Erie, and concentrations of syn- or anti-DDC−CO were consistently at subppb level. These high detection frequencies but low contamination levels of DDC− COs were in a good agreement with previous Great Lakes fish monitoring studies.29 In the present fish the concentrations of anti-DDC−CO were in general greater than for syn-DDC−CO. This is similar to DDC−CO isomer profiles reported in fish29 and herring gull eggs32 from sites spanning the Great Lakes. Also, our results were similar to that of ring-billed gull liver and plasma from birds sampled in the St. Lawrence River, Canada.33 Brominated benzenes, including DPTE, EHTBB, PBP-DBPE, PBBA, HBB, PBPAE, PBT, PBEB, TBCT, pTBX, BEHTBP, OBTMI, TBPAE, have been used as FRs in various applications, that is, thermoset polyester resin, polybutyleneterephthalate, paper, textiles, electronics.7,34 Previous studies have reported the occurrence of HBB, pTBX and PBEB in Great Lakes atmospheric samples.10,35,36 Our present study detected TBPAE (38.5%), pTBX (72.3%), PBEB (56.9%), PBT (16.9%), TBCT (6.2%) in at least one of 65 analyzed fish samples, however, we could not detect any of the other brominated benzenes in any of the analyzed samples. PBEB was not detectable in any samples from Lake Ontario, but had high detection frequency (37 out of 39) for Lake Erie fish samples with concentrations ranging from ND to 0.091 ng/g ww. The greatest mean PBEB concentration was 0.055 ng/g ww in Lake Erie Walleye samples. Compared to PBEB, TBPAE was quantifiable in 25 out 26 fish samples from Lake Ontario, but was not detectable in any of 39 Lake Erie fish samples. The greatest mean TBPAE concentrations were 0.091 ng/g ww in Lake Trout samples from Lake Ontario. The low concentrations of brominated benzenes in the present fish were in agreement with a recent monitoring study of fish or bird egg samples collected in the Great Lakes basin.5,6,29 Decabromodiphenyl ethane (DBDPE) is an additive FR and starting in the early 1990s was used as a FR replacement for the deca-BDE formulation.7 DBDPE was detected in only 7 of 65 fish samples in the present study. This result is consistent with a previous study where DBDPE was found in 3 of the 15 analyzed F

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Table 2. Calculated Doubling Ages (T2) or Half-Life Years (T1/2) from the Slope of the Plots of Natural Log FR Concentrations (Wet or Lipid Weight) vs Age lake trout (Lake Ontario; n = 15) wet weight basis Sc

p

T2

S

BDE-28 BDE-49 BDE-47 BDE-66 BDE-100 BDE-119 BDE-99 BDE-85/155 BDE-154 BDE-153 BDE-183 ∑PBDEs

0.189 0.18 0.2362 0.1867 0.2431 0.1835 0.2249 0.1858 0.2165 0.222 0.1914 0.2297

0.0039 0.0061 0.0001 0.0022 0) were observed for most of the FRs from the plot of natural log wet weight concentrations versus TL (based on δ15N-values) for both Lake Ontario and Lake Erie fishes (SI Table S4). However, these significant positive relationships disappeared when the FR concentrations were normalized with lipid weight (SI Table S5). The exceptions were BDE-28, BDE-47, BDE-119, BB-153, and HBCDD in Lake Ontario fishes, with TMF values of 1.60, 2.11, 2.33, 2.25, and 2.23, respectively, indicating their biomagnification potential in the Lake Ontario aquatic food web. For fishes from Lake Erie, after the FR concentrations were normalized with lipid weight, the relationships for most of FRs were statistically significant (p < 0.05) but negative (slope < 0) (SI Table S5). The difference in the slopes of fitted curves (before and after lipid weight normalization) for Lake Erie fishes could be caused by the difference of lipid content among different TL species. For example, we observed a positive and statistically significant (p < 0.0001) correlative relationship between lipid content and trophic levels of fishes (n = 39) from Lake Erie (SI Figure S8). Based on previous studies, PBDEs appeared to show different biomagnification potentials in different food webs. For example, Kelly et al. determined PBDE concentrations in a Canadian Arctic marine food web, and found that BDE-47 was the only BDE congener with a TMF statistically greater than 1.47 However, Hu et al. investigated PBDE trophodynamics in a freshwater food chain, and found that nine BDE congeners had TMFs greater than 1.48 In a recent study that investigated trophic transfer of PBDEs in a mixed Lake Erie food web (i.e., native and non-native species), most of BDE congeners

showed TMFs greater than 1 with exceptions of BDE-99 and BDE-209.15 Different fish species that occupy the same relative TL may have very different concentrations of contaminants depending the level of exposure and metabolic activity.49 In the present study, it is emphasized that the TMF values should be interpreted with caution due to the lack of higher trophic (i.e., fish-eating bird) or lower trophic (i.e., invertebrate) species in the food web comparisons. Implication for Future Studies. Over the past decades environmental scientists have used fish as key indicators for determining the environmental health/pollution status of aquatic ecosystems worldwide.11,50−54 Predatory and longlived species of fish are especially useful for contaminant biomonitoring. From surrounding waters as well as from their prey organism diets, predatory fish are exposed to organic pollutants with favorable bioaccumulation and biomagnification potentials.29,52,55 However, relationships between organic contaminant concentrations and fish ages remain poorly understood. Our present study provides clear evidence that concentrations of some FRs can increase as a function of the age of fish, that is, Lake Trout and Walleye, and we estimated the doubling ages for wet or lipid weight-based concentrations of several FRs to range from 2.9 to 6.4 years in Lake Trout from the slopes of the plots of natural log concentrations versus fish age. The present results also demonstrated that concentrations of FRs in fish from the same water body can vary widely depending on the age of the fish. In Lake Ontario for example, ∑PBDE concentrations were as low as 19.1 ng/g ww (264 ng/g lw) in a 3-year old Lake Trout, whereas in a 9-year old Lake Trout concentrations were as great as 162 ng/g ww (1070 ng/g lw). The findings of this study strongly suggest that fish age should be regarded as a key factor in future FR monitoring and surveillance in fish. Another critical fact related to human fish consumption in the Great Lakes. Although numerous local guides to eating fish have proposed that smaller fishes tend to contain less contaminants than larger fish of the same species,56 the underlying knowledge is limited to several specific contaminants, that is, mercury.45 Our results provide evidence that larger and older Lake Trout and Walleye contain greater concentrations of FRs. Further research is warranted in studying the speciesspecific differences of FR bioaccumulation in Great Lakes fish, and determining the differences between whole-body homogenates and edible parts of fishes in consideration of human consumption. H

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(8) Iqbal, M.; Syed, J. H.; Katsoyiannis, A.; Malik, R. N.; Farooqi, A.; Butt, A.; Li, J.; Zhang, G.; Cincinelli, A.; Jones, K. C. Legacy and emerging flame retardants (FRs) in the freshwater ecosystem: A review. Environ. Res. 2017, 152, 26−42. (9) Gauthier, L. T.; Hebert, C. E.; Weseloh, D. V.; Letcher, R. J. Dramatic changes in the temporal trends of polybrominated diphenyl ethers (PBDEs) in herring gull eggs from the Laurentian Great Lakes: 1982−2006. Environ. Sci. Technol. 2008, 42 (5), 1524−30. (10) Venier, M.; Salamova, A.; Hites, R. A. Halogenated flame retardants in the Great Lakes environment. Acc. Chem. Res. 2015, 48 (7), 1853−61. (11) Zhu, L. Y.; Hites, R. A. Temporal trends and spatial distributions of brominated flame retardants in archived fishes from the Great Lakes. Environ. Sci. Technol. 2004, 38 (10), 2779−84. (12) Liu, L.; Venier, M.; Salamova, A.; Hites, R. A. A novel flame retardant in the Great Lakes atmosphere: 3,3′,5,5′-tetrabromobisphenol A bis(2,3-dibromopropyl) ether. Environ. Sci. Technol. Lett. 2016, 3 (5), 194−199. (13) Salamova, A.; Ma, Y.; Venier, M.; Hites, R. A. High levels of organophosphate flame retardants in the Great Lakes atmosphere. Environ. Sci. Technol. Lett. 2014, 1 (1), 8−14. (14) Arnot, J. A.; Gobas, F. A. P. C. A review of bioconcentration factor (BCF) and bioaccumulation factor (BAF) assessments for organic chemicals in aquatic organisms. Environ. Rev. 2006, 14 (4), 257−297. (15) Perez-Fuentetaja, A.; Mackintosh, S. A.; Zimmerman, L. R.; Clapsadl, M. D.; Alaee, M.; Aga, D. S. Trophic transfer of flame retardants (PBDEs) in the food web of Lake Erie. Can. J. Fish. Aquat. Sci. 2015, 72 (12), 1886−1896. (16) Peng, H.; Wan, Y.; Zhang, K.; Sun, J. X.; Hu, J. Y. Trophic transfer of dechloranes in the marine food web of Liaodong Bay, North China. Environ. Sci. Technol. 2014, 48 (10), 5458−5466. (17) Law, K.; Halldorson, T.; Danell, R.; Stern, G.; Gewurtz, S.; Alaee, M.; Marvin, C.; Whittle, M.; Tomy, G. Bioaccumulation and trophic transfer of some brominated flame retardants in a Lake Winnipeg (Canada) food web. Environ. Toxicol. Chem. 2006, 25 (8), 2177−86. (18) McGoldrick, D. J.; Clark, M. G.; Keir, M. J.; Backus, S. M.; Malecki, M. M. Canada’s national aquatic biological specimen bank and database. J. Great Lakes Res. 2010, 36 (2), 393−398. (19) Greaves, A. K.; Letcher, R. J.; Chen, D.; McGoldrick, D. J.; Gauthier, L. T.; Backus, S. M. Retrospective analysis of organophosphate flame retardants in herring gull eggs and relation to the aquatic food web in the Laurential Great Lakes of North America. Environ. Res. 2016, 150, 255−263. (20) Chen, D.; Martin, P.; Burgess, N. M.; Champoux, L.; Elliott, J. E.; Forsyth, D. J.; Idrissi, A.; Letcher, R. J. European starlings (Sturnus vulgaris) suggest that landfills are an important source of bioaccumulative flame retardants to Canadian terrestrial ecosystems. Environ. Sci. Technol. 2013, 47 (21), 12238−12247. (21) Chen, D.; Letcher, R. J.; Martin, P. Flame retardants in eggs of American kestrels and European starlings from southern Lake Ontario region (North America). J. Environ. Monit. 2012, 14 (11), 2870−6. (22) Saito, K.; Sjodin, A.; Sandau, C. D.; Davis, M. D.; Nakazawa, H.; Matsuki, Y.; Patterson, D. G., Jr. Development of a accelerated solvent extraction and gel permeation chromatography analytical method for measuring persistent organohalogen compounds in adipose and organ tissue analysis. Chemosphere 2004, 57 (5), 373−81. (23) Hebert, C. E.; Hobson, K. A.; Shutt, J. L. Changes in food web structure affect rate of PCB decline in herring gull (Larus argentatus) eggs. Environ. Sci. Technol. 2000, 34 (9), 1609−1614. (24) McGoldrick, D. J.; Letcher, R. J.; Barresi, E.; Keir, M. J.; Small, J.; Clark, M. G.; Sverko, E.; Backus, S. M. Organophosphate flame retardants and organosiloxanes in predatory freshwater fish from locations across Canada. Environ. Pollut. 2014, 193, 254−61. (25) Gandhi, N.; Gewurtz, S. B.; Drouillard, K. G.; Kolic, T.; MacPherson, K.; Reiner, E. J.; Bhavsar, S. P. Polybrominated diphenyl ethers (PBDEs) in Great Lakes fish: Levels, patterns, trends and

ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.7b02338. Further details are given on concentrations (ng/g ww and ng/g lw) of individual PBDE congeners, concentrations of (ng/g lw) of individual non-PBDE halogenated FRs, trophic magnification factor (TMF, based on both ng/g ww and ng/g lw), chemical structure of target PB-DiPhOBzs and MeO-PB-DiPhOBzs, sampling locations, PCA analysis for PBDEs in fishes from Lake Ontario, Log transformed FR concentrations (ng/g lw) versus fish (Lake Trout or Walleye) ages, biological characteristics (lipid content, length, weight) versus fish (Lake Trout or Walleye) ages (PDF)

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AUTHOR INFORMATION

Corresponding Author

*Phone: 1-613-998-6696; fax: 1-613-998-0458; e-mail: robert. [email protected]. ORCID

Robert J. Letcher: 0000-0002-8232-8565 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The Chemicals Management Plan (ECCC), the Natural Science and Engineering Research Council (NSERC) of Canada (to R.J.L.) provided financial support. The collection of the aquatic biota samples and subsequent processing were accomplished by Michael Keir, Mandi Clark, and Mary Malecki (ECCC)..

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REFERENCES

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