Concentrations of Polycyclic Aromatic Hydrocarbons (PAHs) in the

Nov 3, 2009 - The eggs of several marine species in Britain and The Netherlands have been found to contain low residues of PAHs that, in concentration...
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Environ. Sci. Technol. 2009 43, 9010–9015

Concentrations of Polycyclic Aromatic Hydrocarbons (PAHs) in the Eggs of Predatory Birds in Britain ´ R I A P E R E I R A , * ,† L E E A . W A L K E R , † M. GLO JULIAN WRIGHT,† JENNIFER BEST,‡ AND RICHARD F. SHORE† NERC Centre for Ecology and Hydrology, Lancaster Environment Centre, Library Avenue, Bailrigg, Lancaster, LA1 4AP, U.K., and Natural England, Northminster House, Peterborough, PE1 1UA, U.K.

Received June 19, 2009. Revised manuscript received September 30, 2009. Accepted October 14, 2009.

The eggs of gannets from two Scottish colonies (Ailsa Craig, Bass Rock) of golden eagles from the Hebrides and Highlands and of merlin eggs from the Scottish borders were analyzed for 52 PAHs, including 2-7 ring parent and alkylated PAHs. Phenanthrene was the most abundant PAH in gannet eggs from Ailsa Craig, and methylnaphthalenes predominated in the eggs from other locations and species. Most PAHs were detected in eggs but none were at likely embryotoxic concentrations. The sum concentrations for all the PAHs analyzed (3.1-5.7 ng g-1 wet wt.) and for the U.S. EPA 16 priority PAHs (2.0-4.3 ng g-1 wet wt.) did not differ significantly betweenspeciesorlocations.Thisuniform,low-levelaccumulation suggests background exposure to diffuse sources. PCA indicated that 3 ring parent and alkylated PAHs predominated in the eggs of merlins and gannets from Ailsa Craig and Hebridean golden eagles; other eggs had a more mixed profile. Source signature diagnostics largely suggested a petrogenic origin for the PAHs in the merlin eggs that we analyzed but otherwise gave equivocal results and further work is needed to determine which diagnostics can be successfully applied to PAHs in eggs.

Introduction Polycyclic aromatic hydrocarbons form a large group of organic contaminants that range in their structure from two to seven rings with (alkylated) or without (parent) alkyl groups. Releases are predominantly to the atmosphere and may be from point or diffuse sources. PAHs are ubiquitous in the environment because they originate from both natural (forest fires, natural oil seeps, volcanoes, diagenesis of sedimented organic matter) and anthropogenic (combustion of fossil fuels, accidental oil spills, waste incineration, coke and asphalt production) sources (1, 2). Depending on their mechanism of formation, PAHs can be designated as pyrogenic (produced during incomplete combustion of organic matter at high temperatures), petrogenic (produced at relatively low temperatures over geological time scales * Corresponding author tel: +44 (0)1524 595963; fax: +44 (0)1524 61536; e-mail: [email protected]. † NERC Centre for Ecology and Hydrology, Lancaster Environment Centre. ‡ Natural England. 9010

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(for example petroleum and other fossil fuels)), and diagenetic (arising from rapid formation from biogenic precursors such as plant terpenes) (3). Some PAHs have been widely studied because they are well-known human carcinogens and mutagens (4, 5), and are listed as priority pollutants by the World Health Organisation, the European Economic Community, and the U.S. Environmental Protection Agency (U.S. EPA). Although PAHs are likewise potentially toxic to other vertebrates (6-10), there are relatively few data on the exposure of wild vertebrates. This is partly due to the fact that vertebrates (and many invertebrates) have well developed mixed-function oxidases that enable them to metabolize efficiently and excrete some PAHs, and so tissue residues are often not detectable (11-14). However, large aromatic hydrocarbons remain difficult to metabolize and excrete (12-15). The presence of detectable residues and metabolites in the body tissues and eggs of some biota (10) indicates that accumulation does occur and is mostly associated with lipid content (10, 16). Comparison of PAH residues indicated that concentrations in bird eggs can be some 2 or 3 orders of magnitude higher than in livers (17). Relatively high levels of accumulation are one characteristic that may mean eggs can be potentially good biomonitors of PAH contamination in the environment. PAHs are also highly embryotoxic to birds, as demonstrated by laboratory studies in which individual compounds, mixtures of PAHs, or oil have been injected into eggs or topically applied to the shell (8, 9, 18-20). Despite this, there is generally little information on concentrations in bird eggs. Most data relate to coastal nesting species and seabirds (17, 21-23). The eggs of several marine species in Britain and The Netherlands have been found to contain low residues of PAHs that, in concentrations, can reduce embryo survival or cause cellular and developmental abnormalities (23, 24). The Predatory Bird Monitoring Scheme (PBMS) is a longterm, UK-wide chemical surveillance scheme in which temporal and spatial variation in assimilation of contaminants by predatory birds is monitored by measuring residues in the livers and eggs of various species (25). To date, PAH concentrations in eggs collected by the PBMS have not been quantified but such measurements would provide some of the first data on PAH assimilation by predatory birds in Britain, and in particular for terrestrial raptors. The overall aim of this work was to conduct a pilot study to ascertain whether there is evidence of accumulation of PAHs in the eggs of predatory birds in Britain from both terrestrial and marine environments. If so, eggs could be used as biomonitors of PAHs in the future. This involved quantifying and comparing PAH profiles and concentrations in the eggs of merlins (Falco columbarius) which feed mostly on terrestrial small birds, golden eagles (Aquila chrysaetos) from Scotland which feed on carrion, medium-sized mammals, and coastal seabirds, and Northern gannets (Morus bassanus) which prey on marine fish. PAH signatures and specific ratios have been used to identify major sources of PAH contamination in sediments and some biota (26, 27), but, as far as we are aware, this approach has rarely been applied to PAHs in birds (28). Pyrogenic sources are characterized by high abundance of high molecular weight parent (parPAHs) compounds and a low proportion of alkylated PAHs (alkPAHs); petrogenic sources are characterized by high concentrations of alkPAHs and low molecular weight PAHs (27). Ratios of the concentrations of specific PAHs, namely phenanthrene/anthracene (P/AN) and fluoranthene/pyrene (F/PY), are also widely used 10.1021/es901805e CCC: $40.75

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ND-0.313 ND-0.254 ND-0.236 ND-0.186 ND-0.200 ND-0.215 ND-0.215 ND-0.638 ND-0.207 ND-0.235 ND-0.192

0.046 0.041 0.024b 0.031 0.029 0.054 0.018b 0.058b 0.019b 0.021b 0.019b

0.027 0.048b 0.005b 0.035b 0.009 0.034 0.002b 0.005b 0.012 ND ND

0.057

0.836 0.469 0.208b ND 0.287 0.243 2.148 0.645 0.038 0.116 0.375 0.016 0.251 0.016 0.030b 0.006 0.039 0.015 0.017 0.047 0.108 0.007

mean

ND-0.166 ND-0.411 ND-0.018 ND-0.345 ND-0.056 ND-0.125 ND-0.009 ND-0.030 ND-0.082 ND ND

ND-0.298

ND-2.329 ND-1.086 ND-1.873 ND ND-0.862 ND-1.236 ND-6.392 ND-2.316 ND-0.336 ND-0.342 ND-0.623 ND-0.060 ND-0.748 ND-0.060 ND-0.129 ND-0.030 0.012-0.159 ND-0.053 0.007-0.079 ND-0.222 ND-0.323 ND-0.045

min-max

gannets: Ailsa Craig (10 eggs)

Less than half of the samples had detectable values.

ND-1.068

0.156

b

ND-5.380 ND-1.504 ND-0.783 ND-0.436 ND-1.052 ND-0.961 ND-2.345 ND-0.256 ND-0.328 ND-0.250 ND-0.557 ND-0.178 ND-0.374 ND-0.178 ND-0.236 ND-0.236 0.009-0.175 0.006-0.809 0.004-0.305 ND-0.772 ND-0.533 ND-0.289

min-max

0.595 0.426 0.158b 0.063b 0.260 0.351 0.367 0.094 0.039 0.060 0.314 0.022 0.119b 0.022b 0.046b 0.028b 0.050 0.089 0.044 0.112 0.107 0.027

ND: below detection limit.

C1-naphthalenes C2-naphthalenes C3-naphthalenes acenaphthylene acenaphthene fluorene phenanthrene C1- phenanthrenes C2-phenanthrenes anthracene fluoranthene C1-fluoranthene pyrene C1-pyrene benzo[a]fluorine benzo[b]fluorine benzo[ghi]fluoranthene benzo[c]phenanthrene cyclopenta[cd]pyrene benz[a]anthracene chrysene C1-chrysene benzo[b and j & k]fluoranthene benzo[e]pyrene benzo[a]pyrene perylene ideno[1,2,3-cd]pyrene dibenz[ah]anthracene benzo[ghi]perylene anthanthrene dibenzo[a,i]pyrene coronene dibenzo[a,e]pyrene dibenzo[a,h]pyrene

mean

gannets: Bass Rock (11 eggs)

ND-2.245 ND-1.093 ND-3.004 ND ND-2.245 ND-0.376 ND-3.568 ND-0.329 ND-0.056 ND-0.145 ND ND

0.182b 0.501b ND 0.382b 0.063b 0.606 0.055 0.009b 0.024b ND ND

ND-2.818 0.083-0.414 ND-ND ND ND-0.222 ND-0.364 ND-0.545 ND-0.154 ND-0.017 ND-0.055 ND-0.719 ND-0.059 ND-0.808 ND-0.059 ND-0.192 ND-0.025 0.010-0.863 0.004-0.208 0.005-0.198 0.013-1.147 0.030-1.894 ND-0.102

min-max

0.383

1.284 0.270 ND ND 0.099 0.171 0.091b 0.026b 0.007 0.035 0.317 0.024 0.193 0.024 0.052 0.004b 0.163 0.042 0.043 0.215 0.370 0.018

mean

golden eagles: Highlands (6 eggs)

0.018 0.020b ND 0.017b 0.007 0.069 0.010 ND 0.015 ND 0.002

0.033

0.596 0.297 0.070b ND 0.261 0.384 0.572 0.065b 0.010 0.065 0.324 0.023 0.262 0.023 0.017b ND 0.046 0.027 0.017 0.011b 0.041 0.003

b

mean

0.013-0.025 ND-0.061 ND-ND ND-0.050 0.003-0.011 0.053-0.080 0.006-0.017 ND-ND ND-0.023 ND-ND ND-0.007

0.025-0.049

ND-1.489 0.161-0.494 ND-0.210 ND-ND 0.230-0.319 0.282-0.453 ND-1.123 0.010-0.195 ND-0.022 0.045-0.088 0.214-0.427 ND-0.040 ND-0.571 ND-0.040 ND-0.050 ND-ND 0.023-0.068 0.007-0.064 ND-0.040 ND-0.034 ND-0.070 ND-0.007

min-max

golden eagles: Hebrides (3 eggs)

ND ND ND ND ND 0.013 ND ND ND ND ND

ND

1.919 0.261 ND 0.116 0.169 0.343 0.781 0.071 0.011 0.099 0.286 ND 0.100 0.008 ND 0.011b 0.016 0.005 0.011 0.024 0.066 0.002

mean

ND-ND ND-ND ND-ND ND-ND ND-ND ND-0.023 ND-ND ND-ND ND-ND ND-ND ND-ND

ND-ND

ND-3.974 ND-0.601 ND-ND ND-0.262 ND-0.397 ND-0.584 ND-1.382 ND-0.168 ND-0.036 0.043-0.141 0.116-0.406 ND-ND ND-0.228 ND-0.018 ND-ND ND-0.042 ND-0.035 ND-0.014 0.009-0.012 ND-0.049 0.029-0.119 ND-0.003

min-max

merlins (4 eggs)

TABLE 1. Mean PAH Concentrations (ng g-1 wet weight) in the Eggs of Gannets from Bass Rock and Ailsa Craig, Golden Eagles from Western Highlands and the Hebrides, and Merlins

as diagnostic tools (29, 30) because different ratios are obtained from pyrogenic and petrogenic processes. P/AN 1 generally indicate pyrogenic origin whereas P/AN >15 and FL/PY 0.05; Figure 1). The 16 Priority Pollutant PAHs (that form part of the U.S. EPA’s list of priority compounds) comprised at least 45% of the total PAHs (Figure 1) and their sum concentration also did not vary significantly between the

FIGURE 1. Mean (and standard deviation) sum of total and the 16 priority pollutant PAH concentrations in eggs of gannets from Bass Rock (Gt-BR) and Ailsa Craig (Gt-AC), golden eagles from the Highlands (Ge-HL) and Hebrides (GE-He), and merlins (M). different groups of eggs (F4,29 ) 0.28, P > 0.05; Figure 1). Concentrations of these 16 PAHs were similar to those measured previously in the eggs of coastal nesting birds (1.6-8.4 ng g-1 wet wt. (23)) but were at least an order of magnitude lower than the concentrations (21-461 ng g-1 wet wt.) in the peregrine falcon eggs collected after the Prestige oil spill (32). The general uniformity of the PAHs profile and the low amounts accumulated in the eggs suggests that the assimilation detected in the present study was likely to have been the result of exposure to background concentrations from diffuse sources. Toxicity. The most potent PAHs are those that bind to the Ah receptor and are additive in their toxicity (9). Concurrent exposure to a mixture of PAHs alone and/or in combination with other organic pollutants is therefore likely to enhance toxicity (34). While Toxic Equivalency Factors have been suggested for PAHs (35), these are not based on avian embryotoxicity end points and so were not extrapolated to the present study. However, it is possible to conduct a limited assessment of potential toxicity by comparing the residues we measured in eggs to experimentally derived adverse effect concentrations for single PAHs, although such assessment may underestimate potential embryotoxicity. The embryotoxicity of 24 PAHs was assessed by injecting them into chicken eggs. Benzo[k]fluoranthene, dibenz[a,h]anthracene, and benzo[a]anthracene were the most toxic with LD50 values of 14, 39, and 79 ng g-1 wet wt., respectively (8). Doses of approximately 36 ng g-1 wet wt. benzo[a]pyrene and 270 ng g-1 wet wt. chrysene both caused significant reduction in embryonic growth and increased incidence of abnormal chicks when applied externally to mallard (Anas platyrhynchos) eggs (19). In the present study, mean concentrations of all these compounds were greatest in gannet eggs from Bass Rock and maximum concentrations were

FIGURE 3. Phenanthrene/anthracene (P/AN) ratio versus the fluoranthene/pyrene (Fl/PY) ratio in eggs of gannets from Bass Rock (Gt-BR) and Ailsa Craig (Gt-AC), golden eagles from the Highlands (Ge-HL) and Hebrides (GE-He), and merlins (M). detected in the eggs of Highlands golden eagles (Table 1). However, even the maximum concentrations were at least 5-10 fold lower than the LD50 concentrations of the individual compounds. The concentrations of individual compounds in the eggs we analyzed, therefore, appear unlikely to be embryotoxic. Source Signature Diagnostics and PCA of PAH Profiles. Despite the similarity in sum PAH concentrations for the different groups of eggs, source signature diagnostics indicated there were some differences in PAH profile. Two source signature diagnostics suggested that the PAHs in the merlin eggs were mainly petrogenic in origin. Low molecular weight (LMW) three-ring parPAHs predominated (74.1%) (Figure 2) and occurred in significantly greater concentrations than high molecular weight (HMWs4 + 5 + 6 ring) PAHs (paired t test: t(3) ) 3.44, P < 0.05). Merlin eggs also had the highest percentage (54%) of alkPAHs of any of the eggs, although the difference between the summed alkPAHs and parPAHs concentrations was not statistically significant. However, the third diagnostic (P/AN and FL/PY ratios) did not indicate a petrogenic origin for the PAHs (Figure 3). Source signature diagnostics gave much more equivocal results for the other eggs. Concentrations of LMW 3-ring PAHs were significantly higher than those of HMW compounds in the eggs of golden eagles from the Hebrides (t(2) ) 18.0, P < 0.05; Figure 2), suggesting PAHs were of petrogenic origin. However, parPAHs, characteristic of pyrogenic origin, predominated (56%) over alkPAHs in these eggs while the P/AN and FL/PY ratios failed to characterize the PAHs (Figure 3). For the remaining groups of eggs, none of the diagnostics gave a clear PAH source signature. Overall, the general lack of success of these diagnostics is perhaps not surprising. Although PAHs from combustion or petroleum sources have

FIGURE 2. Contribution (%) of three (C3), four (C4), five (C5), six and seven (C6 and C7) ring PAHs to the sum of parent PAHs in eggs of gannets from Bass Rock (Gt-BR) and Ailsa Craig (Gt-AC), golden eagles from the Highlands (Ge-Hl) and Hebrides (GE-He), and merlins (M). VOL. 43, NO. 23, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 4. Scores (a) and loadings (b) of the two first principal components from a principal component analysis of the individual PAHs. specific signatures, they can undergo physical, chemical, and biological weathering in the environment. For example, most PAHs in sediments are degraded to some extent under aerobic conditions and there can also be selective anaerobic degradation of compounds such as phenanthrene (36). In addition, PAHs may also be biotransformed by the birds and their prey to more polar metabolites that can either be retained or excreted. We also used PCA to investigate the causes of the variation in PAH concentrations in the eggs. PC1 explained 27% and PC2 explained some 23% of the variance in the data (Figure 4). Gannets formed two clusters, with most of the Ailsa Craig eggs grouped on the positive side of PC1 and the Bass Rock eggs on the negative side (Figure 4a). The loadings plot (Figure 4b) suggested that the separation was driven petrogenic (3rings and alkPAHs) or pyrogenic (g4-rings) PAHs. The majority of the Ailsa Craig eggs were strongly influenced by petrogenic parent and alkPAHs whereas the position of most of the Bass Rock eggs in the PCA suggested a pyrogenic signature. Differences in PCB profiles and temporal trends have likewise been detected for the two colonies (37). Intercolony differences in contaminant (PAH and PCB) profiles may reflect differences between the North Sea and the Eastern Atlantic in source inputs and/or dietary differences between birds from the two colonies. PCA analysis of the golden eagle eggs also suggested spatial differences in PAH assimilation and/or metabolism. The eggs from Hebridean eagles were characterized by 3-ring parent 9014

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and alkPAHs, suggesting a petrogenic source, whereas eggs from Highland coastal eagles did not form a cluster, suggesting a mixed source for PAHs. This may reflect a diverse diet that includes seabirds as well as terrestrial mammals and birds (38). The PCA position of merlin eggs was largely governed by LMW parPAHs and alkPAHs (positive side of PC1; Figure 4). This suggests that merlins may be mostly exposed to and assimilate petrogenic PAHs, but the provenance of the merlin eggs in the present study was limited and it is not clear how far these results can be extrapolated to eggs from other locations. In conclusion, our study has demonstrated that eggs from birds of prey in Britain can contain a wide number of PAHs. There were differences between species and locations in the relative concentrations of individual PAHs, suggesting variation in exposure and/or capacity to metabolize PAHs, but concentrations of all individual compounds were low and unlikely to be embryotoxic. Sum PAH concentrations in eggs were also low and this was uniform across species and locations, suggesting that accumulated residues were due to exposure to background concentrations, presumably from diffuse sources. Given this, it might be expected that the PAHs in the eggs would be predominantly pyrogenic in origin, especially given pyrogenic PAHs are more persistent and less subject to microbial attack (22). It was unexpected, therefore, that the PAHs in the merlin and some other individual eggs had a largely petrogenic signature, and may indicate a greater availability of oil-derived PAHs in the environment

than hitherto realized. It is also possible that PAHs were assimilated into some eggs as a result of direct contact with oiled feathers on incubating birds and diet may not necessarily be the main exposure route. Further work is required, however, to determine the extent to which diagnostic source signatures can be applied with confidence to PAHs in eggs.

Acknowledgments The eggs were collected by licensed collectors for the Predatory Bird Monitoring Scheme (http://pbms.ceh.ac.uk) which is currently funded by Centre for Ecology & Hydrology (CEH), Natural England (NE), Environment Agency (EA), and Campaign for Responsible Rodenticide Use (CRRU).

Supporting Information Available Figure (S1) showing location of the gannets, golden eagles, and merlin eggs. This material is available free of charge via the Internet at http://pubs.acs.org.

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