Environ. Sci. Technol. 2007, 41, 8491–8497
Temporal Trends (1986–2004) of Organochlorines and Brominated Flame Retardants in Tawny Owl Eggs from Northern Europe J A N O . B U S T N E S , * ,† N I G E L G . Y O C C O Z , †,‡ GEORG BANGJORD,§ ANUSCHKA POLDER,| AND J A N N E C H E U . S K A A R E |,⊥ Norwegian Institute for Nature Research, The Polar Environmental Centre, N-9296 Tromsø, Norway, Biology Department, Faculty of Science, University of Tromsø, N-9037 Tromsø, Norway, Oddatunet, 7057 Jonsvatnet, Norway, Norwegian School of Veterinary Science, P.O. Box 8146 Dep., N-0033 Oslo, Norway, and National Veterinary Institute, P.O. Box 8156 Dep., N-0033 Oslo, Norway
Received June 28, 2007. Revised manuscript received September 12, 2007. Accepted September 24, 2007.
Eggs (n ) 139) from tawny owls (Strix aluco) were collected annually (1986–2004) in Central Norway and analyzed for organochlorines (OCs) and brominated flame retardants (BFRs). p,p′-DDE (2,2-bis(4-chlorophenyl)-1,1-dichloroethene) and polychlorinated biphenyls (PCBs) were the dominating contaminants (mean/median ) 2.7/1.7 and 2.9/1.6 µg/g, lipid weight [l.w.], respectively), comprising 90% of the contaminant burden. Other OCs (hexachlorobenzene [HCB], hexachlorocyclohexanes [HCHs], trans-nonachlor and oxychlordane) comprised less than 4% of the contaminant burden. Concentrations of OCs dropped 74–96% during the study period; p,p′-DDE, HCB, β-HCH, oxychlordane, and PCBs decreased rapidly in the early (1986–1989) study period (23–34% per year; mean ) 27.4%), but leveled off to less than 7% (mean ) 3.6%) in the late period (2001–2004). The decrease in p,p′-DDE concentrations leveled off in the early 1990s, possibly due to an early ban on the use of DDT. R-HCH showed the strongest decline (always >20% per year), while trans-nonachlor and γ-HCH dropped at a constant rate of 9% per year. Toxaphene made up less than 0.6% of the measured contaminants (mean/median ) 39/13 ng/ g, l.w.), and the concentrations of these compounds were lower in the late period compared to the early period, but not significant. BFRs, including hexabromocyclododecane (HBCD) and polybrominated diphenyl ethers (ΣPBDE: mean/median ) 182/ 85 ng/g, l.w.) made up about 3% of the measured contaminants. ΣPBDE declined significantly over the study period (62%). Most PBDE congeners declined: significantly for BDE-47 (80% reduction) and BDE-153 (50% reduction), but the patterns differed; i.e., congeners associated with PentaBDE mixtures * Corresponding author e-mail:
[email protected]; phone: +47 77 75 04 07; fax: +47 77 75 04 01. † Norwegian Institute for Nature Research, The Polar Environmental Centre. ‡ University of Tromsø. § Oddatunet. | Norwegian School of Veterinary Science. ⊥ National Veterinary Institute. 10.1021/es071581w CCC: $37.00
Published on Web 11/15/2007
2007 American Chemical Society
showed a rapid annual decline early (22–26%) and a slower decline late in the study period (6–12%), while the PBDEs associated with OctaBDE declined at a constant rate (1–4%). This may result from a larger reduction in the use of PentaBDE compared to other PBDE products in Europe.
Introduction Long-term monitoring of top predators, especially in aquatic ecosystems, has shown that the concentrations of many pollutants, notably organochlorines (OCs) such as polychlorinated biphenyls (PCBs) and organochlorine pesticides, have decreased as a result of bans in the 1970s and early 1980s (1–4). In terrestrial top predators, the picture is less consistent. For example, in predatory birds, the few long-term data series available have shown decreasing concentrations for some OCs, such as the DDT metabolite p,p′-DDE (2,2-bis(4chlorophenyl)-1,1-dichloroethene) ethylene), but there have been no consistent temporal trends for PCBs (5–7). Polybrominated diphenyl ethers (PBDEs) are a class of brominated flame retardants (BRFs) with widespread industrial and commercial applications. As for many OCs, PBDEs are distributed globally, environmentally persistent, and bioaccumulative, and in contrast to the OCs their levels have increased in biota (8–10) and humans (11, 12) since the 1970s. Moreover, some of the highest concentrations of PBDEs have been found in terrestrial predatory birds (13–16). However, since the discovery of these compounds in biota in the 1980s (17) the use of some BRFs, notably PentaBDE products, has declined in Europe, and since 2004 both OctaBDE and PentaBDE formulations have been banned in the European Union (overview in ref (18)). Reduced use of these products has led to declines of PBDEs in marine birds in the Baltic Sea (18), and in freshwater fish in southern Sweden (19). However, so far no declines have, to our knowledge, been found in terrestrial birds. Relatively little is known about temporal trends of organic pollutants in terrestrial ecosystems in northern regions, and in this study we quantified the pattern of temporal change (1986–2004) of OCs (PCBs and different pesticides) and BRFs (hexabromocyclodecane [HBCD] and PBDEs) in the tawny owl (Strix aluco) at its northern distribution limit in Central Norway. Owls are suitable for monitoring organic pollutants in terrestrial ecosystems, since they are top predators and accumulate various pollutants (20, 21). Although the main diet of tawny owls is ground-dwelling voles, they also feed on passerine birds (22). However, since tawny owls are territorial (22) and lay their eggs in early April (23), before migrating birds start to arrive, the concentrations of different contaminants in their eggs will mostly reflect the pollution in local environments.
Materials and Methods The study was carried out in the area surrounding the city of Trondheim (63.42° N, 10.23° E) in Sør-Trøndelag County, Central Norway, between 1986 and 2004. Sample Collection. More than 100 tawny owl nest boxes were checked annually in the first half of May, and all nonhatching eggs were collected. Eggs were frozen shortly after collection. The sample consisted of one egg per female per year (n ) 139), but eggs were collected from 15 individuals (known from banding) in more than one year (between two and four eggs per individual, and from one to seven years between eggs). However, variance component analyses for these individuals for ΣPCB, p,p′-DDE, ΣPBDE, and HCB showed that >72% of the sample variation was explained by VOL. 41, NO. 24, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 1. Concentrations (ng/g, lipid weight) and Summary Statistics for Different Organic Pollutants in Tawny Owl Eggs from Central Norway Collected between 1986 and 2004 (Detection Limits Are Shown for Compounds with Values below the Limits (Min); Mean Values Are Also Given for the Early (1986–1989; 1986–1995 for Toxaphenes) and Late Sampling Periods (2001–2004; 1998–2004 for Toxaphenes)) whole sample
n
detection limit % detected wet weight
p,p′-DDE HCB R-HCH β-HCH γ-HCH trans-nonachlor oxychlordane
139 139 139 139 139 139 139
100 100 92.8 74.1 54.7 94.2 99.3
PCBs CB-101 CB-99 CB-118 CB-153 CB-138 CB-187 CB-180 CB-170 CB-194 ΣPCB ΣOC
139 139 139 139 139 139 139 139 139 139 139
76.3 98.6 99.3 100 100 100 100 100 100 100 100
0.42 0.42 0.40
40 40 40 40 40 40
95.0 35.0 42.5 85.0 7.5 97.5
0.03 0.03 0.01 0.04 0.20
Toxaphenes CHB-26 CHB-40 CHB-41 CHB-50 CHB-62 ΣCHB
Brominated flame retardants BDE-28 139 BDE-47 139 BDE-100 139 BDE-99 139 BDE-154 139 BDE-153 139 BDE-209 137 ΣPBDE 137 HBCD 139
30.9 100 100 100 100 100 63.5 100 24.5
0.08 0.21 0.11 0.15 0.20
0.01
0.03 0.03
mean
median
9
min
max
2743 1666 4261 236 43288 111.7 72.0 133.7 18.0 1264 8.51 3.37 12.86 0.45 98.1 9.58 5.36 14.04 1.07 108.1 16.3 1.69 62.7 0.27 446.2 20.8 10.9 33.9 0.66 297.4 76.2 40.6 152.0 5.88 1646 16.4 94.7 94.8 1001 488.3 242.9 654.6 188.6 106.0 2888 5873
9.33 41.1 44.8 544.5 274.1 163.2 337.2 91.4 54.0 1581 3441
20.73 0.94 0.64 13.35 3.14 38.8
0.14 37.1 20.6 67.2 6.81 46.7 2.11 181.9 2.21
6.98 0.18 0.10 3.19 1.49 13.0
0.08 15.8 10.2 29.4 3.16 20.0 0.53 86.0 0.22
variation between individuals. Thus the effect of repeated samplings was negligible. The number of eggs per year varied from one (1990) to 18 (2004), except for 1988 when no eggs were found. Chemical Analyses. The chemical analyses were carried out at the Laboratory of Environmental Toxicology at the Norwegian School of Veterinary Science using gas chromatography (GC) with mass spectrometry (MS; Agilent 5973 Network, Agilent Technologies, PA), and/or electron capture detection (ECD) (GC; Agilent 6890 Series gas chromatography system). All details about the analyses have been described elsewhere (24–26). The laboratory is accredited for analyzing the components reported here according to the requirements of NS-EN ISO/IEC 17025(2005). The analytical quality of the laboratory has been approved in several intercalibration tests. As standard procedure, recoveries of spiked samples, blanks, and reference samples were analyzed in each series and acceptable results were achieved. Hence, a minimum of 80% of the recoveries were (20% within the target value and the results of the reference sample were within two times standard deviation of the established value. The following PCB-congeners were determined: CB-101, -99, -118, -153, 8492
std dev
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24.2 189.5 211.3 1661 746.3 301.4 1226 377.7 195.0 4766 9029 58.07 1.80 1.32 35.46 5.74 98.5
0.26 86.4 56.8 227.1 18.6 112.2 7.95 472.9 4.95
1.36 3.13 8.51 92.0 46.0 24.9 45.2 12.3 7.26 249.4 583.9 0.25 0.10 0.05 0.23 0.65 3.16
0.01 1.31 0.66 2.55 0.30 2.5 0.13 9.8 0.04
133.6 1498 2174 15353 6864 2639 11447 3605 1710 44196 90836 359.34 9.20 6.36 198.94 29.80 598.5
percentof compounds
mean 1986-1989 (n ) 12)
mean 2001-2004 (n ) 42)
of ΣOC 48.0 2.4 0.2 0.2 0.01 0.4 1.4
9064 290.9 39.1 36.4 16.4 69.1 265.4
1700 72.0 1.76 4.0 15.3 8.92 36.4
0.3 1.4 1.6 16.3 8.3 4.7 10.0 2.8 1.7 47.1
48.4 7.42 310.9 37 254.3 42 3338 431.3 1616 219.1 695.8 141.7 2498 238.5 713.5 69.2 403.2 37.1 9878 1223 19659 3063 1986–1995 1998–2004 of ΣCHB (n ) 22) (n ) 18) 54.0 31.3 7.76 3.6 1.3 0.5 1.8 0.92 0.29 26.6 20.8 4.2 14.1 4.5 1.5 58.9 14.2
of ΣPBDE 2.94 0.2 946.4 20.2 651.8 11.8 2644 35.1 202.8 3.7 896.4 27.4 90.60 1.6 5273 36.5
1986–1995 1998–2004 (n ) 12) (n ) 42) 0.13 0.10 115.0 19.8 73.4 12.6 278.6 34 21.2 4.12 106.9 21.9 1.25 1.28 596.5 93.7 6.35 2.07
-138, -187, -180, -170, -194. Other organochlorines analyzed were hexachlorobenzene (HCB), trans-nonachlor, oxychlordane, p,p′-DDE, and R-, β-, and γ-hexachlorocyclohexane (HCH). In addition we analyzed for the following toxaphene congeners: CHB-26, -40, -41, -50, and -62. PBDE congeners analyzed included BDE-28, -47, -99, -100, -153, -154, and -209, in addition to total HBCD. BDE-183 concentrations were low and the blanks showed concentrations in the same range, and it was therefore excluded. The analytical standards were provided by Cambridge Isotope Laboratories, Inc., Andover, MA (OC-pesticides, PCBs, BFRs); Ultra Scientific, RI (PCBs); Supelco, Bellefonte, PAA (OC-pesticides, PCBs); and LGC Promochem, Wesel, Germany (toxaphenes). Concentrations of all compounds were measured in all eggs, except BDE-209 which was measured in 138 eggs, and toxaphene which was measured in 40 eggs. In addition, one extreme value was removed for BDE-209 since its level was 135 times higher than the mean of the rest sample (266.7 vs 1.96 ng/g, lipid weight). The detection limit for BDE-209 was increased due to findings of low PBDE concentrations in the procedural blanks.
TABLE 2. Results of Additive Models (See Materials and Methods) for the Decline of Different Organic Pollutants in Tawny Owl Eggs between 1986 and 2004 (n = 139 except for ΣPBDE and BDE-209: n = 137) intercept
standard error
effective model degrees of freedom
F
P value
P value for linear model
p,p′-DDE HCB R-HCH β-HCH γ-HCH trans-nonachlor oxychlordane
7.460 4.391 1.472 1.663 0.782 2.398 3.808
0.069 0.054 0.050 0.067 0.121 0.083 0.066
3.141 4.450 5.285 4.702 1.000 1.000 4.202
4.09 5.84 41.29 11.82 16.41 36.42 6.00
