Environ. Sci. Technol. 2006, 40, 7938-7943
Polyaromatic Hydrocarbon and PAH Metabolite Burdens in Oiled Common Guillemots (Uria aalge) Stranded on the East Coast of England (2001-2002) G E R A M . T R O I S I , * ,† S T E V E B E X T O N , ‡ AND IAN ROBINSON§ School of Engineering and Design, Brunel University, Kingston Lane, Uxbridge, Middlesex, UB8 3PH, U.K., Norfolk Wildlife Hospital (RSPCA), Station Road, East Winch, King’s Lynn, Norfolk, PE32 1NR, U.K., and Emergency Relief Program, International Federation for Animal Welfare, 31 Workshop Road, South Yarmouth, Massachusetts 02664
Aside from the physical effects of oiling (e.g., hypothermia, dehydration, emaciation), chronic toxicity of polycyclic aromatic hydrocarbons (PAHs) contamination is an important factor influencing long-term recovery of oiled sea birds following an oil spill. Monitoring PAH exposure can help identify populations at risk from toxic effects of PAHs for further study and/or protection. This is the first study to quantify PAH and metabolite tissue burdens in sea birds directly oiled following oil spills. PAHs and hydroxylated PAHs were quantified in liver samples from oiled Common Guillemots (Uria aalge) stranded along the East Coast of England using gas chromatography-mass spectroscopy (GC-MS). Mean parent and metabolite PAH concentrations were 0.25 ( 0.09 (range 0.04-0.97) and 0.52 ( 0.14 (range 0.05-1.48) µg/g (wet wt.), respectively. The main source of PAH exposure was via ingestion of crude oil during preening, resulting in PAH uptake and tissue contamination beyond levels expected from exposure via the food chain. PAH composition corresponded with number of benzene rings in each compound and was typical of contamination from petrogenic sources; pentacyclic < tri- and tetracyclic < tricyclic < dicyclic PAHs. The occurrence of PAH metabolites detected in liver samples also provided evidence of the presence and stereoselectivity of hepatic microsomal CYP1A1 in common guillemots.
Introduction Releases of petroleum to the marine environment are mainly from incidental discharges from day to day transport and refining activities, industrial and municipal discharges, disposal of waste oil and diesel (e.g., contaminated ballast from oil tankers, contaminated oil-rig brines), rivers, and urban runoff. Tanker accidents and other non-routine releases of oil and diesels are also other important sources of marine oil pollution. Consequently, petroleum components such as polycyclic aromatic hydrocarbons (PAHs) and * Corresponding author phone: +44 1895 266 958; fax: +44 1895 256 392; e-mail:
[email protected]. † Brunel University. ‡ Norfolk Wildlife Hospital (RSPCA). § International Federation for Animal Welfare. 7938
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ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 40, NO. 24, 2006
aliphatic hydrocarbons are now ubiquitous marine pollutants. Sea birds, fish, and aquatic mammals, especially, become significantly oiled within minutes of contact with a crude oil or diesel spill. Mass mortalities of sea birds are a common feature of past and recent oil spill events, such as Exxon Valdez in 1989 (Prince William Sound, Alaska), Sea Empress in 1996 (Milford Haven, UK), and Prestige spill in 2002 (Galician Coast, Spain). Long-term population studies of over-winter survival of common guillemots (Uria aalge) in the Northern Atlantic, have shown that after controlling for other factors adult mortality is doubled by major oil pollution incidents (1). In addition to direct oiling following oil spills, sea birds are also exposed to the persistent and bioaccumulative components of petroleum, such as PAHs, via the marine food chain. However, sea birds coming into direct contact with oil, and/or ingesting crude oil through preening, tend to be significantly more exposed to PAHs and over a short time period. This can exacerbate the condition of oiled birds which become hypothermic soon after oiling when crude oil displaces insulating air between the feathers (2, 3). Oiled birds are usually extremely emaciated. Their fat reserves become rapidly exhausted because they are unable to dive and forage efficiently (4). The toxic effects of oiling in sea birds are many and varied. Observations from crude oil dosing experiments on sea birds include the following: adrenal and thyroid hypertrophy, bursa atrophy, weight loss, hemolytic anaemia, changes in salt gland weight and salt gland ATPase activity, gut damage, dehydration, kidney damage (renal necrosis and hemosiderin accumulation), liver damage (inflammation, hemosiderin accumulation, fatty liver), and morphological changes in lymphoid glands (5-11). Severe weight loss and, to a lesser degree, hemolytic anaemia, liver damage, foot problems, gut damage, and immunosuppression, have also been identified in field studies of wild guillemots and comparative studies of oiled versus unoiled rehabilitated sea birds (2-4, 12). Although much is known about the physical effects of external oiling on sea birds, there have been no studies of associated PAH contamination. In this study we investigated the pattern and concentration of parent and metabolite PAHs in liver samples collected from guillemots (Uria aalge) which had stranded in The Wash (Norfolk, East Coast of England) as a result of severe oiling (direct oiling by contact and/or ingestion) during the winter of 2001-2002. This served as a preliminary investigation of a small sample (n ) 10) of birds to provide an insight into the internal exposure profile of oiled sea birds and their capacity to detoxify PAHs.
Materials and Methods (a) Chemicals. Certified PAH reference standards were purchased from Sigma-Aldrich (10 parent compounds: acenaphthene, phenanthrene, acenaphthylene, pyrene, fluorene, chrysene, naphthalene, fluoranthene, and benzo(a)pyrene), and ChemService (internal standard, phenanthreneD12 diluted to 50 µg/mL in methanol and 6 PAH metabolites: 1-hydroxy-chrysene (1-OH--CHRY), 2-hydroxy-phenanthrene (2-OH-PHEN), 1-hydroxy-pyrene (1-OH-PYR), 2-hydroxy-fluorene (2-OH-FLUO), phenanthrene-9,10-diol (DiolPHEN), 1-hydroxy-BaP (1-OH-BaP). Solvents were highpurity glass distilled grade and purchased from Rathburn Chemicals. All other chemicals were purchased from SigmaAldrich Chemicals unless otherwise specified. All glassware was acid-washed and then hexane-washed prior to use to remove any interfering contaminants. 10.1021/es0601787 CCC: $33.50
2006 American Chemical Society Published on Web 11/16/2006
(b) Sampling. Liver samples (>5 g) from 10 adult common guillemots (Uria aalge) were provided by the RSPCA Norfolk Wildlife Hospital (Kings Lynn, Norfolk, UK) from their sample archive in July 2002. All of the birds in this study were found stranded between December 2001 and January 2002 in The Wash (Norfolk, East England) and had died from the effects of oiling (e.g., emaciation, hypothermia, secondary infections, dehydration) either prior to (stranded dead), or following, admission to the Norfolk Wildlife Hospital. Liver samples were taken as soon as possible after death (max. 12 h) with carcasses stored in a cold room until sampling. Samples from birds stranded dead only collected only if carcasses were fresh (
