Environ. Sci. Technol. 2010, 44, 3520–3526
Historical Contaminants, Flame Retardants, and Halogenated Phenolic Compounds in Peregrine Falcon (Falco peregrinus) Nestlings in the Canadian Great Lakes Basin K I M J . F E R N I E * ,† A N D R O B E R T J . L E T C H E R * ,‡ Wildlife and Landscape Science Directorate, Science and Technology Branch, Environment Canada, Burlington, Ontario L7R 4A6, Canada, and Wildlife and Landscape Science Directorate, Science and Technology Branch, Environment Canada, National Wildlife Research Centre, Carleton University, Ottawa, Ontario K1A 0H3, Canada
Received October 7, 2009. Revised manuscript received March 8, 2010. Accepted March 29, 2010.
Concentrations and spatial patterns of persistent organic (chlorinated) pollutants (POPs), polybrominated diphenyl ether (PBDE), hexabromocyclododecane (HBCD), other flame retardants, and hydroxylated (OH) PBDE and PCB compounds were determined in nestling peregrine falcons across the Canadian Great Lakes Basin. The highest geometric mean plasma POP concentrations (ng/g ww) were sum (Σ)PCBs (35.16), ΣPBDEs (15.38), and ΣOH-PCB (8.77) with the lowest mean levels in nestlings from urban versus remote nests. PBDE congeners derived from PentaBDE and OctaBDE technical mixtures had the highest concentrations, sometimes exceeding 100 ng/g wet weight (ww); BDE-99, -153, -47, -100, and -183 comprised 92.7% of the Σ14PBDE levels. BDE-209 proportions were minimal ( 5 values and are thus persistent and bioaccumulative (e.g. ref 1). Increasingly, BFRs such as HBCD, PBBs, hexabromobenzene (HBB), and decabromodiphenyl ethane (DBDPE) are detected in birds (8). Despite increasing regulation in North America and Europe, like PCBs, PBDE concentrations still show increasing or nondecreasing temporal trends in biota throughout the world, including in peregrine falcons from China, Greenland, Belgium, and the U.S.A. (9-15). While γ-HBCD dominates the technical HBCD product, the R-HBCD isomer is the dominant isomer detected in humans and biota (1). The interspecies differences in BFR profiles in birds are determined by differences in diet, habitat, location, age, and other factors that determine the bioaccumulation, fate, toxicokinetics (e.g., metabolism), and potential toxicity of BFRs. The dominant PBDE congener profile was BDE-153 > -99 > -100 in peregrine eggs from Sweden (12) versus BDE153 > -99 > -183 in the United States (13, 14). PBDE congeners, HBCD isomers, but less so other BFRs, are metabolized via debromination and oxidative pathways although BFR metabolism is not well understood in birds and especially birds of prey (16). Regardless, PBDEs resulting from debromination e.g., BDE-209, were suggested in the eggs of herring gulls (Larus argentatus) (17) and peregrine falcons (14). Hydroxylated (OH) PCBs and methylsulfonyl-PCBs (MeSO2-PCBs) are metabolites of PCBs (18). OH-PCB metabolites and putative OH-PBDE metabolites were reported in the plasma of adult glaucous gulls (Larus hyperboreus) (19) and bald eaglets (Haliaeetus leucocephalus) (20). Peregrine falcons have an exclusively avian diet, usually terrestrial birds but occasionally aquatic bird species, putting them at the top of the food chain (21). Peregrine falcons declined significantly in the 1960s as a result of exposure to DDT and eggshell thinning but have since recovered globally. Assessments of temporal and spatial PBDEs and current-use BFRs are valuable as such information is minimal for birds of prey, and there have been no reports to date regarding the metabolism of contaminants by peregrine falcons. PBDE concentrations in eggs were negatively correlated with average brood size of individual peregrine females in Sweden (12) and resulted in thinner eggshells (22), reduced reproductive success (22, 23), and altered courtship behaviors (24) of captive American kestrels (Falco sparverius), another Falconidae species. Of the measured contaminants, only ΣPBDE concentrations in the eggs of free-ranging ospreys (Pandion haliaetus) were negatively correlated with reproductive productivity (25). The aim of this study is to quantify plasma concentrations of, and identify spatial patterns in, historical and chlorinated POPs, BFRs, and their degradation products, in nestling peregrines from Canadian nesting sites across the Great Lakes Basin.
Materials and Methods All research was completed with necessary permits and according to Canadian Animal Care Guidelines (26). Blood 10.1021/es100400n
Published 2010 by the American Chemical Society
Published on Web 04/12/2010
FIGURE 1. Nestling peregrine falcons were sampled from 34 active nests across Ontario and western Quebec in 2004 and 2005. The active nests were among the peregrine falcon territories, territorial pairs, and confirmed nesting attempts shown in Figure 1 (41). samples were collected from nestling peregrine falcons without harm at active nests located in one of three geographical regions: the urban region included the large urban centers and surrounding areas of southern Ontario and western Que´bec; the Thunder Bay region involved the small industrial city of Thunder Bay on western Lake Superior and areas immediately west; and the remote North Shore region of Lake Superior (Figure 1). Nestlings were banded, weighed, and blood sampled at 28.0 ( 0.4 days of age from 34 nests in 2004 and 2005. Blood plasma of sibling chicks was pooled for chemical analysis. Chemical Analysis. The analysis and workup of the plasma samples are described elsewhere (8, 17, 20). Briefly, plasma samples were analyzed for various classes and congeners of historical organochlorine contaminants (i.e., PCBs, chlordanes, p,p′-DDT, p,p′-DDE, Mirex, Photomirex, hexachlorobenzene, octachlorostyrene, bis(4-chlorophenol)sulfone (BCPS) and Dieldrin), methylsulfonyl-PCBs (MeSO2-PCBs), 14 major PBDE congeners, BB-101 and total-(R)-hexbromocyclododecane (total-HBCD) flame retardants, and several brominated and chlorinated phenolic compounds, specifically pentachlorophenol (PCP), hydroxylated (OH) PCBs and 14 OH-PBDEs (Table S1), 16 MeO-PBDE congeners, tris(4chlorophenyl)methanol (TCPM), and 4-OH-heptachlorstyrene (4-OH-HpCS). Pooled plasma samples (1.5 g) were spiked with internal standards: six 13C12-labeled PCBs (CB28, -52, -118, -153, -180, and -194), BDE-30 (25 µL of 428 pg/µL), 3-MeSO2-2-CH3-2′,3′,4′,5,5′-pentachlorobiphenyl, four 13 C12-labeled OH-PCBs (4′-OH-CB120, 4′-OH-CB159, 4′-OHCB172, and 4′-OH-CB187), and 2′-OH-BDE28 (25 µL of 211 pg/µL). The recovery efficiency of BDE-30 is representative
of all PBDE congeners and non-PBDE BFRs allowing its use as an internal standard and surrogate for all GC amenable BFRs and other brominated compounds (e.g., MeO-PBDEs) (8, 17). All PBDE congener, BFR standards, and OH-PCBs were purchased from Wellington Laboratories (Guelph, ON, Canada) or Sigma-Aldrich (Mississauga, ON, Canada). MeOPBDE and OH-PBDE congener standards were provided by Dr. Goran Marsh and Dr. Åke Bergman (Stockholm University, Sweden). The Supporting Information provides all details regarding GC-MSD analysis and Quality Control and Assurance procedures. Statistical Analysis. Statistical analysis was completed using SAS. All continuous data were log-transformed, and statistical differences in plasma contaminant concentrations were assessed for geographical differences using ANOVAs and Scheffe´’s S test as a posthoc test or Kruskal-Wallis nonparametric ANOVA tests. Pearson’s or Spearman’s correlation analysis was used to determine associations among contaminants and/or lipids. Statistical significance was p < 0.05 with geometric means presented unless noted.
Results and Discussion Overall Contaminant Patterns. The plasma lipid concentrations of the peregrine chicks were similar across the Great Lakes Basin and were not correlated with any of the measured contaminant concentrations. Rankings of the three major contaminant classes were consistent across all three regions: ΣPCBs then ΣPBDEs and ΣOH-PCBs. Each measured pesticide, including p,p′-DDE, contributed minimally to the overall contaminant burden (e2.8%) (Table 1). In all three regions, the Σhexa-PCB congeners had the highest concentrations of the PCB congeners, followed by Σhepta-PCBs, equal contributions of Σpenta- and Σocta-PCBs, then tetraPCBs, Σnona-PCBs, and tri-PCB congeners, with similar concentrations of ΣOH-PCBs or ΣMeSO2-PCBs. Comparatively, peregrine nestlings in Rankin Inlet had considerably higher plasma ΣPCB concentrations in 1991 and 1994 (27). Contaminants of Historical Interest: PCBs and Chlorinated Hydrocarbons (Pesticides). The plasma ΣPCB concentrations were significantly lower (p ) 0.0009) in the urban nestlings compared to Thunder Bay (p ) 0.0225) or North Shore nestlings (p ) 0.0014) (Table 2). The urban nestlings were fed Columbidae avian species that are low on the food chain and sedentary during the year, whereas the North Shore chicks consumed many avian species that are higher on the food chain and migrate through, or overwinter at Green Bay and Saginaw Bay, which have historically high PCB concentrations. A plasma-to-egg PCB conversion factor (0.905*(log plasma) -1.193) developed for Great Lakes birds
TABLE 1. Ranking by Concentration of All Chemicals Measured in the Plasma of Nestling Peregrines Across the Great Lakes Basina
ΣPCB ΣPBDE ΣOH-PCB PCP p,p′-DDE ΣChlordane ΣOH-PBDE p,p′-DDT Mirex Heptachlor epoxide Photomirex hexachlorobenzene ΣMeSO2-PCB a
geometric mean (ng/g ww)
range (min - max) (ng/g ww)
arithmetic mean ( SEM (ng/g ww)
% of total burden (based on GM)
% of total burden (based on AM)
35.16 15.38 8.77 3.16 2.70 1.37 1.07 1.16 0.77 0.95 0.96 0.13 0.20
3.52 - 368.21 0.87 - 195.79 0.51 - 46.21 0.46 - 24.44 0.08 - 15.43 0.19 - 9.84 0.01 - 12.06 0.26 - 8.59 0.07 - 2.31 0.26 - 3.23 0.30 - 2.86 0.03 - 0.80 0.03 - 36.64
73.28 ( 16.97 37.62 ( 8.81 14.39 ( 1.75 5.76 ( 0.93 4.11 ( 0.75 2.35 ( 0.41 2.33 ( 0.48 1.02 ( 0.22 0.89 ( 0.12 0.77 ( 0.15 0.46 ( 0.15 0.18 ( 0.03 0.11 ( 0.05
48.98 21.42 12.22 4.40 3.77 1.90 1.49 1.62 1.08 1.32 1.33 0.19 0.28
51.60 26.60 9.70 3.90 2.80 1.60 1.60 0.70 0.60 0.50 0.30 0.10 0.10
N ) 34 nests. Concentrations are measured in ng/g ww. GM, geometric means; AM, arithmetic means.
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5.89
3.41
8.31
5.37 7.95 6.95 8.3
8.88 5.56
N.S. N.S. N.S. 2,31 0.0068 N.S. N.S. N.S. N.S.
N.S. 2,31 0.0009 2,31 0.0087 N.S. N.S. N.S. 2,31 0.01 2,30 0.0017 2,31 0.0032 2,29 0.0014 N.S. 2,30 0.0013 N.S. 2,19 0.0534 N.S. N.S. N.S. N.S.
df
AM
SEM
Max.
Min.
GM
AM
0.0069
0.39 0.16 0.13 0.11 0.06 0.04 0.04 0.02
0.41 0.17 0.14 0.11 0.09 0.05 0.01 0
0.02 0.01 0.01 0.01 0.02 0 0 0
0.63 0.24 0.26 0.24 0.54 0.1 0.08 0.03
0.16 0 0.06 0 0 0 0 0
0.39 0.20 0.14 0.12 0.06 0.04 0.05 0
0.42 0.17 0.17 0.11 ab 0.03 0.05 0.02 0
0.56 0.57 0.01 0.72 0.39 0.53 0.54 e0.0225 35.16 73.28 16.97 368.21 3.52 85.31 153.02 0.0099 15.38 37.62 8.81 195.79 0.87 51.17 57.03 a 14.13 92.73 0.54 98.21 86.29 46.56 91.76 10.94 72.08 1.82 82.63 39.93 39.22 76.76 0.40 4.31 1.81 62.15 0.92 0.41 2.68 e0.0505 6.12 16 3.79 82.25 0.38 21.35 24.80 a 0.0018 2.56 6.53 1.68 39.79 0 8.66 9.52 a e0.0220 2.02 5.67 1.36 30.51 0.12 8.32 10.33 a 0.0015 1.61 3.79 0.94 20.84 0 5.69 5.38 a 0.90 1.94 0.44 9.71 0 1.34 1.64 e0.0432 0.08 1.65 0.41 9.8 0 2.50 2.95 a 1.82 1.32 0.67 16.41 0 1.39 1.18 N.S. 0.29 0.3 0.08 2.12 0 0.39 0.44 0.48 0.27 0.1 2.24 0 1.13 0.17 0.35 0.12 0.04 0.88 0 0.38 0 0.39 0.02 0.02 0.46 0 0 0 0.03 0.002 0.002 0.06 0 0 0
GM
Max.
Min.
GM
AM
SEM
Max.
Thunder Bay Region (N ) 13 nests) Min.
GM
AM
0.02 0.01 0.02 0.02 0.01 0.01 0.01 0
0.54 0.24 0.23 0.18 0.08 0.08 0.07 0
0.31 0.11 0.07 0 0.01 0.03 0 0
0.37 0.14 0.10 0.11 0.06 0.04 0.03 0
0.38 0.18 0.12 0.14 a 0.1 0.05 0.01 0
0.03 0.02 0.02 0.01 0.04 0.01 0.01 0
0.54 0.24 0.26 0.24 0.45 0.1 0.08 0
0.17 0 0.06 0.08 0 0.02 0 0
0.43 0.15 0.15 0.10 0.06 0.04 0.03 0.02
0.45 0.14 0.14 0.08 b 0.11 0.04 0 0
0.04 0.01 0.01 0.01 0.04 0.01 0 0
0.63 0.2 0.23 0.13 0.54 0.07 0.03 0.03
0.16 0.01 0.07 0 0 0 0 0
0.72 0.47 28.94 5.29 29.39 0.87 98.21 87.79 82.63 39.93 62.15 0.97 16.16 0.38 3.35 0.14 4.33 0.16 2.34 0 9 0 1.22 0 0.66 0 0.28 0 1.7 0 0.88 0 0.46 0 0 0
SEM Max. Min.
Urban Region (N ) 12 nests)
0.03 0.65 0.39 0.57 0.57 0.02 0.68 0.45 0.58 0.58 0.02 41.32 368.21 27.36 62.35 101.64 34.12 357.33 3.52 13.67 17.54 1.92 9.71 111.63 27.77 12.95 47.52 ab 20.73 195.79 1.47 7.52 12.33 b 2.66 1.07 95.89 86.29 12.01 93.18 0.97 98.13 86.85 6.89 92.96 0.84 1.53 82.28 70.66 8.69 67.97 2.94 81.13 42.81 5.39 73.03 3.68 0.4 5.04 1.42 0.55 1.89 0.17 2.89 0.92 0.28 7.94 4.94 5.02 54.8 11.88 4.68 19.41 b 8.71 82.25 0.51 3.21 5.70 b 1.56 1.5 18.71 4.63 2.90 9.07 ab 4.03 39.79 0 0.90 1.54 b 0.33 2.25 21.02 2.33 1.48 6.29 b 2.87 30.51 0.12 0.98 1.49 b 0.35 0.97 10.08 0 1.76 5.44 ab 2.21 20.84 0.22 0.58 0.81 b 0.2 0.39 3.74 0.51 0.85 2.47 0.93 9.71 0 0.68 1.59 0.73 0.65 7.15 1.19 0.60 1.91 b 0.87 9.8 0.04 0.26 0.39 b 0.11 0.58 5.05 0 6.10 2.56 1.68 16.41 0 0.58 0.1 0.07 0.12 1.13 0 0.51 0.35 0.19 2.12 0 0.17 0.14 0.03 0.07 0.53 0 0.19 0 0 0 0 0.34 0.29 0.14 0 0 0 0 0 0 0 0 0.33 0.22 0.09 0 0 0 0 0.01 0 0.06 0 0.39 0.07 0.05 0 0 0 0.03 0.001 0 0.005 0 0 0 0
SEM
Lake Superior North Shore (N ) 9 nests)
a Raw means are presented although statistical results are based on least square means calculated using Scheffe´’s post-hoc tests. df, degrees of freedom; GM, geometric means; AM, arithmetic means; Σ3PBDEs: BDE-99, -153, -47 and Σ5PBDEs plus BDE-100, BDE-154/BB-153.
%Lipids ΣPCBs Σ14PBDEs Σ5PBDEs Σ3PBDEs BDE-99:-153 BDE-99 BDE-153 BDE-47 BDE-100 BDE-183 BDE-154/BB-153 BDE-209 BDE-138 BDE-85 BDE-190 HBCD BB-101 Proportion of Σ14PBDEs BDE-99 BDE-153 BDE-47 BDE-100 BDE-183 BDE-154/BB-153 BDE-209 HBCD
F-value
Scheffe´’s overall Posthoc p-value p-values
overall concentrations (N ) 34 nests)
TABLE 2. Regional Concentrations (ng/g ww) of ΣPCB and Brominated Flame Retardants in the Plasma of Peregrine Nestlings Across the Great Lakes Basin in Canadaa
of prey (28) was used to convert the plasma ΣPCB levels to estimated in ovo ΣPCB concentrations (0-4.15 µg PCB/g egg ww) for Great Lakes peregrines. These estimated egg levels are lower than measured levels in post-term, mid-Atlantic peregrine eggs (0.14-57.91 µg/g ww) (7), potentially from the bias of sampling successfully versus unsuccessfully hatched eggs if higher contaminant concentrations reduced hatchability. During the 1960s, elevated concentrations of p,p′-DDE contributed to the extirpation of peregrine falcons in large regions of North America, Europe, and the U.K. Today, North American peregrines are no longer exposed to significant p,p′-DDE residues (13 ng/g ww) when overwintering in South America (29). Similarly, the plasma p,p′-DDE concentrations of the Great Lakes peregrine nestlings (2.70 ng/g ww; Table 1) are also low. Using the p,p′-DDE plasma-to-egg conversion factor for Great Lakes raptors (0.676*(log plasma) -0.578) (28), the estimated p,p′-DDE egg concentrations (2.24 µg/g ww; ND - 9.85 µg/g ww) for Great Lakes peregrines are well below the threshold of 15-20 µg/g ww determined for reproductive effects (ref 27and references therein). Emerging Contaminants: Brominated Flame Retardants. The ΣPBDE plasma concentrations (15.38; 0.87-195.79 ng/g ww) ranked second overall of all measured POPs (Tables 1 and 2); when lipid corrected, all arithmetic mean Σ14PBDE concentrations exceeded 1000 ng/g lw with maximal concentrations of 17,174 ng/g lw in North Shore nestlings and 28,793 ng/g lw in Thunder Bay nestlings. These ΣPBDE levels are much higher than the reported plasma levels of Lake Superior bald eaglets (geometric mean Σ9PBDE: 7.9 ng/g ww, 6.0-10.4 ng/g ww) (1989-2001) (30) that consume a diet lower on the food chain (fish) than peregrines (birds). There is a lack of studies reporting plasma PBDE concentrations in peregrines and no plasma-to-egg PBDE conversion factor exists, but the following concentrations of ΣPBDE were reported in peregrine eggs from South Greenland (Σ12PBDE: 300-12900 ng/g lw) (11), Norway (Σ9PBDE: 77-406 ng/g ww) (31), Sweden (Σ14PBDE: 29-17200 ng/g lw) (12), the northeastern U.S.A. (Σ17PBDE: 74.5-6610 ng/g ww) (13), and California (Σ15PBDE 80-53,100 ng/g lw) (15). The large differences in ΣPBDE concentrations among species and tissues are a function of several factors, regardless of the number of PBDE congeners since concentrations are generally dominated by BDE-47, -99, and -153. Lipid levels are much lower in plasma ( BDE-47 > BDE-153 in the North Shore chicks compared to BDE-99 > BDE-153 > BDE-47 in the nestlings from the other two regions (Table 2). These regional differences may be linked to diet since BDE-47 usually dominates the PBDE congener profile in birds with an aquatic-sourced diet (19, 20) consistent with aquaticbased avian prey remains found at the North Shore nests only. Dietary differences likely also explain the inter-regional differences of the BDE 99:153 concentration ratios and the intraregional differences in BDE-99 levels in the peregrine nestlings. In the Thunder Bay chicks, the geometric (arithmetic) mean BDE-99:BDE-153 concentration ratio was 0.53 (1.9 ( 0.2) compared to 0.41 (2.7 ( 0.4) in North Shore chicks and 0.28 (7.9 ( 4.9) in urban peregrine chicks (Figure S1). Within the North Shore region, the chicks in the northern subregion had much higher BDE-99 concentrations (28.14 ng/g ww) than those in the NW (18.39 ng/g ww) or NE subregions (15.37 ng/g ww). Chen and colleagues (9) hypothesized that greater BDE-99 versus BDE-153 concentrations reflect dietary differences among peregrines, from a diet predominantly composed of passerines to one consisting more of doves. In the present study, the diet of urban chicks was mostly Columbidae compared to the broader diet of the Lake Superior nestlings. The more highly brominated congeners that were monitored, BDE-209, BDE-190, and BDE-183, were detected at low concentrations in the peregrine chicks’ plasma (Table 2). The presence of BDE-209 in all peregrine chicks, and herring gull eggs (17), across the Great Lakes indicates that BDE-209 is recently and widely bioavailable in the Basin. The BDE-209 concentrations accounted for only 0.4 to 1.9% of Σ14PBDE levels in the peregrine plasma (Table 2), similar to peregrine eggs from Greenland (0.4 to 4.1%) (11) and California (∼6%) (14, 15). The low concentrations of BDE209 in the chicks may be a function of its debromination to lower brominated PBDE congeners as suggested for Great Lakes herring gulls (17) and Californian peregrines (14). The plasma BDE-209 concentrations are much higher, albeit not statistically, in the remote Thunder Bay and North Shore peregrines compared to the urban chicks, contrasting with previously reported patterns whereby urban peregrine eggs had higher BDE-209 concentrations (14). Given that the urban peregrines in both studies (here, ref 14) have the same diet, the current results support the hypotheses that exposure to BDE-209 is a function of 1) atmospheric deposition since industry in these two relatively remote regions is dominated by pulp and paper mills and 2) differences in local sources because the half-life of BDE-209 is short in birds (i.e., 11-18 d) (34). HBCD was only detected in the plasma of urban peregrines, including those in the small city of Thunder Bay, and consistently at concentrations
