Environ. Sci. Technol. 2006, 40, 5297-5303
Accumulation of Organochlorines and Brominated Flame Retardants in the Eggs and Nestlings of Great Tits, Parus major T O M D A U W E , * ,† V E E R L E L . B . J A S P E R S , † ADRIAN COVACI,‡ AND MARCEL EENS† Department of Biology and Toxicological Center, University of Antwerp, Universiteitsplein 1, B-2610 Antwerp, Belgium
Insectivorous birds may be very useful sentinels for local point-source contamination with persistent pollutants, such as polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs) and organochlorine pesticides (OCPs). Eggs have been used extensively to monitor lipophilic contaminants, as females can pass contaminants stored in their body tissues into their eggs. Concentrations and profiles in eggs therefore relate to contamination in the female. Because nestlings are raised on food items collected locally, it is expected that the body burden in nestlings would reflect their diet and local pollution levels better than eggs. In this study we compared the accumulation and the profile of PCBs, PBDEs, and OCPs in great tit (Parus major) eggs, nestlings (5-, 10-, and 15-days old), and their food in two study sites. Our results showed that concentrations in great tit eggs were 4 to 6 times higher than those in nestlings. Concentrations in nestling great tits corresponded with concentrations predicted by a bioenergetics-based model. Most of the persistent organic pollutants in 15-day old nestlings were still from maternal origin. The profile of these persistent pollutants in eggs and nestlings also gradually changed during development. With increasing age, the proportion of the most persistent compounds decreased. This study shows that most of the persistent pollutants in fully grown nestlings may still be from maternal origin. For nestlings to be suitable as indicators of local contamination, most of the POPs they accumulate should originate from dietary sources rather than from maternal transfer via the egg. Nestling birds may therefore not be good sentinels for local contamination with persistent pollutants.
Introduction The presence of persistent organic pollutants (POPs) in the environment has been a cause of concern for over 40 years (1). After reports on the toxicity of polychlorinated biphenyls (PCBs) and organochlorine pesticides (OCPs) on humans and wildlife, the production of many organochlorines was banned worldwide resulting in a decrease of levels in both environment and biota (2), although some studies have reported that levels tended to stabilize in recent decades (3). Polybrominated diphenyl ethers (PBDEs) are widely used as * Corresponding author e-mail:
[email protected]; phone: 32 3 820 22 85; fax: 32 3 820 22 71. † Department of Biology. ‡ Toxicological Center. 10.1021/es060747a CCC: $33.50 Published on Web 07/28/2006
2006 American Chemical Society
flame retardants in numerous applications such as textiles, plastics, and foams. PBDEs can leach from the commercial materials in which they are incorporated and pollute the environment. From the 1980s to 2000s concentrations of PBDEs have increased markedly in the environment, biota, and humans (4). Recently, the production of the most persistent PBDE congeners was banned in Europe. Among the most critical effects of PBDEs on wildlife are developmental neurotoxicity and altered thyroid hormone homeostasis (5). After it was demonstrated in the 1960s that DDT negatively affected many raptorial and piscivorous bird populations, avian predators have been used intensively to monitor environmental contamination with POPs (6-8). However, because most of these birds are migratory or forage in an extended area, they are less suited to monitor local pollution levels. PCB contamination from point-source pollution has, in some cases, resulted in a high but very local contamination (cf. certain superfund sites in the United States; 9). To be able to monitor pollutant levels in small study sites with point-source pollution, interest shifted to birds with a smaller home range and insectivorous diet. In North America, studies with tree swallow (Tachycineta bicolor; 10, 11) and European starling (Sturnus vulgaris; 9, 12) have shown the usefulness of passerine model species to assess contaminant levels and harmful effects of POPs in field studies. In this study we have used the great tit (Parus major) as a sentinel species to determine PCB, PBDE, and OCP contamination in a terrestrial food web. Great tits are residential passerines that live throughout most of Europe. They are hole nesting birds that preferably use nest boxes over natural nest sites, which permits easy sampling and studying of populations. Although several studies have reported heavy metal accumulation in and effects on great tits (13), there are only a few studies on POPs (14, 15). Eggs have been used predominantly to monitor lipophilic contaminants, such as PCBs, as females can pass contaminants stored in their body tissues into their eggs. Because birds are mobile and can metabolize POPs, concentrations and profiles of POPs in eggs may not adequately reflect local pollution. To overcome this problem, the accumulation of contaminants in nestlings has been determined. Because nestlings are often raised on food items collected locally and the biomass of nestlings increases manifold between hatching and fledging, it is expected that the body burden of contaminants in nestlings would predominantly reflect their diet rather than maternally derived xenobiotic compounds (16). In this study we examined and compared the accumulation and the profile of PCBs, PBDEs, and OCPs in great tit eggs and nestlings in two sites with low to moderate pollution levels. We also determined the concentration of persistent pollutants in caterpillars, the main food item of great tit nestlings. Finally, a bioenergetics-based model, previously developed for nestling tree swallows (17, 18), was adjusted and evaluated to predict PCB, PBDE, and OCP concentrations in nestling great tits.
Materials and Methods Sample Collection. In the spring of 2005, 22 great tit nests were studied in two sites (F4 and F5) in the south of Antwerp (Belgium) that differ slightly in POP contamination (Figure SI-1 in the Supporting Information; 14). During the reproductive cycle, great tit nests were regularly visited from nest building until egg laying. When 6 or more eggs were laid, one egg was randomly collected. A previous study showed that variability was considerably lower within than among nests VOL. 40, NO. 17, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
5297
and that laying sequence had no effect on PCBs, PBDEs, or OCPs concentrations (19). After egg collection, nests were not visited for at least 12 days. To determine the exact hatching date, nests were again checked daily at the end of the incubation period. After hatching we collected one nestling ad random 5-, 10-, and 15-days post hatching from each nest (22 nests in total). Nestlings were immediately sacrificed with CO2 intoxication. Eggs and nestlings were stored frozen (-20°) until analysis. We collected the most important food items of great tit nestlings in the vicinity of each nest box, i.e., caterpillars, which comprise 73-92% of the diet of nestling great tits in deciduous woodland (20). In 4 nests, we weighed all the eggs and nestlings with an electronic balance (( 0.1 g). Eggs were weighed once before the female started incubation and nestlings were weighed daily from hatching until they were fully grown (16 days old). Sample Preparation. Sample Extraction and Cleanup. The whole egg (∼1 g), homogenized nestlings (∼5 g), and caterpillars (∼4 g) were weighed, mixed with anhydrous Na2SO4, and spiked with internal standards (CB46, CB143, BDE77, and BDE128). Further sample treatment and analysis were performed according to previously described methods (14, 21). Briefly, extraction was carried out with 100 mL of hexane/acetone (3:1, v/v) in a hot Soxhlet extractor for 2 h. The lipid content was determined on an aliquot of the extract (1 h, 105 °C), while the rest of the extract was cleaned up on a column filled with ∼8 g of acidified silica and eluted with 15 mL of hexane and 10 mL of dichloromethane. The eluate was concentrated to 100 µL under a gentle nitrogen stream, and transferred to an injection vial. Analysis. For PBDEs and OCPs, analysis was done with a gas chromatograph coupled with a mass spectrometer (GC/MS) in electron capture negative ionization (ECNI) mode, equipped with a HT-8 capillary column (25 m × 0.22 mm × 0.25 µm). For PCBs, a GC/MS in electron ionization (EI) mode, equipped with a DB-1 capillary column (30 m × 0.25 mm × 0.25 µm) was used. In all samples, 7 PBDE congeners, 22 PCB congeners, hexachlorobenzene (HCB), trans-nonachlor (TN), oxychlordane (OxC), and p,p′-DDE were analyzed. Limits of detection for the analyzed compounds ranged between 0.2 and 2.25 ng/g lipid weight (or 0.01 and 0.15 ng/g wet weight). Quality Assurance. The quality control was done by daily check of calibration curves, and regular analyses of procedural blanks, solvent blanks, duplicate samples, and a certified reference material (CRM 350, PCBs in mackerel oil). Recoveries of individual PBDE congeners were between 87 and 104% (RSD e 12%), while recoveries of PCBs and pesticides ranged between 75 and 90% (RSD < 10%). Procedural blank values were found to be consistent (RSD < 10%) and therefore the mean procedural blank value was used for subtraction. Accuracy of the method was evaluated through the analysis of CRM 350 for which results were within 10% of the certified values, while precision was assessed through analysis of a duplicate sample and results were found to differ with no more than 5%. The method is also regularly evaluated through participation to international interlaboratory studies. Bioenergetics-Based Model. We used a model developed by Nichols et al. (17) to predict PCB, PBDE, and p,p′-DDE concentrations in nestling great tits. The POP body burden of nestling great tits was calculated as
mass POP ) mass POPegg +
∫(POP
foodCAW)/CDfood
(1)
where mass POPegg refers to the POP content in eggs (ng); POPfood (ng/g wet weight) and CDfood (kcal/g) refer to the POP concentration in and the caloric density of caterpillars, C is the food consumption rate (kcal/g/d), A is the assimilation efficiency, and W (g) is the body weight of the nestlings. POPegg was deduced from the concentration in the eggs and 5298
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 40, NO. 17, 2006
the mean weight of great tit eggs (1.2 g). The caloric density of Lepidoptera larvae was estimated from previously published papers. Koplin et al. (22) and Graber and Graber (23) determined the caloric density of a number of Lepidoptera and found a mean CD of 5.83 and 5.59 kcal/g dry weight (dw), respectively. In two Pieris species, the wet-to-dry weight conversion was 0.148 (24), so we used a caloric density of 0.85 kcal/g wet weight (ww) for caterpillars. The body weight of great tit nestlings was determined daily in 4 nests from hatching until 16-days post hatching. The food consumption rate of nestlings was estimated with an allometric equation of the form C ) RWβ. The allometric constants for C (R and β) were fitted using the observed growth data for great tits (and resulted in R ) 0.501 and β ) 0.198; for a full description of the model see 17). Drouillard and Norstrom (25) determined the assimilation efficiency of several PCB congeners ranged between 85 and 95%, with a mean of 90% which we used for all compounds in the model (25). The model does not take into account the possibility that PCBs are eliminated (the assimilation efficiency remains constant) and/or biotransformed (26). Statistical Analysis. Data are presented as ng/g ww to emphasize differences in concentration, irrespective of lipid content. PCB, PBDE, and OCP concentrations were compared among age groups (eggs, 5-, 10-, and 15-day old nestlings) and between sites with a two-way repeated measures ANOVA. Because assumptions of normality were not met, data were log(x + 1) transformed. The profile of PCBs, PBDEs, and OCPs between sites and among age groups was compared with principal component analysis on normalized concentrations (PCA without rotation). PCA was used to simplify the contaminant data by summarizing them into a smaller set of independent composite components, which helped to define the underlying contaminant patterns. First, each sample was mean centered by subtracting the mean of all compounds and scaled by dividing with the standard deviation. Then, factor loadings and factor scores were determined and used in interpreting principal component (PC) patterns.
Results Levels of POPs in Caterpillars and Great Tit Eggs and Nestlings. The median concentrations and ranges for major OCPs, PCB congeners, and PBDE congeners are presented in Table 1 for great tit eggs, nestlings, and caterpillars. Medians and ranges of individual pollutants are given in Table SI-1. No significant interactions between study site and age were found for all the pollutants (P > 0.2; although significance was almost reached for ∑PBDE, P ) 0.07). There was a small, yet significant, difference between the two sites in ∑PCB and ∑PBDE levels in great tit eggs and nestlings, with concentrations being highest at Fort 4 (P < 0.001). TN, HCB, OxC, and p,p′-DDE levels did not differ significantly between sites (P > 0.08). For all compounds a highly significant difference was found among age groups (P < 0.001). For all pollutants, concentrations in eggs were significantly higher than concentrations in 5-, 10-, or 15-day old nestlings (Tukey posthoc comparison, P < 0.001). ∑PCB and ∑PBDE concentrations were also higher in 5-day old nestlings: 5-day old great tit nestlings had significantly higher ∑PBDE concentrations than 10-day old nestlings (Tukey post-hoc comparison, P ) 0.01) and significantly higher ∑PCB and ∑PBDE than 15-day old nestlings (Tukey post-hoc comparison, P ) 0.03 and P ) 0.002, respectively). Concentrations of p,p′-DDE did not differ significantly among nestlings. For the other pesticides, 15-day old nestlings accumulated the highest concentrations. HCB and TN levels were significantly higher in 15-day old nestlings than in 5and 10-day old nestlings (Tukey post-hoc comparison, P < 0.02). OxC levels were only significantly higher in 15-day old
TABLE 1. Lipid Content and Concentrations (ng/g ww) of PCBs, PBDEs, and OCPs in Great Tit Eggs, Nestlings (5-, 10-, and 15-day old), and Caterpillars from Two Study Sites (F4 and F5) in the South of Antwerp (N ) 22; Median and Range Are Given) FORT 4 egg % lipid
8.19 7.3-10.7 CB 101 11.4 6.0-18.1 CB 149 6.15 3.5-9.4 CB 153 74.0 52-115 CB 138/136 44.4 35-69 CB 180 58.0 39-94 ∑PCB 298 209-406 BDE 47 2.66 1.4-3.7 ∑PBDE 6.85 4.2-9.8 p,p′-DDE 35.6 30-69 HCB 1.82 1.3-2.9 OxC 0.54 0.49-1.70 TN 0.99 0.7-2.5 a
FORT 5
5-d
10-d
15-d
caterpillars
egg
5-d
10-d
15-d
caterpillars
2.51 1.9-4.0 2.23 1.6-3.1 1.46 0.9-1.7 11.8 8.6-18.5 8.03 5.6-11.7 8.52 5.3-14.2 50.5 34-74 0.50 0.28-0.58 1.23 0.9-1.5 8.10 5.0-15.0 0.28 0.17-0.48 0.12 0.08-0.33 0.16 0.10-0.58
4.33 2.9-6.2 3.04 1.7-9.0 1.73 1.1-14.4 10.5 8-28 6.48 5.3-22.6 6.81 5.8-14.5 45.9 35-126 0.33 0.28-0.60 0.96 0.63-1.31 6.28 4.8-21.2 0.23 0.17-0.49 0.15 0.10-0.99 0.18 0.14-0.63
5.26 4.4-6.2 2.33 2.0-3.2 1.53 1.4-2.9 8.12 6.9-12.4 5.77 4.8-10.9 5.08 4.1-7.1 37.6 32-57 0.36 0.31-0.45 0.82 0.75-1.11 5.87 5.3-16.8 0.35 0.23-0.57 0.18 0.12-0.65 0.25 0.17-0.58
4.0
7.32 6.1-12.4 7.18 3.4-15.8 3.02 1.6-6.2 49.1 30-85 30.5 19-55 28.0 19-54 179 113-331 1.49 1.0-3.5 4.19 3.2-10.4 36.9 21-65 1.63 0.8-3.5 0.62 0.34-1.62 0.68 0.43-2.46
3.28 1.8-3.8 1.70 1.1-3.3 1.14 0.71-1.59 9.18 7.4-16.2 6.61 4.8-10.7 5.45 4.0-9.4 37.7 29-64 0.34 0.24-0.46 0.92 0.69-1.29 7.15 4.6-14.4 0.20 0.11-0.32 0.18 0.13-0.53 0.16 0.14-0.42
4.27 2.5-6.4 1.75 1.3-3.9 1.33 0.9-5.2 6.98 5.2-14.7 5.41 3.7-14.3 4.03 3.0-10.1 30.9 24-75 0.28 0.21-0.41 0.69 0.52-0.92 5.59 3.7-21.1 0.19 0.15-0.30 0.17 0.14-0.49 0.25 0.15-0.35
6.23 3.7-9.4 2.27 1.6-2.6 1.43 1.1-2.1 6.94 5.2-10.2 5.34 4.1-9.3 3.54 2.8-4.7 32.3 25-46 0.37 0.26-0.54 0.79 0.62-1.23 6.22 4.5-24.2 0.30 0.20-0.51 0.25 0.15-0.54 0.36 0.20-0.42
3.9 3.7-9.4 0.15 1.6-2.6 0.14 1.1-2.1 0.22 5.2-10.2 0.17 4.1-9.3 0.17
Caterpillars from Fort 4 and Fort 5 combined.
b
0.19 0.18 0.29 0.30 0.22
0.030
0.37a NAb NA NA
0.027
0.37a NA NA NA
NA, not analyzed.
nestlings than in 5-day old nestlings (Tukey post-hoc comparison, P ) 0.012). Profile of POPs in Great Tit Eggs and Nestlings. The PCA identified six factors with a factor score of more than 1. For the statistical analysis we only used the two most important factors, which accounted for a total of 58.5% of the total variance (39.2% and 19.4% for PC1 and PC2, respectively, Figure 1). There was a significant effect of age on PC1 (P < 0.001) and PC2 (P ) 0.001). There was also a significant difference between the sites in PC2 (P ) 0.02), but not in PC1 (P ) 1.0). For both PC1 and PC2, the interaction term between site and age was not significant (P > 0.8 in both cases). There was a remarkable relationship between PC1 and PC2 and the age (Figure 1b), suggesting a gradual change of the profile with increasing age of the nestlings. PC1 was positively associated with all PBDEs and some persistent PCBs (CB128, CB156, CB183, and CB199), while it was negatively associated with low chlorinated PCBs (CB110 and CB101; Figure 1a). The significant decrease of PC1 with age (Figure 1b), thus shows that the contribution of ∑PBDE and persistent PCBs to the total pollution load decreased with the age of the nestlings. PC2 on the other hand, was positively associated with all OCPs (p,p′-DDE, OxC, TN, and HCB), while it was negatively associated with some persistent PCBs (CB 153, CB180, CB170, and CB187; Figure 1a). The gradual increase of PC2 with the age of the nestlings thus signifies that the contribution of these persistent PCBs decreased with the age of the nestlings. The contribution of OCPs on the other hand, increased with the age of the nestlings. In Figure 2, the contribution of PCB homologues and individual PBDE congeners to ∑PCB and ∑PBDE is given. For PCBs, this figure corroborates with the PCA, i.e., the contribution of the most chlorinated and persistent PCBs decreased with the age of the nestlings. For PBDEs, the PCA showed that the contribution of all PBDE congeners to the total pollution load decreased. Figure 2 does suggest that the PBDE profile changed slightly with the age of the nestlings.
FIGURE 1. (a) Factor loadings; and (b) mean factor scores (( SE) of Principal Components 1 and 2 of eggs and 5-, 10-, and 15-day old great tit nestlings from two study sites (2 Fort 4; b Fort 5) in the south of Antwerp. VOL. 40, NO. 17, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
5299
FIGURE 2. Profiles of PCBs and PBDEs (% of ∑PCB and ∑PBDE) in eggs, and 5-, 10-, and 15-day old great tit nestlings from two study sites in the south of Antwerp (F4 Fort 4, F5 Fort 5). The contribution of low brominated PBDEs (such as BDE28 and 47) to ∑PBDE increased with the age of the nestlings. Predicted versus Observed Concentrations. The bioenergetics-based model was used to predict the CB 101, 149, 153, 138/163, 180, and BDE 47 concentrations in 5-, 10-, and 15-day old nestlings originating from Fort 4 and Fort 5 (Figure 3). For p,p′-DDE, expected concentrations in nestlings were calculated for the two sites combined, as concentrations in eggs and nestlings did not differ significantly between sites. The predictions were generally within a reasonable margin of the observed concentrations (Figure 3). The mean absolute difference was 15.5%. In most cases, predicted concentrations were lower than the concentrations we observed. Especially for 5- and 15-day old nestlings, the predicted concentrations resembled the observed concentrations well (respectively, 10.5% and 13.5%). For 10- day old nestlings, the differences between observed and predicted concentrations were higher (22.8%).
Discussion Levels of POPs in Caterpillars and Great Tit Eggs and Nestlings. Concentrations reported in this study were comparable to PCB, PBDE, and OCP levels in great tit eggs (19) and nestlings (14) from the same study sites. PCBs were by far the most important POPs in the great tits but, compared to other studies, concentrations were low. Tree swallow nestlings accumulated up to 96 000 ng/g ww and eggs up to 24 000 ng/g ww ∑PCB in the Hudson River watershed, New York (18). Starling nestlings from a Superfund site in Illinois accumulated 27 700 ng/g ww ∑PCB (9). The concentrations found at these highly polluted sites are markedly (more than 2000 times) higher than the concentrations found in nestling 5300
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 40, NO. 17, 2006
great tits from the current study. In our study however, pollution originated only from diffuse sources of PCBs, PBDEs, and OCPs. Unlike PCBs, few data exist on PBDE levels in passerine birds. Sellstro¨m (6) reported ∑3BDE levels in the muscle of starlings (collected in 1988) that ranged between 5.7 and 13 ng/g lw, which was comparable to the levels found in the great tit nestlings (∑7PBDE ranged between 7.1 and 25 ng/g lw, if we only include the three most abundant PBDE congeners: ∑3PBDE ranged between 5.9 and 20.1 ng/g lw). POP concentrations in adipose tissue of adult great tits (collected near and at the sites used in this study; 27) were comparable to the concentrations found in eggs in this study (cf. 3300 ng-1 g lw ∑PCB and 465 ng-1 g lw p,p′-DDE in eggs vs 3060 ng-1 g lw and 610 ng-1 g lw p,p′-DDE in adults). Great tits lay a large percentage of body weight in eggs over a short period of time and invest large quantities of lipids and energy into egg production, therefore concentrations were expected to be similar to those in the female. In other bird species which invest large quantities of nutrients in eggs concentrations were also similar in laying females and in eggs (see 9, 25). Profile of POPs in Great Tit Eggs and Nestlings. The profile of PCBs, PBDEs, and OCPs gradually changed with the development of nestling great tits. The profile in eggs reflects the profile in the laying female, which depends on uptake, clearance, and metabolization rates of the female. Generally, eggs contained relatively higher levels of the most persistent POPs (such as highly chlorinated PCBs and brominated PBDEs) and the proportion of these compounds decreased when nestlings grew. This was, however, not the case for all compounds. The proportion of p,p′-DDE increased with the age of the nestlings, despite its high persistence.
FIGURE 3. Model performance (expressed as the percentage deviation of the predicted value: (predicted concentration - observed concentration)/predicted concentration × 100; positive values denote that predicted concentrations are higher than observed concentrations) for (a) 5-day old great tit nestlings; (b) 10-day old great tit nestlings, and (c) 15-day old great tit nestlings from two study sites in the south of Antwerp (dark gray box, Fort 4; light gray box, Fort 5; black box, Forts 4 and 5 combined). The most important factor explaining the change in profile during development appeared to be the relative difference between concentrations in eggs and food items. If the difference was relatively small, the contribution of a compound to ∑POPs increased with age. This was the case for CB28/31, CB101, CB110, CB149, BDE49, TN, and p,p′-DDE. For all these compounds, levels in caterpillars were less than 100 times lower than in eggs. Consequently, the amount in nestlings increased more rapidly during development than the amount of CB153 and CB180, which were up to 260 times higher in eggs than in caterpillars. The mass of CB149 in 15-day old nestlings was more than 4 times higher than that in eggs, while the mass of CB180 was only 1.4 times higher in 15-day old nestlings. Winter and Streit (15) also measured PCBs and p,p′-DDE in caterpillars and great tit eggs and found much smaller differences. While concentrations in eggs were comparable between studies (CB153 929 ng/g lw vs 903 and 673 ng/g lw in our study), concentrations in caterpillars were markedly higher (CB153 10 ng/g dw or 75 ng/g lw) compared to our results (up to 7.5 ng/g lw). As expected, this resulted in higher levels of PCBs and p,p′-DDE in nestling great tits than in our study (15). Another contributing factor to the changing profile might be the differential accumulation efficiencies. The assimilation efficiency of POPs ranges between 85 and 95% and decreases with increasing log Kow value (28). However, our results suggested that assimilation efficiency did not have an important effect on the accumulation of POPs. In the model, the difference between predicted (with a fixed assimilation efficiency of 90%) and observed concentrations did not appear to be related to log Kow values. Moreover, because concentrations in food were low, the model predicted that small differences in assimilation efficiency (i.e., from 85 to 95%) only had a very marginal effect on the POP accumulation
in nestlings. This has also been found for much higher contaminant levels (18). For PBDEs, BDE47 and BDE99 contributed most to ∑PBDE, followed by BDE153 and BDE100. This was consistent for both great tit eggs and nestlings, although the profile did change with increasing age (low brominated compounds were more important in 15-day old nestlings than in eggs). In adult great tits a similar pattern was found (27). BDE47 was also by far the most important congener in many piscivorous bird species, such as terns (29), glaucous gulls (Larus hyperboreus; 30), great crested grebe (Podiceps cristatus), and grey heron (Ardea cinerea; 31). In most terrestrial species, this pattern was distinctly different. In peregrine falcon (Falco peregrinus) and merlin (Falco columbarius) eggs from Norway, BDE99 was the most important compound (32). Belgian sparrowhawks (Accipiter nisus), the most important avian predator of great tits, also had a higher contribution of BDE99 to ∑PBDE than BDE47 (31, 33). In sparrowhawks, buzzards (Buteo buteo), and kestrels (Falco sparverius) from Belgium, the more persistent compounds BDE183 and BDE153 were also relatively more important than in great tits (31). The differences in the PBDE profile between raptorial birds and great tit eggs and nestlings show that the profile of PBDEs changed within the food chain and may be caused by differences in bioaccumulation and metabolic capacities. Bioenergetics-Based Model. The model predicted the concentrations in nestling birds reasonably well, considering the generalizations we made. Although nestlings feed predominantly on caterpillars, other invertebrates, such as spiders and beetles, are also fed to nestling great tits (20). This may explain why the model underestimated the concentrations in nestling birds, especially in 10-day old nestlings. The model also performed differently at the two VOL. 40, NO. 17, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
5301
sites (Figure 3). For nestlings from Fort 4, observed concentrations were in many cases below the predicted values (although not for 10-day old nestlings). In Fort 5, observed concentrations were generally higher than predicted. This difference might have been related to a differential diet. Nevertheless, predicted concentrations differed on average 15.5% (range 0-38.6%) with observed concentrations at both sites, which is comparable with the study of Nichols et al. (17, 26). To date, there is only a limited amount of data on PCB, PBDE, and OCP accumulation in passerines with a terrestrial-based diet. The results from the bioenergetic-based model suggested that screening concentrations in eggs and caterpillars (the most important food item) was sufficient to predict concentrations in nestling great tits within an acceptable margin. The model predicted the low concentrations of persistent pollutants in nestling great tits compared to eggs. In tree swallows at Hudson Bay, the relative difference between PCB concentrations in eggs and food was much lower, which resulted in higher concentrations in 15-day old nestlings (26). For great tit nestlings on the other hand, whole body concentrations were significantly lower than concentrations in eggs. In fact, the model predicted that 15-day old nestlings would accumulate higher concentrations than eggs, if concentrations in eggs were not more than 10 times higher than in food. This is an important characteristic, because for nestlings to be suitable as indicators of local contamination, most of the POPs they accumulate should originate from dietary sources rather than from maternal transfer via the egg. In this study most of the POPs in nestlings were from maternal origin. For instance, 67% of CB153 in 15-day old nestlings originated from the egg (if we assume that no POPs were metabolized or excreted). Especially in migratory species, concentrations in adults and eggs did not necessarily reflect local contaminant levels (34, 35). Sampling nestlings may in this case lead to an over- or underestimation of the contaminant levels at the breeding site. The bioenergeticsbased model proved to be a useful tool in better understanding and interpreting our results.
Acknowledgments This study was supported by the Fund for Scientific Research Flanders (FWO-project G.0397.00 and FWO project G.0137.04). T.D. is a postdoctoral fellow and V.J. is a research assistant of the Fund for Scientific Research Flanders. A.C. acknowledges a postdoctoral fellowship of the Research Funds of the University of Antwerp.
Supporting Information Available Location of the study sites F4 and F5 (Figure SI1), table with the concentrations of all PCB and PBDE congeners and pesticides measured in great tit eggs and nestlings (Table SI1). This material is available free of charge via the Internet at http://pubs.acs.org.
Literature Cited (1) Prestt, I. J.; Jefferies, J. J.; Moore, N. W. J. Polychlorinated biphenyls in wild birds in Britain and their avian toxicity. Environ. Pollut. 1970, 1, 3-26. (2) Olafsdottir, K.; Petersen, A.; Magnusdottir, E. V.; Bjornsson, T.; Johannesson, T. Temporal trends of organochlorine contamination in Black Guillemots in Iceland from 1976 to 1996. Environ. Pollut. 2005, 133, 509-515. (3) Addison, R. F.; Ikonomou, M. G.; Fernandez, M. P.; Smith, T. G. PCDD/F and PCB concentrations in Arctic ringed seals (Phoca hispida) have not changed between 1981 and 2000. Sci. Total Environ. 2005, 351-352, 301-311. (4) Norstrom, R. J.; Simon, M.; Moisey, J.; Wakeford, B.; Weseloh, D. V. C. Geographical distribution 2000 and temporal trends (1981-2000) of brominated diphenyl ethers in Great Lakes herring gull eggs. Environ. Sci. Technol. 2002, 36, 4783-4789. 5302
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 40, NO. 17, 2006
(5) Danerud, P. O. Toxic effects of brominated flame retardants in man and in wildlife. Environ. Int. 2003, 29, 841-853. (6) Sellstro¨m, U. Determination of some polybrominated flame retardants in biota, sediment and sewage sludge. Doctoral dissertation, University of Stockholm, Sweden, 1999. (7) Ratcliffe, D. The Peregrine Falcon; T&AD Poyser: London, 1993. (8) Pekarik, C.; Weseloh, D. V. Organochlorine contaminants in herring gull eggs from the Great Lakes, 1974-1995: change point regression analysis and short-term regression. Environ. Monit. Assess. 1998, 53, 77-115. (9) Arenal, C. A.; Halbrook, R. S.; Woodruff, M. J. European starling (Sturnus vulgaris): avian model and monitor of polychlorinated biphenyl contamination at a superfund site in Southern Illinois, USA. Environ. Toxicol. Chem. 2004, 23, 93-104. (10) Bishop, C. A.; Ng, P.; Mineau, P.; Quinn, J. S.; Struger, J. Effects of pesticide spraying on chick growth, behavior, and parental care in tree swallows (Tachycineta bicolor) nesting in an apple orchard in Ontario, Canada. Environ. Toxicol. Chem. 2000, 19, 2286-2297. (11) Custer, C. M.; Custer, T. W.; Dummer, P. M.; Munney, K. L. Exposure and effects of chemical contaminants on tree swallows nesting along the Housatonic River, Berkshire County, Massachusetts, USA, 1998-2000. Environ. Toxicol. Chem. 2003, 22, 1605-1621. (12) Arenal, C. A.; Halbrook, R. S. PCB and heavy metal contamination and effects in European Starlings (Sturnus vulgaris) at a superfund site. Bull. Environ. Contam. Toxicol. 1997, 58, 254262. (13) Janssens, E.; Dauwe, T.; Bervoets, L.; Eens, M. Heavy metals and selenium in feathers of great tits (Parus major) along a pollution gradient. Environ. Toxicol. Chem. 2001, 20, 28152820. (14) Dauwe, T.; Chu, S. G.; Covaci, A.; Schepens, P.; Eens, M. Great tit (Parus major) nestlings as biomonitors of organochlorine pollution. Arch. Environ. Contam. Toxicol. 2003, 44, 89-96. (15) Winter, S.; Streit, B. Organochlorine compounds in a three-step terrestrial food chain. Chemosphere 1992, 24, 1765-1774. (16) Smits, J. E. G.; Bortolotti, G. R.; Sebastian, M.; Ciborowski, J. J. H. Spatial, temporal, and dietary determinants of organic contaminants in nestling tree swallows in Point Pelee National Park, Ontario, Canada. Environ. Toxicol. Chem. 2005, 24, 31593165. (17) Nichols, J. W.; Larsen, C. P.; Mcdonald, M. E.; Niemi, G. J.; Ankley, G. T. Bioenergetics-based model for accumulation of polychlorinated-biphenyls by nestling tree swallows, Tachycineta bicolor. Environ. Sci. Technol. 1995, 29, 604-612. (18) Echols, K. R.; Tillitt, D. E.; Nichols, J. W.; Secord, A. L.; McCarty, J. P. Accumulation of PCB congeners in nestling tree swallows (Tachycineta bicolor) on the Hudson River, New York. Environ. Sci. Technol. 2004, 38, 6240-6246. (19) Van Den Steen, E.; Dauwe, T.; Covaci, A.; Jaspers, V. L. B.; Pinxten, R.; Eens, M. Within- and among-clutch variation of organohalogenated contaminants in eggs of great tits (Parus major). Environ. Pollut. in press. (20) Cramp, S.; Perrins, C. M. Handbook of the Birds of Europe, the Middle East and North Africa. The Birds of the Western Palearctic. Volume VII. Flycatcher to Shrikes; Oxford University Press: Oxford, 1993; pp 255-281. (21) Voorspoels, S.; Covaci, A.; Schepens, P. Polybrominated diphenyl ethers in marine species from the Belgian North Sea and the Western Scheldt Estuary: levels, profiles, and distribution. Environ. Sci. Technol. 2003, 37, 4348-4357. (22) Koplin, J. R.; Collopy, M. W.; Bammann, A. R.; Levenson, H. Energetics of 2 wintering raptors. Auk 1980, 97, 795-806. (23) Graber, J. W.; Graber, R. R. Feeding rates of warblers in spring. Condor 1983, 85, 139-150. (24) Chen, Y.-Z.; Lin, L.; Wang, C.-W.; Yeh, C.-C.; Hwang, S.-Y. Response of two Pieris (Lepidoptera: Pieridae) species to fertilization of a host plant. Zool. Stud. 2004, 43, 778-786. (25) Drouillard, K. G.; Norstrom, R. J. Quantifying maternal and dietary sources of 2,2′,4,4′,5,5′-hexachlorobiphenyl deposited in eggs of the ring dove (Streptopelia risoria). Environ. Toxicol. Chem. 2001, 20, 561-567. (26) Nichols, J. W.; Echols, K. R.; Tillitt, D. E.; Secord, A. L.; McCarty, J. P. Bioenergetics-based modeling of individual PCB congeners in nestling tree swallows from two contaminated sites on the Upper Hudson River, New York. Environ. Sci. Technol. 2004, 38, 6234-6239. (27) Dauwe, T.; Jaspers, V.; Covaci, A.; Schepens, P.; Eens, M. Feathers as a nondestructive biomonitor for persistent organic pollutants. Environ. Toxicol. Chem. 2005, 24, 442-449.
(28) Drouillard, K. G.; Norstrom, R. J. Dietary absorption efficiencies and toxicokinetics of polychlorinated biphenyls in ring doves following exposure to Aroclor (R) mixtures. Environ. Toxicol. Chem. 2000, 19, 2707-2714. (29) She, J.; Holden, A.; Tanner, M.; Sharp, M.; Adelsbach, T.; Hooper, K. Highest PBDE levels (max 63 ppm) yet found in biota measured in seabird eggs from San Francisco Bay. Organohalogen Compd. 2004, 66, 3889-3894. (30) Verreault, J.; Gabrielsen, G. V.; Chu, S. G.; Muir, D. C. G.; Andersen, M.; Hamaed, A.; Letcher, R. J. Flame retardants and methoxylated and hydroxylated polybrominated diphenyl ethers in two Norwegian Arctic top predators: Glaucous gulls and polar bears. Environ. Sci. Technol. 2005, 39, 60216028. (31) Jaspers, V. L. B.; Covaci, A.; Voorspoels, S.; Dauwe, T.; Eens, M.; Schepens, P. Brominated flame retardants and organochlorine pollutants in aquatic and terrestrial predatory birds of Belgium: levels, patterns, tissue distribution and condition factors. Environ. Pollut. 2006, 139, 340-352.
(32) Herzke, D.; Berger, U.; Kallenborn, R.; Nygård, T.; Vetter, W. Brominated flame retardants and other organobromines in Norwegian predatory bird eggs. Chemosphere 2005, 61, 441449. (33) Voorspoels, S.; Covaci, A.; Lepom, P.; Jaspers, V. L. B.; Schepens, P. Levels and distribution of polybrominated diphenyl ethers in various tissues of birds of prey. Environ. Pollut. in press. (34) Hebert, C. E. Winter severity affects migration and contaminant accumulation in northern Great Lakes Herring Gulls. Ecol. Appl. 1998, 8, 669-679. (35) Kunisue, T.; Watanabe, M.; Subramanian, A.; Sethuraman, A.; Titenko, A. M.; Qui, V.; Prudente, M.; Tanabe, S. Accumulation features of persistent organochlorines in resident and migratory birds from Asia. Environ. Pollut. 2003, 125, 157-172.
Received for review March 29, 2006. Revised manuscript received June 12, 2006. Accepted June 13, 2006. ES060747A
VOL. 40, NO. 17, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
5303
