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19 Aug 2009 - coastal and estuarine environments around the Yellow River. Delta (11, 12) and represent a potential threat to birds. * Correspondence a...
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Environ. Sci. Technol. 2009, 43, 6956–6962

Brominated Flame Retardants, Polychlorinated Biphenyls, and Organochlorine Pesticides in Bird Eggs from the Yellow River Delta, North China FAN GAO,† XIAO-JUN LUO,‡ Z H I - F E N G Y A N G , * ,† X I N - M I N G W A N G , ‡ A N D B I - X I A N M A I * ,‡ State Key Laboratory of Water Environment Simulation, School of Environment, Beijing Normal University, Beijing 100875, China, and State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China

Received April 20, 2009. Revised manuscript received July 14, 2009. Accepted August 10, 2009.

Concentrations of several persistent organohalogen compounds such as dichlorodiphenyltrichloroethane and its metabolites (DDTs), hexachlorocyclohexanes (HCHs), polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), decabromodiphenylethane (DBDPE), and polybrominated biphenyl 153 (PBB 153) were measured in eggs of six species of wild aquatic birds, one species of wild terrestrial bird, and two species of captive birds from North China. Among the contaminants measured, DDTs were the dominant compounds, HCHs and PCBs were in nearly the same concentration range, and PBDEs exhibited lower concentrations than other compound groups. The median concentrations of DDTs, HCHs, PCBs, and PBDEs in all avian species ranged from 21 to 11034, 5.5 to 623, 1.0 to 613, and 4.6 to 146 ng/g lipid wt, respectively. Median concentrations of DBDPE and PBB 153 in all avian species were in the range of not detectable (ND)-1.7 and ND-0.7 ng/g lipid wt, respectively. Significant differences among species in contaminant profiles and contaminant levels were found depending on their feeding habits, habitat, and migration. The captive birds had the lowest contaminant levels and entirely different congener profiles in PCBs and PBDEs from those of wild birds, which can be attributed to differences in dietary compositions and reproduction rates. Octa- to deca-BDEs contributed more to the total PBDEs in wild terrestrial and captive birds than in wild aquatic birds, except for one insectivorous species, possibly due to greater exposure to terrestrial food sources. Preliminary risk assessment suggests that there is no risk of a reduction in offspring survival in avian species from North China due to organohalogen compounds, except for dichlorodiphenyldichloroethylene (DDE), which would be expected to affect some proportion of the populations of several species of birds studied.

* Correspondence author phone: +86-10-58807951 (Z.Y.), +8620-85290146 (B.M.); fax: +86-10-58803006 (Z.Y.), +86-20-85290706 (B.M.); e-mail: [email protected] (Z.Y.), [email protected] (B. M.). † Beijing Normal University. ‡ Guangzhou Institute of Geochemistry. 6956

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Introduction Persistent organic pollutants (POPs) have been of special concern for several decades because of their persistence, toxicity, and tendency to bioaccumulate. Several organochlorine pesticides (OCPs) and polychlorinated biphenyls (PCBs) have been added to the list of POPs by the Stockholm Convention which came into force in 2004. Dichlorodiphenyltrichloroethane (DDT) and hexachlorocyclohexanes (HCHs) are two typical classes of OCPs that have been widely used as insecticides (1). PCBs were used in a wide array of products as dielectric fluids and additives during the 1930s through the mid-1970s (2). Perhaps because of their widespread use, OCPs and PCBs have remained detectable in environmental samples from around the globe despite the ban and restriction on their production and usage (3). More recently, there has been growing evidence that brominated flame retardants, primarily polybrominated diphenyl ethers (PBDEs), are ubiquitous environmental pollutants and are similar in physicochemical properties to other POPs such as PCBs (3-5). PBDEs have been used extensively as flame retardant additives in textiles, thermoplastics, polyurethane foams, and electronic products. However, their continued use is under increased scrutiny because of their potential toxicity to wildlife and humans (6). For example, the production and use of penta-BDE and octa-BDE technical mixtures have been banned or phased-out in most states (6, 7), and deca-BDE was incorporated in the list of hazardous substances banned in the European Union (EU) Restriction of Hazardous Substances (RoHS) directive in July 2008 (8). Decabromodiphenylethane (DBDPE) was used in applications ranging from consumer electronics to wire and cable to insulation foams and can be used in place of deca-BDE (5-7). Several recent reports have documented that DBDPE is widely present in the environment and wildlife (5-7, 9, 10). Birds have been frequently used as sentinel species for monitoring the levels and effects of POPs in the environment because they are widespread and sensitive to environmental changes and often occupy the top position in the food chain (13, 14). A number of papers have confirmed that bird eggs are good biomonitoring tools to measure the levels and effects of different POPs in the environment (15, 16). This is because bird eggs not only can reflect levels of POPs in female birds, but also embryos are thought to be the developmental stage most susceptible to POP effects (17, 18). Moreover, eggs of most bird species can be collected easily, and the removal of a single egg from a clutch is expected to have minimal impact on the population (13). While a vast number of studies have been performed on POP accumulation in avian eggs from Europe and North America (14-19), very limited data have been published on Chinese bird eggs (13, 20). The Yellow River Delta, located in the northern part of Shandong Province and on the southwest coast of the Bohai Sea, is an important breeding ground, stopover site, and wintering ground for migratory water birds from the interior of northeastern Asia and the western Pacific Rim. It is thus a member of the East Asia-Australia wading birds network and a biosphere reserve of China Man and Biosphere Programme. However, as one of the important economic resources for North China, the Yellow River Delta region has been developed into an important chemical and petrochemical industry base. A wide range of persistent contaminants, including polycyclic aromatic hydrocarbons, OCPs (e.g., DDTs), PCBs, and PBDEs have been identified in the coastal and estuarine environments around the Yellow River Delta (11, 12) and represent a potential threat to birds. 10.1021/es901177j CCC: $40.75

 2009 American Chemical Society

Published on Web 08/19/2009

TABLE 1. Concentrations (ng/g lipid wt) of Organohalogen Compounds in Bird Eggs from the Yellow River Delta, North China DDTsa species wild species aquatic bird Saunders’s gull common tern Kentish plover black-winged stilt oriental pratincole common coot terrestrial bird ring-necked pheasant captive species mallard swan goose

n median

range

12 11034 5106-15640 9 3715 1429-9119 8 947 423-22530 6 7177 654-9899 4 3012 1532-4001 4 235 154-383 4 11 9

HCHsb median

533 300 213 301 129 36

8480 3250-14247 623 67 34-87 21 2.1-82

range

PCBsc median

range

PBDEsd median

DBDPE

range

median

rnge

PBB 153 median range

368-1248 613 52-944 216 116-264 181 96-604 96 90-3082 81 25-39 26

362-1006 146 127-660 78 74-515 54 23-158 30 67-92 33 14-34 11

101-233 34-228 30-110 7.1-77 29-46 3.1-20

0.5 0.1 0.4 1.7 nde 0.6

nd-0.9 nd-0.1 nd-0.9 0.3-2.2 NAf 0.4-0.7

0.3 0.5 0.3 nd 0.1 nd

0.1-0.6 nd-0.5 nd-0.4 NA nd-0.1 NA

427-943

380-488

62-125

1.4

0.9-2.4

0.7

0.1-1.4

4.6 2.0-11 9.6 1.1-50

0.5 1.0

0.1-1.0 nd-1.7

nd nd

NA NA

5.5 3.1-6.9 6.9 1.3-12

410

5.5 2.9-9.8 1.0 0.4-4.6

90

a Sum of p, p′-DDT, p, p′-DDE, p, p′-DDD, p, p′-DDM, p, p′-DDMU, o, p′-DDE, o, p′-DDD, and o, p′-DDT. b Sum of R-HCH, β-HCH, γ-HCH, and δ-HCH. c Sum of CB 28/31, 52, 60, 64, 66, 74, 85, 87/115, 90, 95, 97, 99, 101, 105, 107, 110, 114, 117, 118, 119, 123, 128, 130, 131, 135, 137, 138, 141, 146/161, 147, 149/139, 153, 154, 158, 164/163, 167, 170/190, 171, 172, 174/181, 175, 177, 178, 180/193, 183, 187, 189, 194, 195, 197, 199, 201, 202, 203/196, 205, 206, 207, 208, and 209. d Sum of BDE 28, 47, 66, 99, 100, 138, 153,154, 183, 196, 197, 203, 206, 207, 208, and 209. e Not detectable. f Not available.

In the present study, we examined the levels, patterns, and sources of persistent organohalogen compounds such as DDTs, HCHs, PCBs, PBDEs, DBDPE, and polybrominated biphenyl 153 (PBB 153) in bird eggs from females representative of different habitats, migration, and breeding habits in the Yellow River Delta, North China. Furthermore, the potential for adverse effects of organohalogen compounds on avian species was evaluated by comparison of the residue concentrations with toxicity reference values (TRVs). To our knowledge, this is the first comprehensive assessment of organohalogen compounds in avian species from North China.

Materials and Methods Sample Collection. Egg samples (n ) 67) were collected from the Yellow River Delta National Nature Reserve in China in May 2008 (Figure S1 of the Supporting Information). Details of the sampling sites are also given in the Supporting Information. The sampled species included six species of wild aquatic birds [Saunders’s gull (Larus saundersi], n ) 12; common tern (Sterna hirundo), n ) 9; kentish plover (Charadrius alexandrinus), n ) 8; black-winged stilt (Himantopus himantopus), n ) 6; oriental pratincole (Glareola maldivarum), n ) 4; and common coot (Fulica atra), n ) 4], one species of wild terrestrial bird [ring-necked pheasant (Phasianus colchicus), n ) 4], and two species of captive birds [mallard (Anas platyrhynchos), n ) 11 and swan goose (Anser cygnoides), n ) 9]. Common coot and ring-necked pheasant are resident species, while the other wild species are migrants. Biological information (genus, migration, diet, etc.) and details of the egg samples are presented in Tables S1 and S2 of the Supporting Information. Wild bird eggs were collected from each randomly selected nest in the early stages of incubation. Captive bird eggs (one egg per nest) were provided by the Yellow River Delta National Nature Reserve. The egg samples were cleaned with deionized water and stored at -20 °C until chemical analysis. Sample Preparation. Approximately 7 g of egg contents were ground with anhydrous sodium sulfate, spiked with surrogate standards (BDE 77, BDE 181, 13C12-BDE 209, and 13 C-PCB 141 for PBDEs and PCB 65 and PCB 204 for PCBs and OCPs, respectively), and then Soxhlet extracted with 50% acetone in hexane for 48 h. The lipid content was determined gravimetrically from an aliquot of the extract. Another aliquot of the extract used for chemical analysis was subjected to gel permeation chromatography for lipid removal. The lipidfree eluate was concentrated to 2 mL and further purified on

2 g of silica gel solid-phase extraction column (Isolute, International Sorbent Technology, U.K.). The fraction containing organohalogen compounds was concentrated to near dryness and redissolved in 200 µL of isooctane. Known amounts of internal standards (13C-PCB 208, BDE 118, and BDE 128 for PBDEs and PCB 24, 82, and 198 for PCBs and OCPs) were added to all extracts prior to instrumental analysis. Chemical Analysis. Instrumental conditions, quantification procedures, and quality assurance/quality control (QA/ QC) measures and outcomes are provided in the Supporting Information. Data Analysis. All concentrations were lipid-normalized except where indicated (i.e., Risk Assessment). Samples with concentrations below the detection limits were assigned a value equal to half of the detection limits. Statistical analyses were performed with SPSS for Windows Release 13.0 (SPSS, Inc.; U.S.A.). Data were not normally distributed (ShapiroWilk test, p > 0.05) and were, therefore, log-transformed (y ) log10x). One-way analysis of variance (ANOVA) with a post hoc test (Tukey’s HSD test) was used for interspecies comparisons of contaminant levels. To further evaluate the correlative relationships between contaminants and species, we conducted principal component analysis (PCA) on the data of R-HCH, β-HCH, all DDT isomers except for o, p′DDT and p, p′-DDM, all BDE congeners detected, seven indicator PCB congeners (CB 28, 52, 101, 118, 138, 153, and 180), DBDPE, and PBB 153. Kruskal-Wallis tests with Bonferroni corrected significance level were performed to compare factor scores among species. Statistical significance was set at R ) 0.05 throughout this study.

Results and Discussion Levels and Composition Profiles. DDTs and HCHs. All egg samples contained detectable DDTs with median concentrations ranging from 21 (Swan goose) to 11034 ng/g (Saunders’s gull). This level was generally 1-2 orders of magnitude greater than those of HCHs, PCBs, and PBDEs (Table 1 and Figure S2 of the Supporting Information). The composition profiles of DDTs among avian species were generally similar to each other. p, p′-DDE was the dominant DDT compound followed by p, p′-DDD and p, p′-DDT. They collectively constituted 94-100% of total DDT concentrations in all species (Figure S3 of the Supporting Information). This result was similar to a number of previous studies (13, 15). It was worth noting that p, p′-DDMU and p, p′-DDM, two p, p′-DDT metabolites (21), were detected VOL. 43, NO. 18, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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in 85% and 13% of the samples, respectively. Although these two compounds have rarely been reported in wildlife from industrial countries, the occurrence of p, p′-DDMU has been reported in Chinese wildlife recently (22, 23). This might be due to the fact that large amounts of DDTs have been used in China historically. Given the potential adverse effects of p, p′-DDMU to organisms (24), further studies are warranted to better understand its environmental fate and toxicity to wildlife, including birds in China. The lack of o, p′-isomers in bird eggs indicated that the contribution from the currently used insecticide dicofol was limited. Elevated contributions from p, p′-DDT and p, p′-DDD to the total DDTs were observed in Kentish plovers and blackwinged stilts, which may have different metabolic reactions to DDTs, or were exposed to different DDT contamination sources relative to other aquatic birds. In the case of captive birds, the contributions of p, p′-DDT to the total DDTs were similar to those of p, p′-DDT to the total DDTs in eggs of poultry available from markets of several large cities in China (25). Median concentrations of HCHs were in the range of 5.5 (mallard) to 623 ng/g (ring-necked pheasant) (Table 1 and Figure S2 of the Supporting Information). β-HCH was the predominant HCH isomer, accounting for 80-100% of total HCH concentrations. This may be because β-HCH has lower vapor pressure but higher bioaccumulation factor than other HCH isomers (26). R-HCH and δ-HCH were detected in 69% and 24% of samples, respectively, and their concentrations were remarkably lower than those of β-HCH. No γ-HCH was detected in any sample (Figure S4 of the Supporting Information). This congener profile of HCHs showed great consistency with some earlier findings (10, 15). The frequent occurrence of β-HCH at high levels, along with the disappearance of γ-HCH, suggested that HCH residues in the samples were largely derived from historical usage in agriculture instead of recent inputs. PCBs. PCBs were in the same concentration ranges as HCHs in all avian species, with median concentrations ranging from 1.0 (swan goose) to 613 ng/g (Saunders’s gull) (Table 1 and Figure S2 of the Supporting Information). A significant difference in PCB congener profile was found between wild and captive species (Figure S5 of the Supporting Information). For wild birds, PCB 118, 153/132, 138, and 180/ 193 were the major congeners and collectively constituted 54-63% of the total PCB concentrations, which was similar to previous studies (16, 18). For the captive species, however, the highly chlorinated PCB congeners were noticeably diminished, whereas there was a notable enrichment of PCB 28/31 and 52, which was similar to PCB congener profiles in eggs of poultry available from markets of several large cities in China (25) and in the commercial compound feed for poultry from Europe (27). Generally, PCB congener profiles in eggs depend on the uptake, clearance, and metabolization rates of avian species (28). Therefore, differences in dietary composition between wildlife and captive species may be responsible for the distinct congener patterns of PCBs. PBDEs. The concentrations of PBDEs were 2-5-fold lower than those of PCBs for each species, excluding the captive birds, which contained the same levels of PCBs and PBDEs. Median concentrations of PBDEs ranged from 4.6 (swan goose) to 146 ng/g (Saunders’s gull) (Table 1 and Figure S2 of the Supporting Information). Significant distinctions in the congener-specific patterns of PBDEs existed among avian species (Figure 1). With the exception of oriental pratincole, BDE 47 had the highest abundance in all species of wild aquatic birds, comprising 34% of total PBDEs, followed by BDE 99 and 153 at nearly equal proportions. This distribution pattern was consistent with most previous reports on aquatic birds (10, 14). However, BDE 209 was the most abundant congener in eggs of a wild 6958

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terrestrial bird (i.e., ring-necked pheasant). This congener pattern was similar to that reported in some species of birds of prey from North China (29), which reinforces the view that terrestrial biota may experience more highly brominated congeners than aquatic organisms (10, 11). For the captive species, elevated contributions from the octa- to deca-BDE congeners (BDE 196, 197, 203, 206, 207, 208, and 209) were observed. This finding is in line with those in free-range domestic fowl from an e-waste recycling site in South China (30).These results suggest that the captive species might have an entirely different exposure route and/or elimination of PBDEs from those of wild birds. It is interesting that oriental pratincoles were dominated by BDE 209, which suggests that oriental pratincoles are highly exposed to a deca-BDE mixture. Consuming insects via the food chain has been implicated as a major source of BDE 209 exposure in birds (10). Therefore, insects, especially grasshoppers, the food of oriental pratincoles, may be the better explanation for this finding. More importantly, the detection of octa- and nonaBDE congeners in most samples suggests the prevalence of higher BDE congeners in bird eggs, which may be attributed to enzymatic and/or photocatalytic debromination of BDE 209 (31, 32). Currently, large quantities of deca-BDE are still used in many products in China. In light of the above findings, it can be anticipated that the concentrations of PBDEs may further increase in the near future; therefore, limiting unnecessary deca-BDE release to the environment is of great importance and urgency. DBDPE and PBB153. DBDPE was detectable in 54% of the samples, and the median concentrations of DBDPE were in the range from below detection limit to 1.7 ng/g (Table 1 and Figure S2 of the Supporting Information), which were remarkably lower than those in muscles of water birds from an e-waste recycling region in South China and those in herring gull eggs from the Great Lakes in North America (10, 14). The ratios of BDE 209 to DBDPE varied from 1.2 to 38 in the samples containing detectable DBDPE and BDE 209 (Table S2 of the Supporting Information), which may be due to the large difference between the quantities of BDE 209 and DBDPE used commercially as the commercial use of DBDPE began in the 1990s, 20 years later than that of BDE 209 (10). Clearly, even though the concentrations of DBDPE are lower than those of BDE 209 now, the occurrence of DBDPE will undoubtedly trigger a worldwide concern with its increasing global usage. Therefore, further studies concerning DBDPE are urgent to better understand its transformation, uptake, and toxicological effects on wildlife. PBB 153 was detected in only 36% of all samples with concentrations in the range of not detectable to 1.4 ng/g (Table 1 and Figure S2 of the Supporting Information), which were much lower than those of the major BDE congeners, indicating that PBB 153 burdens were negligible in avian species in this region. Most previous studies focused on the exposure of eggs of seabirds and raptors to organohalogen compounds; therefore, only the data with Saunders’s gull and common tern eggs in this study were used to compare with those from other countries or regions and are listed in Table S3 of the Supporting Information (13-20, 33-36). In general, the concentrations of DDTs and HCHs from the present study were at the high end of the worldwide range, while those of PCBs were lower than the reported data for avian eggs in other parts of the world. This result is in agreement with the fact that China has a high consumption of DDTs and HCHs (1) but a relatively modest consumption of PCBs (37). PBDE concentrations were consistent with the commonly observed values for eggs of seabirds and raptors from around the world, which may suggest that the consumption rates of PBDEs in China have been comparable to those in other countries.

FIGURE 1. PBDE congener profiles in bird eggs from the Yellow River Delta, North China. Error bars represent one standard error. Differences among Bird Species. The differences in concentrations of DBDPE and PBB 153 are not discussed here because less than 60% of the samples had concentrations over the detection limit. The size of samples of ring-necked pheasant, oriental pratincole, and common coot are small (n ) 4) and hampered the comparison among species. The concentrations of DDTs, HCHs, PCBs, and PBDEs all were significantly higher in wild birds than in captive birds (p < 0.01, F > 14.4), which is most likely a function of their diet and reproductive rate. The captive birds were raised on a controlled diet, which consists mainly of corn (50%), wheat bran (31-35%), soybean meal (10%), oyster shell whiting, and some trace elements (5%), etc. and is similar to the feeds of poultry, suggesting that they are sitting at the lower end of the food chain. A field sampling survey conducted by the Yellow River Delta National Nature Reserve revealed that wild birds laid only 3-12 eggs per year but captive birds laid 110 and 50, indicating that the captive birds have a higher reproductive rate. No significant differences (p > 0.05, F < 2.4) in the concentrations of DDTs, HCHs, PCBs, and PBDEs were observed among the four species of migrant aquatic birds (Saunders’s gull, common tern, Kentish plover, and black-winged stilt), while Saunders’s gull appeared to be enriched in such compounds. PCA provides an informative visual display, facilitating interspecies comparisons. The loading plot of PCA is shown in Figure 2a. Only the first two factors from PCA, which

together accounted for 71.9% of the total variance (58.4% for PC1 and 13.5% for PC2), were used for the statistical analysis. The score plot of PCA clearly exhibited the species-specific differences in the levels of contaminants (Figure 2b). The factor scores for PC1 were highest in the wild terrestrial bird and lowest in the captive birds. PC1 was heavily weighted with almost all compounds targeted except for octa- to decaBDEs and DBDPE. The low factor scores for captive birds on PC1 indicated that they were contaminated with less organohalogen compounds than wild birds. As discussed above, it may be different exposure routes for different bird species (33, 38). The interspecific differences in contaminant profiles can be explained to a great extent by differences in dietary habits. Table S1 of the Supporting Information displayed the detailed dietary habits of birds. Saunders’s gull feeds mainly on small fishes, shrimps, and clam worms (about 95% together), and common tern is a piscivorous bird feeding primarily on fish (90%) and a few aquatic insects. Kentish plover and blackwinged stilt mainly feed on benthic animals (about 86% and 84%, respectively) such as oysters, insects, and crustaceans. Oriental pratincole feeds on almost entirely insects and other arthropods, in particular, grasshoppers and beetles, mostly caught in the air. Common coot is a phytophage generally feeding on aquatic plants. Saunders’s gull and common tern are enriched in most organohalogen compounds, while other aquatic birds accumulated less such compounds. Previous VOL. 43, NO. 18, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 3. Cumulative probability distribution of DDE (sum of p, p′-DDE and o, p′-DDE) concentrations in eggs of seven species of wild birds from North China with DDEs TRV indicated. TRVs are from refs 13 and 20.

FIGURE 2. (a) Loading and (b) score plots of PCA on the log-transformed database of organohalogen compounds in bird eggs. Organohalogen compounds include all DDT isomers except for o, p′-DDT and p, p′-DDM, r-HCH, β-HCH, seven indicator PCB congeners (CB 28, 52, 101, 118, 138, 153, and 180), all BDE congeners detected, DBDPE, and PBB 153. SA, Saunders’s gull; CT, common tern; KP, kentish plover; BS, black-winged stilt; OP, oriental pratincole; CC, common coot; RP, ring-necked pheasant; MA, mallard; and SW, swan goose. studies (10) also reported that the levels of organohalogen compounds were higher in piscivores birds than in omnivores, insectivores, and granivores. Ring-necked pheasant is a terrestrial omnivore and phytophage, with diets comprising 85% plant seeds and fruits and 15% aquatic insects, which indicated that this species may have entirely different food sources and habits relative to aquatic birds. Moreover, differences in migratory habits, habitats, metabolic capacity, and the age of female birds can also influence the levels and patterns of organohalogen compounds in eggs of different bird species but were not further investigated in the present study because of the lack of data or limited sample size. Risk Assessment. Point estimate comparisons and probabilistic approaches were used to evaluate the potential adverse effects of organohalogen residues on eggs. In the point estimate approach, concentrations of individual residues measured in eggs were compared to published, consensus toxicity reference values (TRVs) for each compound. For calculating the probability of risk quotients (RQs) exceeding unity, Monte Carlo simulation using Crystal Ball (Oracle, Denver, CO) was carried out. No risk assessment was performed on the captive birds because of too low contaminant concentrations. In the cases of DBDPE and PBB 153, an assessment was impossible because of a lack of available toxicological information. DDTs and HCHs. A probabilistic risk assessment of DDE (sum of p, p′-DDE and o, p′-DDE) was conducted by comparing the probability of concentrations in eggs exceed6960

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ing the TRV. The results indicated that all DDE concentrations in eggs except for an outlier in the Kentish plover were lower than the threshold [2800 ng/g wet weight (ww)] associated with reproductive impairment of fish-eating bird populations (20). When the TRV based on the reduction in survival of young in Ardeids (1000 ng/g ww) (13) was compared to the distribution of concentrations in eggs, DDE concentrations in eggs of Saunders’s gull, common tern, kentish plover, and ring-necked pheasant exceeded the TRV. Assuming a lognormal distribution of the concentrations in eggs (Figure 3), we compared a Monte Carlo simulation to the threshold value (1000 ng DDE/g, ww, egg) and the 95% UCI (95% upper confidence interval) of DDE concentrations in eggs to calculate risk quotients (RQs). Using 10000 simulation trials, the probabilities of RQs exceeding unity for saunders’s gull, common tern, kentish plover, and ring-necked pheasant from North China were 44.2%, 14.8%, 7.2%, and 15.6%, respectively. Saunders’s gull is an endangered species. Higher DDE concentrations in eggs may be responsible for the decline of the Saunders’s gull population according to the risk assessment. However, TRV based on the survival of young of Ardeids is not the species-specific TRV for Saunders’s gull. Thus, further studies are necessary to give clear evidence that their population is declining due to DDE. An avian TRV is not available for HCHs, but hatchability of ring-necked pheasants (Phasianus colchicus) and American kestrels (Falco sparverius) eggs were not affected by concentrations of β-HCH and γ-HCH as high as 10 and 5.5 µg/g ww, respectively (39). In the present study, the concentrations of β-HCH in all samples were about 2-3 orders of magnitude lower than that reference value, and the HQs were far less than 1 (Figure S6 of the Supporting Information), whereas γ-HCH was below detection limit. Thus, current concentrations of HCHs in eggs would not likely cause adverse effects on the reproduction of avian species in North China. PCBs. Risk estimates based on the 12 dioxin-like PCBs and total PCBs were conducted (40). The TEQWHO-avian-TEF in the present study was calculated using the World Health Organization toxic equivalency factors (41). The mean concentrations of TEQWHO-avian-TEF ranged from 0.01 to 0.46 pg/g ww (Figure S7 of the Supporting Information). There is a wide range of no observable adverse effect levels (NOAELs) and lowest observable adverse effect levels (LOAELs) suggested for TEQs of dioxin-like compounds in avian eggs (42). In the laboratory, the minimal TRV (66 pg TEQ/g ww egg) was derived from the NOAEL for the white leghorn chicken (Gallus gallus). In the field, the minimal TRV (5 pg TEQ/g ww

egg) was based on the NOAEL for the wood duck (Aix sponsa) (42). These two TRV values were higher than TEQs in the present study (Figure S8 of the Supporting Information), which suggested that there was no immediate risk of a reduction in offspring survival in avian species from North China. TRVs for total PCBs in eggs were based on the NOAELs reported to cause reproductive impairment. In a review by Barron et al. (43), NOAELs (µg/g ww egg) were reported to range from 0.36 in chickens to 23.3 in mallards. Hoffman et al. (44) referred to 1-5 µg/g ww in eggs as threshold concentrations causing decreased hatching success for chickens and 8-25 µg/g ww in eggs as thresholds for decreased hatching success for terns, cormorants, doves, and eagles. Concentrations of PCBs in eggs were less than that TRV (Figure S9 of the Supporting Information) and thus are probably insufficient to cause observable adverse effects on avian species from North China. PBDEs. Fernie and her colleagues (45) have reviewed the cause and effect mechanisms of PBDE exposure on avian reproduction at PBDE concentrations that are currently found in the eggs of terrestrial and aquatic bird species. Exposure of captive kestrels to these environmentally relevant concentrations of PBDEs adversely affected their reproductive success in various ways (45). The concentrations of PBDEs in kestrel eggs were, however, about 1-3 orders of magnitude higher than our results (Figure S10 of the Supporting Information). Thus, the relatively low levels of PBDEs in this study are not expected to have adverse reproductive implications. However, interactions between PBDEs and other environmental pollutants may occur and can be responsible for detrimental health effects. For example, it has been shown that PBDEs can interact with PCBs to cause developmental neurotoxic effects in mice when exposed during a critical period of neonatal brain development (46). Also, it should be noted that the American kestrel is a totally different species from avian species in this study.

Acknowledgments This work was funded by the National Basic Research Program of China (2006CB403303), National Science Fund for Distinguished Young Scholars of China (50625926), National Natural Science Foundation of China (40632012), and Open Fund of the State Key Laboratory of Organic Geochemistry (OGL-200710).

Supporting Information Available Additional information as noted in text. This material is available free of charge via the Internet at http://pubs.acs.org.

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