Subscriber access provided by UNIV OF NEW ENGLAND ARMIDALE
Article
Bioaccumulation of polybrominated diphenyl ethers (PBDEs) and alternative halogenated flame retardants in a vegetation-caribou-wolf food chain of the Canadian Arctic Adam David Morris, Derek Muir, Keith Solomon, Camilla Teixeira, Mark Duric, and Xiaowa Wang Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b04890 • Publication Date (Web): 10 Jan 2018 Downloaded from http://pubs.acs.org on January 10, 2018
Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.
Environmental Science & Technology is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.
Page 1 of 40
Environmental Science & Technology
Bioaccumulation of polybrominated diphenyl ethers (PBDEs) and alternative halogenated flame retardants in a vegetation-caribou-wolf food chain of the Canadian Arctic
Adam D. Morris,†* Derek C.G. Muir,‡ Keith R. Solomon,† Camilla F. Teixeira,‡ Mark D. Duric,‡ Xiaowa Wang‡ †
School of Environmental Sciences, University of Guelph, 50 Stone Road East, Guelph, ON,
Canada, N1G 2W1 ‡
Aquatic Contaminants Research Division, Environment and Climate Change Canada, 867
Lakeshore Road, Burlington, ON, Canada, L7S 1A1
Total word count (Abstract through SI description) = 7336 Main text = 5836 Table 1 + Table 2 + Table 3 = 3 × 300 words =900 words Figure 1 + 2 = 2 × 300 words = 600 Words * Corresponding author. Phone: (289)259-6089); E-mail:
[email protected], ORCID ID : orcid.org/0000-0002-0695-023X. Current address: National Wildlife Research Centre, 1125 Colonel By Drive/Raven Road, Office 330, Desk J, Ottawa, ON, Canada, K1S 5B6
1
ACS Paragon Plus Environment
Environmental Science & Technology
TOC Art Graphic for TOC
1 2
Keywords: Bioaccumulation, trophic magnification, halogenated flame retardants,
3
polybrominated diphenyl ethers, terrestrial
4
2
ACS Paragon Plus Environment
Page 2 of 40
Page 3 of 40
5 6
Environmental Science & Technology
Abstract The trophodynamics of halogenated flame retardants (HFRs) including polybrominated
7
diphenyl ethers (PBDEs) and alternative HFRs were investigated in the terrestrial, vegetation-
8
caribou-wolf food chain in the Bathurst Region of northern Canada. The greatest concentrations
9
in vegetation (geometric mean of lichens, moss, grasses, willow, and mushrooms) were of the
10
order 2,4,6-tribromophenyl allyl ether (TBP-AE) (10 ng g-1 lw) > BDE47 (5.5 ng g-1 lw) >
11
BDE99 (3.9 ng g-1 lw) > BDE100 (0.82 ng g-1 lw) > 1,2,3,4,5-pentabromobenzene (PBBz) (0.72
12
ng g-1 lw). Bioconcentration between types of vegetation was consistent, though it was typically
13
greatest in rootless vegetation (lichens, moss). Biomagnification was limited in mammals; only
14
BDE197, BDE206 to -208 and ΣPBDE biomagnified to caribou from vegetation
15
[biomagnification factors (BMFs) = 2.0–5.1]. Wolves biomagnified BDE28/33, BDE153,
16
BDE154, BDE206, BDE207, and ΣPBDE significantly from caribou (BMFs = 2.9–17) but
17
neither mammal biomagnified any alternative HFRs. Only concentrations of BDE28/33,
18
BDE198, nonaBDEs, and ∑PBDE increased with trophic level, though the magnitude of
19
biomagnification was low relative to legacy, recalcitrant organochlorine contaminants [trophic
20
magnification factors (TMFs) = 1.3–1.8]. Despite bioaccumulation in vegetation and mammals,
21
the contaminants investigated here exhibited limited biomagnification potential and remained at
22
low parts per billion concentrations in wolves.
3
ACS Paragon Plus Environment
Environmental Science & Technology
23 24
Introduction Halogenated flame retardants (HFRs) are consistently reported in environmental media
25
and wildlife across the globe. The polybrominated diphenyl ethers (PBDEs) are environmentally
26
abundant brominated FRs, with 209 congeners that were available as three commercial (c)
27
mixtures (c-pentaBDE, c-octaBDE, c-decaBDE).1 The c-pentaBDE and c-octaBDE mixtures
28
have been under phase-out in Europe and North America since the early 2000s, with c-decaBDE
29
regulated later.2-4 The prominent congeners in all three c-PBDE mixtures are now regulated
30
globally as new persistent organic pollutants (POPs) as of 2009 (c-penta- and c-octaBDE) or
31
2017 (c-decaBDE).5 Despite regulations on production and new applications, PBDEs are
32
released to the environment from a number of in-use products.6 These regulations have also led
33
to the production of replacement (alternative) HFRs which are also detected in the environment,
34
but less consistently than PBDEs.7-11
35
Some of the most environmentally relevant alternative HFRs such as pentabromotoluene
36
(PBT), hexabromobenzene (HBB), 1,2-bis 2,4,6-tribromophenoxy ethane (BTBPE),
37
hexabromocyclododecane (HBCDD), and pentabromoethylbenzene (PBEB) have been detected
38
throughout the arctic environment and the arctic marine food web.9, 12-17 Despite these
39
observations, few studies have reported on the trophodynamics of these compounds in the
40
terrestrial environment, particularly in the Arctic or Subarctic. The limited studies of PBDEs in
41
terrestrial food chains suggest that like the marine environment, the biomagnification of PBDEs
42
in mammals is congener, location, and food chain-specific.9, 18-24 Modeling has shown that
43
organic contaminants with intermediate-high octanol-water partitioning (KOW > 102) and high
44
lipid-air partitioning (KOA ≥106), including some PBDEs and alternative HFRs, can theoretically
45
biomagnify more effectively in terrestrial food chains than in aquatic ones.11 This is primarily 4
ACS Paragon Plus Environment
Page 4 of 40
Page 5 of 40
Environmental Science & Technology
46
due to reduced depuration across the lungs and kidneys of terrestrial animals, an effect that can
47
be particularly apparent in food chains with multiple air-breathing consumers.11, 25, 26
48
The objective of this study was to improve scientific understanding of the
49
bioaccumulation of PBDEs and alternative HFRs in terrestrial food chains. The study system was
50
the vegetation-caribou-wolf food chain, sampled within the Bathurst Region caribou herd range,
51
which overlaps the border between Nunavut (NU) and the Northwest Territories (NWT,
52
Canada). This food chain was selected in conjunction with the Government of the NWT due to
53
concerns regarding population declines of the caribou herd from approximately 186 000 to 22
54
000 (2003–2015) and the related ecological and socioeconomic impacts.27, 28 Nearby mining
55
operations, roadways, wildfires in their winter range, and climate change were among the
56
challenges highlighted in the Bathurst Caribou Range Plan.29 Ecological interactions and current
57
use pesticides,30 legacy organochlorine (OC) contaminants,11, 25, 31 and perfluorinated alkyl
58
substances32 have previously been reported in this food chain. However the trophodynamics of
59
HFRs have been poorly described in terrestrial ecosystems and in general there has been much
60
less work on studies of trophic magnification factors (TMFs) in terrestrial food webs compared
61
to aquatic systems.33 Therefore, in addition to adding to the overall profile of HFR
62
contamination, this study provides valuable data for assessment of terrestrial TMFs, as well as
63
for food chain modeling.
64
Materials and Methods
65
Sample collection and preparation
66
Samples of lichens (Cladonia rangiferina/mitis and Flavocetraria cucullata, both n = 6),
67
moss (Rhytidium rugosum, n = 6), willow leaves (Salix sp., n = 6), graminoids (Eriophorum
68
vaginatum and Carex aquatilis, n = 8) and mushrooms (not speciated, n = 5) were collected 5
ACS Paragon Plus Environment
Environmental Science & Technology
69
within the Bathurst caribou herd range (64°04′N, 114°08′W) in the Northwest Territories (NWT)
70
in August 2009. Muscle and liver samples were collected from caribou (Rangifer tarandus
71
groenlandicus, n = 6) and wolves (Canis lupus, n = 7) in 2008-2009 and 2010 respectively by
72
local subsistence hunters and trappers. Details of sample collection have been published
73
previously [Supporting Information (SI), Table S1].30
74 75
Analytes, sample extraction and cleanup
76
The analytes and recoveries are provided in the SI (Table S2, structures in Figure S1).
77
The PBDEs and alternative HFRs analyzed included 28 tri- to nonaBDE congeners (BDE17–
78
BDE208), 1,2-bis(2,4,6-tribromophenoxy) ethane (BTBPE), 2,4,6-tribromophenyl allyl ether
79
(TBP-AE), 2,4,6-tribromophenyl 2-bromoallyl ether (TBP-BAE), 2,4,6-tribromophenyl 2,3-
80
dibromopropyl ether (TBP-DBPE), 1,2,3,4,5-pentabromobenzene (PBBz), pentabromotoluene
81
(PBT), pentabromoethylbenzene (PBEB), hexabromobenzene (HBB), syn- and anti-Dechlorane
82
plus (DP) (nomenclature from Bergman et al.34). The results of spike-recovery experiments were
83
consistent for the mono-heptaBDEs (82–105%), and acceptable for the octa-nonaBDEs (57–
84
93%), though recoveries decreased and became more variable with increasing bromination.
85
Inconsistency of recoveries and in quantifications using two standards when run for confirmation
86
(concentrations were 21–110% different) led us to eliminate BDE209 from further discussion.
87
The alternative HFRs had more variable recoveries (42%–147%; Table S2), which may be
88
related to their structural diversity (details in the SI).
89
The sample extraction methods followed Hoesktra et al.35 and Johansen et al.,36 except
90
that pressurized solvent extraction was used (ASE 300, Dionex, Sunnyvale, CA). Samples of
91
muscle and liver (5–10 g) were extracted for contaminant analysis using the ASE, with the 6
ACS Paragon Plus Environment
Page 6 of 40
Page 7 of 40
Environmental Science & Technology
92
method and cleanup as described in Morris et al.,30 with secondary fractionation for HFR
93
analyses. Lipid contents were determined gravimetrically via gel permeation chromatography
94
(details of extraction/cleanup in the SI).
95 96
Stable isotopes of carbon and nitrogen (13C/12C = δ13C and 15N/14N = δ15N respectively) were analyzed in muscle and have been reported previously with their analytical details.30
97 98 99
Data analyses, quality assurance and quality control (QA/QC) Separation and measurement of contaminants was achieved using gas chromatography-
100
low resolution mass spectrometry (GC-LRMS) with electron-capture negative chemical
101
ionization (NCI) with the MS run in selective ion monitoring (SIM) mode (Agilent 7890A GC–
102
5975C MS, Agilent Technologies, Mississauga, ON, Canada). Analytes were identified and
103
quantified based on comparison with retention times and the relative responses of multilevel,
104
external calibration standards. BDE198 co-eluted with BDE199, -200 and -203, but will be
105
referred to as “BDE198”. Details regarding compounds excluded for QA/QC issues are provided
106
in the SI.
107
Batches of 10 to 12 samples were extracted with method blanks and standard reference
108
materials (SRM 1588b or SRM 1947, National Institute of Standards and Technology,
109
Gaithersburg, MD, USA, Table S2 and Table S3). Vegetation, caribou and wolf data were blank
110
corrected separately, and data were recovery corrected relative internal spikes of BDE71
111
(discussed further in the SI). Method detection limits (MDLs) were established as three times the
112
standard deviation of the blank concentrations (Table S2). When detection frequencies (DFs) of
113
an analyte were below 20 % in a subset of samples (type of vegetation, mammalian tissue), it
114
was considered a non-detect (< MDL) When DFs were greater than 20 % but were not 100 %, 7
ACS Paragon Plus Environment
Environmental Science & Technology
Page 8 of 40
115
MDL/2 concentrations were substituted for zero values in the wet weight (ww) dataset. If
116
concentrations were below MDLs these were included rather than substituting MDL/2 values.37
117
Instrument detection limits (IDLs)38 were used in place of MDLs if contaminants were not
118
detected in the blanks (details of data handling in the SI).
119
Lipid equivalent-normalized concentrations (φLeq) were calculated for vegetation to
120
incorporate the sorption capacity of proteins and carbohydrates11, 18 while the φLeq in the
121
relatively lipid-rich samples (mammals) were considered to be negligibly different than their
122
lipid fractions (φLipid) as in previous investigations (calculations in the SI).18 Though correction
123
for the φLeq accounts for the sorption capacity of some other non-lipid components, there are
124
other components of vegetation that may not be accounted for here and that may affect the
125
sorption of organic contaminants. Previously outlined methods were used here for consistency.11
126
Total body concentrations (TBCs) were based on measured values in muscle and liver
127
and estimated concentrations in fat, assuming that these tissues were the main deposits for HFRs.
128
Calculations used previously reported body composition estimates32 and separately estimated
129
body fat percentages (details of calculations in the SI).31
130
Bioaccumulation and biomagnification
131
Volumetric bioconcentration factors (BCFv) were calculated as the ratio of the geometric
132
mean concentration of an analyte in vegetation to the total concentration (particulate + gas
133
phases) in air from Alert, NU (Hung et al.39 supplied separately for 2009 alone) using Equations
134
1 and 2:
135
Cv = Cm × ρ × (1.0 × 106)
(1)
136
BCFv = Ct,v/CA,T
(2)
8
ACS Paragon Plus Environment
Page 9 of 40
Environmental Science & Technology
137
Air samples were collected bi-weekly and the annual concentration was used for analysis here.39
138
Cv is the φLeq corrected, volumetric concentration (pg m-3), Cm represents the mass-based ww
139
tissue concentration in vegetation (pg g-1 ww), ρ is the density of the vegetation (g cm-3, densities
140
in the SI), 1.0 × 106 is the pg cm-3 to pg m-3conversion factor and CA is the air concentration (pg
141
m-3). Mean BCFv values were then calculated for “Lichens,” “Green Plants” (moss, willow,
142
graminoids), mushrooms, and “Total Vegetation (VT, all vegetation included),” as well as
143
functionally grouped “Rootless” (lichens and moss) or “Rooted” (willow and graminoids)
144
vegetation. Mushrooms are non-vascular organisms (fungi); however they were included in the
145
geometric means calculated for VT. The BCFv has been shown to be a good measure of
146
contaminant concentrations in fresh plant tissues, and relates well to the fugacity capacity in
147
modeling studies.40
148
Biomagnification factors (BMFs) for wolves were calculated as the ratio of the arithmetic
149
mean, lipid-normalized concentrations in wolves to caribou, using tissue specific concentrations
150
and TBCs. BMFs in caribou were calculated using TBCs compared to mixed diets of vegetation,
151
calculated using proportions observed in feces of caribou from the Yukon Territory41 for
152
fall/winter (70 % lichens, 30 % moss), spring (40 % lichens, 60 % graminoids) and summer (100
153
% willow) as in Morris et al.30 The proportionate BMFs were then modeled using Monte Carlo
154
analyses (Crystal Ball, Oracle Inc.) to obtain means and standard deviations. The different
155
proportions of vegetation used for the caribou BMFs were used to gauge the effects of variable
156
diet composition on the biomagnification of the HFRs. Since caribou and wolf samples were
157
largely collected in fall or late summer (respectively), the “fall/winter” estimates are the most
158
applicable (calculations provided in the SI).
9
ACS Paragon Plus Environment
Environmental Science & Technology
159
Trophic magnification factors (TMFs) were calculated as the anti-log of the slope of log-
160
linear regression analyses of individually plotted, lipid-normalized concentrations (CB, pg g-1 lw)
161
versus TL.42 TMFs were calculated using TBCs for mammals in combination with different
162
groups of vegetation (VT, lichens, or green plants). TMFs were only presented when the DFs of
163
the analytes exceeded 50 % across all of the biota included in the regression (Table S9).
164
Statistics
165
Sigmaplot v.11 and SYSTAT® v.11.0 (Systat Software, Inc) were used for the statistical
166
analyses. Significant results were all assessed against a type-1 error rate of α = 0.05. The n
167
values were relatively small which made normality tests less reliable, and also complicated the
168
assessment of the type-1 error rate. Large differences in concentration are briefly discussed as
169
these do provide some evidence of potential differences; however the variability of the data
170
affected the significance of many of the tests. The log-transformed data were a better
171
representation of the normal distribution (Shapiro-Wilk Test), so the data are presented as
172
geometric means with their 95 % confidence intervals (CIs) and all statistical tests used log-
173
transformed data.
174
Multigroup comparisons were made using one-way analysis of variance (ANOVA) with
175
Tukey’s post hoc tests. Pair-wise comparisons between mammals, and tests of BMFs for
176
significant differences from one were assessed using 2-tailed student’s t-tests. When the log-
177
transformed data failed the normality test (p < 0.05), equal variance tests (Levene’s median test,
178
p < 0.05) or the power did not exceed 80 %, Kruskal-Wallis ANOVAs on ranks (with Dunn’s
179
post hoc test), or Mann-Whitney U-tests were applied for multi-group and two-group
180
comparisons (with recognition that the normality tests were less reliable due to the small n
181
values). 10
ACS Paragon Plus Environment
Page 10 of 40
Page 11 of 40
Environmental Science & Technology
182
TMFs were reported when log-linear regressions had slopes significantly different from
183
zero (p < 0.05). Pearson correlation analysis between bioaccumulation metrics (logBCFv, BMF,
184
TMF) and the logKOA or logKOW used empirical values for the octanol partition coefficients
185
where possible, or the values provided by the US EPA Estimation Programs Interface Suite (EPI
186
Suite) v. 4.10 if they were unavailable (Table S6).
187 188
Results & Discussion
189
Ecological interactions
190
The ecological data have been discussed previously,30 but are outlined here for context.
191
These ecological interactions could also be useful in future assessments given the potential
192
impact of climate warming on vegetation throughout the Arctic environment.43 Caribou graze
193
opportunistically, having a seasonally variable diet.41 This complicates assessments of dietary
194
transfer of contaminants from specific food sources, as the vegetation had broad ranges of stable
195
isotope values for both δ13C [-23.8 ± 0.783 ‰ (Flavocetraria) to -29.9 ± 0.791 ‰ (willow)], and
196
δ15N [-5.19 ± 1.86 ‰ (Cladonia) to 4.24 ± 2.02 ‰ (graminoids)] (Table S4). This range of stable
197
isotope values reflects different modes of nutrient acquisition and interactions between the
198
vegetation such as atmospheric uptake alone (lichens, moss), across roots (graminoids, willows),
199
through decomposition (fungi/mushrooms), and via mycorrhizal symbioses between fungal
200
mycelia and willow roots.30, 44, 45
201
No vegetation (dietary) δ13C signal overlapped exceptionally well with the caribou δ13C
202
except Flavocetraria lichens (Table S4 and Table S7), likely due to the efficient mixing and
203
fermentation characteristic of digestion in ruminants,30, 46 in addition to relatively long isotopic
204
turnover times in ruminant muscle (≈ 4.5 months).47 These factors made direct dietary 11
ACS Paragon Plus Environment
Environmental Science & Technology
205
interpretation illogical, so dietary compositions reported from a nearby caribou herd in
206
fall/winter, spring and summer were used to test the effects of a variable diet (see methods and
207
SI).41 The wolves in the Bathurst Region are known to feed primarily on caribou from this area,48
208
an observation supported by the overlap of the δ13C in wolves (-23.1 ± 0.643 ‰) compared with
209
that of caribou (-23.3 ± 0.255 ‰).
210
The calculated TLs were logical for most vegetation (TLs = 1.0–1.5), and the consumers
211
(mushrooms = 3.2 ± 0.20, caribou = 3.8 ± 0.081, wolves = 4.6 ± 0.16). Graminoid δ15N signals
212
are representative of soil,44, 45 and thus had a relative enrichment of δ15N and an illogical TL out
213
of range of the other primary producers (TL = 3.5 ± 0.53, Table S4). To position them in the
214
food chain for TMF analyses, graminoids were randomly assigned TLs between 1.0 and 1.5.
215 216
Concentrations and bioconcentration of HFRs in vegetation
217
When assessed in VT, the descending order of geometric mean concentrations of
218
individual contaminants was TBP-AE (10 ng g-1 lw) > BDE47 (5.5 ng g-1 lw) > BDE99 (3.9 ng
219
g-1 lw) > BDE100 (0.82 ng g-1 lw) > PBBz (0.72 ng g-1 lw) > BDE153 (0.49 ng g-1 lw) > BTBPE
220
(0.45 ng g-1 lw) (Table S4). BDE28/33, -66, and -154, were detected at lesser frequencies and
221
concentrations (0.30–0.35 ng g-1 lw), but were found in at least one caribou food source. The
222
octa- and nonaBDEs, which are generally particle-bound in the environment,49 had the fewest
223
detections and had high variability in vegetation. When concentrations were assessed in
224
vegetation grouped as lichens, green plants, or mushrooms, there were few differences in
225
concentrations. TBP-AE was the only compound that varied significantly, being statistically
226
greater in lichens (17 ng g-1 lw) than mushrooms (5.0 ng g-1 lw) (KW ANOVA with Dunn’s test,
227
p < 0.05) (Figure 1A, Table S4). 12
ACS Paragon Plus Environment
Page 12 of 40
Page 13 of 40
Environmental Science & Technology
228
The Σtri-heptaBDE concentrations were greatest in moss (34 ng g-1 lw) > Cladonia (29
229
ng g-1 lw) ≥ mushrooms (12 ng g-1 lw) > graminoids (9.8 ng g-1 lw) > willow (5.5 ng g-1 lw) >
230
Flavocetraria (0.58 ng g-1 lw). The ∑tri-heptaBDE of Flavocetraria was significantly smaller
231
than all other vegetation except willow, and no other significant differences were observed (KW
232
ANOVA with Dunn’s tests, Table S4). The ∑tri–heptaBDE concentrations in Cladonia lichens
233
were greater than those previously reported in Northern Quebec [9.3 (2.9–30) ng g-1 lw] between
234
1999–2003,18 however comparisons should be made cautiously due to the substantial spatial and
235
temporal differences.
236
Most HFRs had their greatest concentrations in Cladonia lichens and/or moss, though
237
few statistical differences were detected between vegetation due to the variability in
238
concentrations (Table S4). Concentrations of HFRs in Flavocetraria lichens were particularly
239
small in contrast to Cladonia, and there were few detections in excess of the MDLs (Table S4).
240
This is likely due to their fruticose (Cladonia) versus foliose structures, and the maximization of
241
surface area for gas/nutrient/contaminant exchange in fruticose species.50 Statistical differences
242
were only observed for less prevalent PBDEs (BDE28/33, -49, -66), and HBB, BTBPE, and syn-
243
DP, which were only greater in moss (range 0.64–1.4 ng g-1 lw) than in Flavocetraria and/or
244
willow (< MDL) (Table S4).
245
The greatest concentrations among the alternative HFRs were found for TBP-AE and
246
PBBz (10 and 0.72 ng g-1 lw respectively in VT), which had concentrations comparable to
247
prominent PBDE congeners (BDE47, -99, -100, -153, -154; Table S4). BTBPE was detected less
248
frequently than TBP-AE and PBBz, but was generally more abundant (VT = 0.45 ng g-1 lw) than
249
most of the remaining alternative HFRs (Figure 1A, Table S4). A significant, positive
250
relationship was observed between concentrations of TBP-AE and BTBPE in VT (Pearson r2= 13
ACS Paragon Plus Environment
Environmental Science & Technology
251
0.12, p = 0.036, n = 37) and green plants (r2= 0.32, p = 0.0087, n = 20) (Table S5), which may be
252
a result of common delivery pathways, and/or of environmental weathering and
253
biotransformation (Figure S2).51, 52 TBP-AE concentrations can be increased by both photolytic
254
and anaerobic debromination of TBP-DBPE for example,7, 51 however how this affected patterns
255
here is unknown because TBP-BAE and TBP-DBPE were not detected.
256
Most of the bromobenzene compounds had very low frequencies of detection excluding
257
PBBz (Table S4). The order of decreasing concentrations in VT were PBBz > PBT (0.24 ng g-1
258
lw) > HBB (0.23 ng g-1 lw) (Table S4). A wider range of bromobenzenes were detected in air
259
around the Great Lakes,53 but transport to the Arctic may be limited for many due to their short
260
atmospheric half-lives. PBBz, HBB, and PBT have greater atmospheric stability (Table S6)
261
resulting in a greater likelihood of reaching high latitudes. The DP isomers were found at low
262
frequencies (≤ 33 %) and concentrations (0.23–0.94 ng g-1 lw) in moss (anti- and syn-DP) and
263
mushrooms (syn-DP only), though detections are supportive of reports of DP in arctic media.12, 15
264
The homologue group profile of PBDEs measured in air at Alert (6 % triBDEs, 34 %
265
tetraBDE, 27 % pentaBDEs, 3 % hexaBDEs, 5 % heptaBDEs, 25 % decaBDE) resembled the
266
composition of c-pentaBDE (Bromkal 70-5DE = < 1 % triBDEs, 40 % tetraBDEs, 52 %
267
pentaBDEs, 8 % hexaBDEs, < 1 % heptaBDEs), though air had measurable concentrations of
268
decaBDE (based on total air concentrations, Figure 2).1 Comparing vegetation types (note that
269
Flavocetraria were excluded from this comparison because they had few detectable
270
concentrations) revealed only minor differences in their PBDE profiles relative to air and the
271
technical mixture. The bulk of the ∑PBDE burden in vegetation are tetra- and pentaBDEs with
272
minor contributions from the tri- and hexaBDEs, as well as some contribution from the hepta- to
273
octaBDEs in mushrooms. Moss had a greater proportion of tetraBDEs and a less contribution 14
ACS Paragon Plus Environment
Page 14 of 40
Page 15 of 40
Environmental Science & Technology
274
from the pentaBDEs (≈ 60 % and 28 %, respectively) than did the remaining vegetation (≈44–50
275
% and 42–50 %, respectively), with triBDEs only contributing to the ∑PBDE of Cladonia and
276
moss (3.1–3.4 %). Accumulation of PBDEs in vegetation was in relative proportion to the
277
pattern of congeners in the c-pentaBDE mixture and air, with the exception of BDE209 (Figure
278
2).
279
The logBCFv values in vegetation grouped as VT, lichens, green plants, or mushrooms
280
also varied within a relatively small range (Table 1). The greatest values were observed for
281
BTBPE (logBCFv = 8.2–8.6) , while the smallest logBCFv values were found for BDE28/33, -85,
282
and -183 (logBCFv = 7.2–7.3), which likely corresponds to their lesser representation in the c-
283
PBDE mixtures and atmosphere.1, 39. The most frequently detected PBDEs varied little across
284
vegetation types, including BDE47 (logBCFv = 7.4–7.7), BDE99 (7.5–7.8), BDE100 (7.5–7.6),
285
BDE153 (7.7–8.0), and BDE154 (7.7). Note that the air concentrations were collected
286
throughout 2009 at Alert, NU, and thus represent average air concentrations about 2000 km north
287
of the Bathurst caribou range. Therefore, the BCFv values may be overestimated due to low air
288
concentrations. However, these were the only available atmospheric HFR data for the Canadian
289
Arctic.39 The vegetation also have different life-cycles and modes of nutrient acquisition as
290
indicated by their stable isotope values (as previously discussed),54,30 which affects their
291
contaminant exposure regimes. These factors do increase the uncertainty of the BCFv, however
292
they were suitable to compare bioconcentration between types of vegetation and contaminants.
293 294 295 296
Concentrations of HFRs in mammals The TBCs of HFRs were almost universally greater in wolves than caribou (BDE99 and PBBz were exceptions; Figure 1B, Table S7). The ΣPBDE concentration in wolves was 15
ACS Paragon Plus Environment
Environmental Science & Technology
297
approximately two times greater than caribou (51 ng g-1 lw and 23 ng g-1 lw), and the Σtri-
298
heptaBDE was approximately three times greater in wolves, though they were not significantly
299
different (2-tailed t tests, p > 0.05). The greatest TBCs in mammals were: wolves BDE207 (10
300
ng g-1 lw) > BDE206 (8.7 ng g-1 lw) > BDE208 (5.0 ng g-1 lw) > BDE28 (4.1 ng g-1 lw) >
301
BDE47 (3.3 ng g-1 lw); caribou BDE207 (6.8 ng g-1 lw) > BDE208 (3.8 ng g-1 lw) > BDE206
302
(3.7 ng g-1 lw) > BDE99 (< 2.3 ng g-1 lw) > BDE47 (1.6 ng g-1 lw).
303
The TBC of BDE28/33 in wolves was significantly greater than that in caribou (< MDL,
304
2 tailed t test, p < 0.05) (Figure 1B, Table S7). BDE153 and BDE154 were the only other
305
significant differences among TBCs in wolves (0.81 and 0.82 ng g-1 lw respectively) versus
306
caribou (< 0.16 and 0.16 ng g-1 lw; p < 0.05), though there are other differences in HFR
307
concentrations that seem visually disparate, but were not significant. Metabolic formation of the
308
significantly different congeners in addition to biomagnification may be a factor in these
309
differences. BDE28 and -154 have been identified as debromination products of higher
310
brominated PBDEs in carp (Cyprinus carpo, ).55 Though BDE153 has been hypothesized to be
311
part of the debromination pathway to BDE47, stable formation to this congener has not been
312
catalogued to our knowledge.56, 57 Other top predators with high metabolic capacities such as
313
polar bears (Ursus maritimus),58 cetaceans and pinnipeds,18, 59-62 and raptorial birds63 have been
314
shown or hypothesized to metabolize PBDEs, though the specific capacity varies considerably
315
by species and congener.
316
In tissue-specific comparisons, the Σtri-heptaBDE concentrations were significantly
317
smaller in muscle of caribou (2.7 ng g-1 lw) than in their liver and in both tissues of wolves,
318
which were not significantly different from each other (caribou liver = 11 ng g-1 lw, wolf muscle
319
= 30 ng g-1 lw, wolf liver = 14 ng g-1 lw) (KW ANOVA with Dunn’s tests). The ∑PBDE (tri16
ACS Paragon Plus Environment
Page 16 of 40
Page 17 of 40
Environmental Science & Technology
320
nonaBDEs) was greater in tissues of wolves (72–83 ng g-1 lw) than those of caribou (23–36 ng g-
321
1
322
differences in the order of TBCs in tissues of wolves: muscle = BDE207 > BDE206 > BDE28/33
323
> BDE47 > BDE99; liver = BDE207 > BDE206 > BDE208 > BDE28/33 > BDE154. The pattern
324
in liver in particular is again indicative of biotransformation of PBDEs, as nonaBDEs, BDE28/33
325
and BDE154 have been identified as metabolic debromination products in fish and wildlife.55, 57,
326
63, 64
327
lw), however the results were not statistically significant (Table S7). There were distinctive
Concentrations of most PBDE congeners were not statistically different between tissues
328
of mammals, though concentrations did tend to be highest in liver of caribou and muscle of
329
wolves (Table S7). Greater concentrations of HFRs in muscle over liver in wolves are likely
330
related to depletion of metabolically active HFRs58, 63 in the liver. Metabolism during
331
fermentation via gut microorganisms is theoretically possible in ruminants, however this was
332
found to be insignificant in dairy cows, while reductive debromination in liver was hypothesized
333
to be the most important pathway producing higher brominated PBDE congeners.65 Species and
334
congener-specific differences in hepatic biotransformation and depuration of organic
335
contaminants are the most reasonable explanations for the differences between the tissues of
336
wolves and caribou, as was observed for PCBs.31
337
Mammalian ΣPBDE profiles had greater proportions of the highly brominated PBDEs
338
than vegetation (Figure 2). The comparison is complicated as BDE 209 is not reported, however
339
the consistent detections of nonaBDEs is suggestive that BDE209 is present in mammals. Both
340
mammals had ΣPBDE congener profiles dominated by the nonaBDEs (TBC proportions ≈ 53 %
341
and 66 % in wolves and caribou respectively) (Figure 2). Caribou had greater contributions from
342
the pentaBDEs (≈16 %) than did wolves (≈ 8.5 %), while wolves had greater proportions of the 17
ACS Paragon Plus Environment
Environmental Science & Technology
343
hexaBDEs (5.5 % and 1.8 % in wolves and caribou respectively). In grizzly bears (Ursus arctos
344
horribilis) from Western Canada, the highest concentrations of PBDEs were BDE209 > BDE206
345
> BDE47 > BDE207 > BDE208 when the bears shifted to diets that had significant amounts of
346
vegetation (grizzlies are omnivorous).66 Conversely the same bears had greater proportions of
347
lower brominated PBDEs during salmon-feeding periods of their seasonal cycle, which
348
suggested that eating vegetation increased their exposure to nonaBDEs.66 Measurable amounts of
349
nonaBDEs in herbivorous caribou may be supportive of these previous results,66 however this
350
hypothesis requires further validation. Unfortunately, the concentrations of most octa- to
351
nonaBDEs were < MDL in vegetation, and thus the degree of debromination55, 57, 63, 64, 67, 68
352
versus direct uptake and absorption (air inhalation or diet) is impossible to ascertain. Changing
353
melt conditions and growing seasons in arctic terrestrial environments can alter exposure regimes
354
of vegetation and ultimately of consumers, a factor which will be increasingly important in
355
future assessments.43
356
The concentrations of PBDEs in terrestrial consumers presented here were comparable to
357
previous studies (Table S8). Concentrations of PBDEs in moose from two southern NWT herds
358
were generally in a similar range as those for caribou,24 as were PBDEs in Norwegian moose.21
359
However rodents in Belgium had concentrations of BDE153 and BDE183 that were
360
approximately 5-fold greater than those in caribou (Table S8).22 Concentrations of most PBDE
361
congeners in common between studies were greater in the Bathurst wolves than in Belgian
362
foxes.22, 23
363
TBP-AE and PBBz were the most frequently detected and abundant alternative HFRs in
364
the mammals, as they were in vegetation (Table S5). TBP-AE was highest in muscle of wolves
365
(4.0 ng g-1 lw), however significant differences were only detected between liver of caribou over 18
ACS Paragon Plus Environment
Page 18 of 40
Page 19 of 40
Environmental Science & Technology
366
those in the liver of wolves (3.3 and 0.99 ng g-1 lw respectively; Figure S3). BTBPE was
367
detected solely in the muscle of wolves (2.4 ng g-1 lw), negating tests for correlations in caribou.
368
Unlike vegetation, TBP-AE and BTBPE were not correlated within or between tissues of wolves
369
or in TBCs (r2 = 0.0072–0.40, p = 0.13–0.86, n = 7). Terrestrial results for comparison are rare,
370
however TBP-AE was also detected in liver of moose from southern NWT (