Ecotoxicology (2009) 18:802–813 DOI 10.1007/s10646-009-0323-4
Polybrominated diphenyl ether flame retardants in eggs may reduce reproductive success of ospreys in Oregon and Washington, USA Charles J. Henny Æ James L. Kaiser Æ Robert A. Grove Æ Branden L. Johnson Æ Robert J. Letcher
Accepted: 8 May 2009 / Published online: 10 June 2009 Ó US Government 2009
Abstract Spatial and temporal assessments and reports of polybrominated diphenyl ether (PBDE) flame retardants in birds remain sparse. In the present study, PBDEs were detected in all 120 osprey (Pandion haliaetus) eggs collected. The eggs were collected from nests along the Columbia, Willamette and Yakima rivers of Oregon (OR) and Washington (WA) and in Puget Sound (WA) between 2002 and 2007. PBDE congeners: 17, 28, 47, 49, 66, 85, 99, 100, 138, 153, 154 (possible coelution with brominated biphenyl 153 [BB153]), 183, 190 (detected in one egg), 209 (not detected), and BB101 (only detected in 2006 and 2007) and total-a-hexabromocyclododecane (only detected in five eggs) were analyzed for in the egg samples. Eggs from reservoirs in the forested headwaters of the Willamette River (2002) contained the lowest concentrations of RPBDEs (geometric mean [range], 98 [55.2–275] ng/g wet weight [ww]), while those from the middle Willamette River (2006) contained the highest (897 [507–1,880] ng/g ww). Concentrations in eggs from the Columbia River progressively increased downstream from Umatilla, OR (River Mile [RM] 286) to Skamokoa, WA (RM 29), which indicated additive PBDE sources along the river. In general, regardless of the year of egg collection, differences in PBDE concentrations reported in osprey eggs along the three major rivers studied (Columbia, Willamette and Yakima) seem to reflect differences in river flow (dilution effect) and the extent of human C. J. Henny (&) J. L. Kaiser R. A. Grove B. L. Johnson US Geological Survey, Forest and Rangeland Ecosystem Science Center, 3200 SW Jefferson Way, Corvallis, OR 97331, USA e-mail:
[email protected] R. J. Letcher National Wildlife Research Centre, Environment Canada, Carleton University, Ottawa, ON K1A 0H3, Canada
123
population and industry (source inputs) along the rivers. PBDE concentrations increased over time at two locations (Seattle, WA; Columbia River, RM 29-84) where temporal patterns could be evaluated. Only during 2006 (on the middle Willamette River, RM 61–157) and 2007 (on the lower Columbia River, RM 29–84) did RPBDE concentrations in osprey eggs exceed 1,000 ng/g ww with negative relationships indicated at both locations between productivity and RPBDE concentrations in eggs (P = 0.008, P = 0.057). Osprey eggs from Everett, WA contained nearly twice the RPBDE concentration (geometric mean 239 vs. 141 ng/g ww, range 124–384 vs. 22.2–819 ng/g ww, P B 0.05) as double-crested cormorant (Phalacrocorax auritus) eggs collected at the same location and time, which is likely due to dietary differences. No significant relationship (all Ps [ 0.147) was indicated between PBDE congeners (including RPBDEs) and eggshell thickness at the concentrations observed in this study. Keywords Osprey Polybrominated diphenyl ethers Washington Oregon Productivity Double-crested cormorant
Introduction Polybrominated diphenyl ether (PBDE) and hexabromocyclododecane (HBCD) are widely used as flame retardants in thermoplastics, textiles, polyurethane foams and electronic circuitry. PBDEs persist in the environment and lower-brominated PBDEs bioaccumulate and biomagnify up the food web to the top predatory fish, mammal and bird species in many ecosystems (de Wit 2002). In contrast to the organochlorines (including DDE and other pesticides, and polychlorinated biphenyls [PCBs]) which have decreased in
PBDE flame retardants in eggs
the Pacific Northwest (Henny et al. 2008, 2009), PBDEs have increased in biota since the 1970s (de Wit 2002; Law et al. 2006). PBDE residues have been reported in muscle tissue of ospreys (Pandion haliaetus) from Sweden (Jansson et al. 1993) and in osprey eggs from Norway during 1993–2000 (Herzke et al. 2005), from Delaware, Maryland and Virginia in 2000 and 2001 (Rattner et al. 2004, Toschik et al. 2005), and from British Columbia during 1991–2000 (Elliott et al. 2005). A number of PBDE congeners have been reported in eggs of peregrine falcons (Falco peregrinus) from Sweden (Lindberg et al. 2004; Johansson et al. 2009) and the northeastern United States (Chen et al. 2008). Eggs collected from several owl species in northern Europe and China also contained PBDEs (Jaspers et al. 2005; Bustness et al. 2007; Chen et al. 2007). Further, hydroxylated (OH) PBDEs, which may be metabolites resulting from PBDE exposure, were recently reported in blood samples of bald eagle (Haliaeetus leucocephalus) nestlings from British Columbia and California (McKinney et al. 2006). RPBDE concentrations in mountain whitefish (Prosopium williamsoni) from the Columbia River increased 12-fold between 1992 and 2000, with a doubling period of 1.6 years (Rayne et al. 2003). RPBDEs in two osprey eggs collected on the Columbia River near Castlegar, British Columbia in 1997 increased 15-fold over concentrations reported for two eggs collected from the area in 1991; all congeners analyzed increased in concentration, prompting concerns over possible toxicological effects if PBDEs continued to increase (Elliott et al. 2005). Research in laboratory mammals suggests that PBDEs and their metabolites are embryotoxic, hepatotoxic, neurotoxic, and impair the thyroid hormone system (Darnerud et al. 2001; Darnerud 2003). OH-PBDEs, including analogues of major PBDE congeners, including 2,20 ,4,40 ,tetrabromodiphenyl ether (BDE47), have been found to mimic the thyroid hormones thyroxine (T4) and thyronine (T3). For example, Uca´n-Marı´n et al. (2009) reported that environmentally relevant concentrations of BDE47, 6-OHBDE47 and 6-OH-BDE49 were very effective competitors of T3 and T4 for binding to a major thyroid hormone transport protein, transthyretin (TTR) from the Norwegian Arctic glaucous gull (Larus hyperboreus), which was found to be genetically identical to the herring gull (Larus argentatus) from the Laurentian Great Lakes of North America. Currently, there are few PBDE effects studies available. Laboratory studies with captive American kestrels (Falco sparverius) exposed to a PBDE technical mixture have reported decreased pipping and hatching success (McKernan et al. 2009) and reduced reproductive success (Fernie et al. 2009). Van den Steen et al. (2009) and Johansson et al. (2009) also suggested PBDEs may have
803
negative effects on reproductive performance based on their studies with captive European starlings (Sturnus vulgaris) and wild peregrine falcons. Ospreys are a good indicator species for monitoring persistent contaminants in large rivers, estuaries, lakes, and reservoirs. In fact, the species has been proposed as a worldwide sentinel species for toxic contaminants that bioaccumulate and biomagnify up the food web (Grove et al. 2009). Several useful life history traits include: a diet comprised almost exclusively of fish captured relatively close to the nest site, nests that are relatively easy to locate and study, tolerance of short-term nest disturbance and human activity, sensitivity to many contaminants, nests that are often in urban and industrialized areas where contaminants are expected to be more prevalent, and nests that are spatially distributed at regular intervals instead of clumped in colonies. Although migratory at many locations, osprey egg concentrations have been reported to reflect contaminants on the breeding grounds rather than the wintering grounds (Elliott et al. 2007). Thus, PBDE concentrations in eggs are expected to reflect local conditions in the aquatic food web. Many of the osprey eggs evaluated for PBDEs in the current study were also evaluated for organochlorine pesticides, polychlorinated biphenyls, dioxins, furans, and mercury (and often incorporated additional sampling years at each location, i.e., longer time series of data) with results previously reported (Henny et al. 2008, 2009). The objectives of this study were to: (1) determine PBDE and total-a-HBCD concentrations in osprey eggs (one egg per nest) at nine locations in Oregon (OR) and Washington (WA) between 2002 and 2007 and compare congener profiles among locations, (2) compare temporal trends in PBDE concentrations in osprey eggs at two locations (Seattle and RM 29–84 of the Columbia River) and evaluate spatial patterns in PBDE concentrations at two locations (Willamette and Columbia rivers), (3) evaluate reproductive success at each nest with a sample egg collected to determine if an association exists with PBDE residue concentrations from that nest, (4) determine if eggshell thickness is related to PBDE concentrations, and (5) compare PBDE concentrations between osprey and double-crested cormorants (Phalacrocorax auritus) at Everett, WA where both species nested in the same estuary.
Materials and methods Study area locations included Seattle, WA; Everett, WA; Yakima River, WA; lower Columbia River, WA/OR (four segments between River Mile [RM] 29 and 286); Headwater Reservoirs Willamette River, OR (Cottage Grove, Dorena, and Hills Creek); and middle Willamette River,
123
804
Fig. 1 The Pacific Northwest Study area: (A) Everett Harbor and Estuary, (B) Seattle including Duwamish Waterway, Elliott Bay and Lake Washington, (C) Yakima River (RM 83–111), (D) lower Columbia River (RM 29–84), (E) lower Columbia River (RM 85– 122), (F) lower Columbia River (RM 124–143), (G) lower Columbia River (RM 146–286), (H) Willamette Headwater Reservoirs = Cottage Grove, Dorena, Hills Creek, and (I) middle Willamette River (RM 61–157). Shaded areas represent urban areas
OR (between RM 61 and 157; Fig. 1). The Columbia River and Willamette River were divided into reaches based upon several characteristics including industrial boundaries, known point sources of pollution, dams, and the distribution of nesting osprey populations (Henny et al. 2008, 2009). We located occupied osprey nests by boat, car and aircraft. Nests were visited at least two to four times, but often at weekly intervals to determine nesting activity and reproductive success following definitions of Postupalsky (1977). One partially incubated egg (usually about 10 days into incubation) was randomly collected from each nest (usually 3-eggs laid per clutch) to determine exposure to contaminants. We also collected a sample egg from 12 double-crested cormorant nests at Everett, WA in 2002 for similar analyses to compare residues between the two species. In the current study we evaluate reproductive success at individual osprey nests by comparing residue concentrations in a sample egg collected from each nest to the number of advanced-age young (40–45 days) produced from the remaining eggs in the nest, i.e., the sample egg technique (Blus 1984). Egg volume was determined by water displacement. Egg contents were placed in chemically clean jars and frozen for subsequent contaminant analysis. Eggs were shipped to the National Wildlife Research Centre, Science and Technology Branch, Environment Canada, Carleton University, Ottawa, Ontario for analysis
123
C. J. Henny et al.
by the Letcher Organics Research Lab. As described elsewhere (Gauthier et al. 2007, 2008), sample eggs were analyzed for BDE congeners: 17, 28, 47, 49, 66, 85, 99, 100, 138, 153, 154, 183, 190, 209 and total-a-HBCD, and brominated biphenyls (BB) 101 and 153 (coeluted with BDE154; eggs collected from Everett in 2003 [N = 4] and from Seattle in 2003 [N = 11] were not analyzed for BDE 17, 49, 65, 85, and HBCD). Brominated compounds were determined with gas chromatograph–mass spectrometer (GC–MS; Electron Capture Negative Ionization [ECNI]). An Agilent GC 6890 equipped with a 5973 quadrupole MS detector was used. Brominated compounds were identified on the basis of their retention times on the DB-5 columns, relative to authentic standards, i.e., total-a-HBCD, BB-101, and PBDEs (14 congeners). The a-HBCD is total-a-HBCD as b- and c-HBCD thermally isomerize to a-HBCD at GC temperatures [ 160°C. Quantification was performed using an internal standard method based on the relative ECNI response factor (RRF) of the 79Br?81Br anions of BDE-71 and of authentic congener standards. Mean recovery (±1 standard error) of the internal standard was on average 63 ± 16% for BDE-71. Concentrations were recovery-corrected as an internal standard method of quantification was used to reduce heterogeneity within and between analyte classes. Method blank samples were analyzed with each batch of five samples. The method limit of quantification was generally about 0.005 ng/g wet weight (ww). Residue concentrations in eggs were corrected to an approximate fresh wet weight using egg volumes (Stickel et al. 1973). We report on these persistent and bioaccumulative PBDEs in 120 osprey eggs randomly collected (one per nest) at nine regional locations in Oregon and Washington between 2002 and 2007. Residue data for eggs collected from Seattle in 2006 (N = 7) and 2007 (N = 4) were combined because of the low sample size. At two of the study locations, temporal residue trends were available for comparison and spatial patterns were examined at two river systems. Reproductive success at each nest with a sample egg collected was evaluated on a nest-by-nest basis to determine if production was associated with PBDE concentrations. One additional comparison was made between osprey and double-crested cormorant eggs at Everett, WA in 2002 where the two species nested in the same estuary. Residue concentrations were summarized as geometric means and log-transformed for statistical analyses. For statistical purposes, a value of half the lower quantification limit was used for eggs in which a contaminant was not detected. This value was used to calculate geometric means when C50% of the eggs contained detectable residues. When \50% of eggs from a site contained the contaminant, no statistical test was conducted with data from that site. Because of unequal sample sizes, the General Linear Models
PBDE flame retardants in eggs
Procedure (SAS Institute, Cary, NC, 2003) was used for analysis of variance. Tukey’s Studentized Range Test (a = 0.05) was used to separate means. We used the nonparametric Jonckheere-Terpstra (JT) Test with a one-sided test, because a priori we wanted to test for a negative association in productivity vs. RPBDE concentrations in the sample egg from each nest (Hollander and Wolfe 1973). The null hypothesis of the JT states that the distribution of the response variable does not differ among classes (Ho: s1 = s2 = s3 = sn, where s is productivity of the class). The alternative hypothesis is that there is an increasing or decreasing trend (not necessarily linear) (HA: s1 C s2 C s3 C sn, or s1 B s2 B s3 B sn, where at least one of the inequalities is a strict inequality). Unless otherwise noted, differences were considered significant when P B 0.05. Eggshell thickness was measured after eggshells dried for at least 3 months at room temperature. Three locations on the equator of the eggshell were measured with a Starrett Model 1010M micrometer, with the mean used as the thickness. Our large dataset (N = 120) provided an opportunity to evaluate the relationship between seven PBDE congeners (with a minimum of 75% of the eggs with quantifiable congener concentrations) plus RPBDEs and eggshell thickness using regression analyses (SAS 2003). We tested for an effect of PBDEs (log values) on osprey eggshell thickness with models that controlled (by adding DDE as a factor in the model) and did not control for DDEassociated thinning. Columbia River eggs in 2007 were not analyzed for DDE because residues by 2004 and 2006 in osprey eggs were at very low concentrations and not affecting reproduction (Henny et al. 2008). Additionally, we tested for differences in eggshell thickness among PBDE categories using ANOVA (SAS 2003).
Results and discussion Spatial trends and congener patterns All eggs collected during this study contained quantifiable PBDE concentrations. Findings for the 89 osprey eggs collected between 2002 and 2006 (excluding eggs collected at sites more than 1 year, e.g., Seattle in 2006/2007 and Columbia River RM 29–84 in 2007) indicate that the middle Willamette River eggs contained the highest geometric mean RPBDE concentrations and usually had the highest individual congener concentrations (Table 1). Eggs collected from the forested and sparsely populated headwater reservoirs of the Willamette River contained the lowest concentrations. RPBDE concentrations in osprey eggs collected from the Columbia River in 2004 increased in a downstream pattern with a geometric mean (range) RPBDE of 157 (80.5–340) ng/g ww from the upper reach
805
(RM 146–286, above Bonneville Dam) and 403 (48.7–954) ng/g ww from the lowest reach (RM 29–84; P B 0.05). BDE47 was the dominant congener measured in osprey eggs followed by BDE100, 99, 154/BB153, 153, and 28. Geometric means for the other BDE congeners (85, 138, 183, 49, 17, 66) were all below 1 ng/g, except for BDE17 in the series of eggs from the middle Willamette River. BDE190 was detected in one egg from the lower Columbia River in 2007 and BDE209 was not detected in any eggs. For the only BB congener detected (BB101), it was only measured in eggs collected in 2006 and 2007 (all 11 eggs from Seattle, 1 egg from the middle Willamette River, and all 20 eggs from the lower Columbia River). Temporal trends Temporal trends in PBDE concentrations were evaluated for 22 osprey eggs collected from the Seattle area in 2003 and 2006/2007. Two congeners (BDE28 and BDE100) increased (0.28 vs. 4.30 [0.11–0.79 vs. 0.46–71.2] ng/g ww and 23.6 vs. 46.2 [12.7–38.4 vs. 25.5–141] ng/g ww) over time (P \ 0.0001 and P = 0.004), but geometric mean RPBDEs did not increase significantly (203 vs. 299 [83.6– 439 vs. 138–683] ng/g ww; P = 0.184; Table 2). The lower reach of the Columbia River (RM 24–89), where osprey eggs contained the highest concentrations along the river in 2004, was selected in 2007 for an additional collection of eggs to determine if PBDE concentrations changed over time (Table 3). Though geometric mean BDE100 again increased (65.4 vs. 119 [7.73–174 vs. 28.0– 352] ng/g ww; P = 0.031) during the 3-year interval, none of the other congener or RPBDE concentrations (403 vs. 569 [48.7–954 vs. 155–1,320] ng/g ww; P = 0.169) had significant increases, although trends were toward higher levels in the latter time period. Though the specific reason why only BDE100 was observed to increase in eggs from both locations remains unknown, it likely results from the composition of the commercial products most widely used, metabolism within various levels of the food chain, and/or environmental transformation/degradation of PBDEs. Reproductive success and contaminant concentrations Darnerud (2003) in his review of toxic effects of brominated flame retardants concluded that there are several important data gaps that must be filled before a detailed risk assessment can be performed. One of these data gaps is reproduction toxicity studies. In the current study, we examined the relation between concentrations of PBDEs as well as other contaminants (relative to their known toxicity) in sample eggs and reproductive success at each nest of wild ospreys in Oregon and Washington. Egg-PBDE concentrations were divided into five categories each in
123
123
26.8 ABCD (7.07–55.3)
73.9 A (34.1–178)
14.4 CD (1.39–42.1)
11.7 D (4.40–43.7)
14.0 CD (4.87–53.1)
12.8 D (5.40–25.0)
18.4 BCD (8.01–35.3)
52.1 AB (11.2–498)
Yakima R. (RM 82–111)
Columbia R. (RM 29–84)
Columbia R. (RM 85–122)
Columbia R. (RM 124–143)
Columbia R. (RM 146–286)
Willamette Reservoirs
Willamette R. (RM 61–157)
3.8
3.4
3.4
3.5
3.4
2.9
3.8
133 A (53.4–396)
12.2 D (8.08–32.9)
23.1 CD (12.6–53.3)
33.2 BC (18.7–102)
43.1 BC (12.7–100)
65.4 AB (7.73–174)
42.0 BC (23.1–56.2)
23.6 CD (12.7–38.4)
37.5 BC (18.9–60.2)
100
10
7
9
9
11
11
5
4.6
3.9
16c 11
% lipid
N
NC[2] (ND–3.16)
ND
ND
ND
ND
ND
ND
0.03 (ND–0.21)
NC[1] (ND–0.13)
138
14.2 A (4.85–38.5)
2.29 A (1.47–7.70)
4.92 A (2.36–9.65)
2.80 A (0.67–10.4)
NC[5] (ND–6.56)
2.59 A (ND–14.7)
6.72 A (3.97–9.50)
0.28 B (0.11–0.79)
2.78 A (0.22–10.7)
28
32.4 A (10.3–85.7)
4.80 D (2.85–13.8)
5.58 CD (3.06–13.7)
8.31 BCD (5.03–27.3)
13.4 ABCD (3.32–46.5)
21.7 AB (1.90–63.7)
13.7 ABC (7.59–24.1)
10.6 BCD (2.04–34.4)
10.1 BCD (3.88–18.9)
153
6.76 A (1.94–17.1)
0.24 B (0.11–0.86)
0.34 B (0.07–0.92)
0.33 B (0.13–3.49)
NC[4] (ND–2.19)
NC[4] (ND–0.35)
0.36 B (0.22–1.08)
NA
0.25c B (0.05–0.40)
17
PBDE congener
31.7 A (12.2–90.3)
4.21 D (3.17–11.0)
5.31 CD (2.43–14.3)
8.33 BCD (4.64–21.4)
11.1 BCD (2.71–30.5)
14.5 ABC (1.28–39.2)
11.6 ABCD (5.25–19.3)
14.7 AB (3.83–45.2)
10.5 BCD (5.57–21.7)
154/BB153
562 A (265–1020)
54 E (30.1–174)
102 DE (53.4–231)
141 BCD (80.5–385)
203 BCD (59.8–592)
278 AB (32.8–619)
239 BC (139–303)
124 CD (57.6–265)
133 BCD (79.3–225)
47
ND
NC[2] (ND–0.19)
ND
NC[2] (ND–0.32)
ND
NC[1] (ND–0.30)
ND
0.13 A (ND–0.46)
0.06 A (ND–0.18)
183
NC[4] (ND–3.80)
ND
ND
ND
ND
ND
ND
NA
NC[5]c (ND–2.68)
49
887 A (503–1,850)
97.3 D (54.4–274)
156 CD (80.5–340)
211 BCD (119–581)
285 BC (84.4–820)
402 AB (48.3–947)
392 B (216–580)
203 BCD (83.6–439)
239 BC (124–384)
RPBDE
d
0.22 A (ND–9.64)
NC[1] (ND–0.26)
NC[1] (ND–1.02)
NC[1] (ND–2.07)
ND
ND
0.06 A (ND–1.21)
NA
0.04c A (ND–1.93)
66
897 A (507–1,880)
97.7 D (55.2–275)
157 CD (80.5–340)
213 BCD (119–601)
285 BC (84.4–820)
403 AB (48.7–954)
397 B (221–583)
203 BCD (83.5–439)
242 BC (124–384)
RPBDEe
0.14 A (ND–3.97)
ND
ND
NC[2] (ND–1.45)
NC[1] (ND–0.76)
NC[1] (ND–0.74)
ND
NA
0.07c A (ND–0.97)
85
Eggs sampled from Seattle in 2006/2007 (N = 11) and Columbia River (RM 29–84) in 2007 (N = 20) are not included in table, see Tables 2 and 3
RPBDE = sum of congeners: 28, 47, 99, 100, 138, 153, 154/BB153, 183 to account for congeners not analyzed in 2003 (Seattle and Everett)
RPBDE = sum of all analyzed PBDE congeners: 17, 28, 47, 49, 66, 85, 99, 100, 138, 153, 154/BB153, and 183
e
Eggs in 2003 from Everett not analyzed for congeners 17, 49, 66, 85 and HBCD; N = 12 for mean calculations and statistical test
d
c
b
Everett Harbor and Estuary, WA; Seattle, WA = Duwamish Waterway, Lake Washington and Elliott Bay; Yakima River, WA; lower Columbia River, OR and WA; Willamette Headwater Reservoirs = Cottage Grove, Dorena, Hills Creek, OR; middle Willamette River, OR
a
Note: Congeners 190, 209 were not detected in any samples, BB101 was only detected in one sample from the middle Willamette in 2006. HBCD was only detected in five eggs: Everett (2002), 4.96 and 11.4; Yakima R. (2002), 5.18 and 8.87; and Columbia R. (RM 146-286) (2004), 7.36. MC map code (see Fig. 1), NA not analyzed, ND not detected, NC mean not calculated (\50% above detection limit), number of samples with detectable residues shown in []. Percent lipid is arithmetic mean. Columns sharing the same letter are not significantly different, Tukey’s Studentized Range Test (a = 0.05)
40.2 ABC (15.9–77.7)
Seattle
2006
2002
2004
2004
2004
2004
2002
2003
2002/03
Year
Everett
99
PBDE congener
I
Willamette R. (RM 61–157)
Location
H
Willamette Reservoirs
a,b
G
Columbia R. (RM 146–286)
D
Columbia R. (RM 29–84)
E
C
Yakima R. (RM 82–111)
F
B
Seattle
Columbia R. (RM 124–143)
A
Everett
Columbia R. (RM 85–122)
MC
Locationa,b
Table 1 Geometric means and ranges (in parentheses) of polybrominated diphenyl ether (PBDE) and hexabromocyclododecane (HBCD) concentrations (ng/g wet weight) in osprey eggs collected from rivers, reservoirs, and estuaries in the Pacific Northwest 2002–2006
806 C. J. Henny et al.
PBDE flame retardants in eggs
807
Table 2 Geometric means of polybrominated diphenyl ether (PBDE), brominated biphenyl 101, and hexabromocyclododecane (HBCD) concentrations and (ranges in parentheses) (ng/g wet weight) in osprey eggs collected from Seattle, WA (Duwamish Waterway, Lake Washington and Elliott Bay), 2003 versus 2006/2007
Table 3 Geometric means of polybrominated diphenyl ether (PBDE), brominated biphenyl 101, and hexabromocyclododecane (HBCD) concentrations (ranges in parentheses; ng/g wet weight) in osprey eggs collected from the lower Columbia River (RM 29–84), OR and WA, 2004 versus 2007
Congener
2003 2006/2007 P values N = 11, 4.6% lipid N = 11, 4.4% lipid
Congener
2004 2007 P values N = 11, 2.9% lipid N = 20, 4.2% lipid
BDE17
ND
1.00 (0.01–15.3)
BDE17
NC [4] (ND–0.55)
1.71 (0.23–5.30)
BDE28
0.28 (0.11–0.79)
4.30 (0.46–71.2)
