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ArticleJune 11, 2015

PAH Exposure in Gulf of Mexico Demersal Fishes, Post-Deepwater Horizon
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Cite this: Environ. Sci. Technol. 2015, 49, 14, 8786–8795

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https://doi.org/10.1021/acs.est.5b01870

Published June 11, 2015

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Abstract

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Following the 2010 Deepwater Horizon (DWH) blowout, we surveyed offshore demersal fishes in the northern Gulf of Mexico (GoM) in 2011–2013, to assess polycyclic aromatic hydrocarbon (PAH) exposure. Biliary PAH metabolites were estimated in 271 samples of golden tilefish (Lopholatilus chamaeleonticeps), king snake eel (Ophichthus rex), and red snapper (Lutjanus campechanus), using high performance liquid chromatography with fluorescence detection. Mean concentration of naphthalene metabolites in golden tilefish (240 μg g^–1) was significantly higher (p = 0.001) than in red snapper (61 μg g^–1) or king snake eel (38 μg g^–1). Biliary naphthalene metabolite concentration decreased over the study period in red snapper (58%) and king snake eel (37%), indicating likely episodic exposure, while concentrations were persistently high in golden tilefish. Naphthalene metabolite levels measured in golden tilefish are among the highest concentrations measured in fishes globally, while concentrations for red snapper and king snake eel are similar to pre-DWH levels measured in GoM species. In contrast, concentrations of benzo[a]pyrene metabolites were similar for all three species (p = 0.265, mean 220 ng g^–1) and relatively low when compared to GoM, global data and previous oil spills. These data support previous findings that fish life history and physiology play significant roles in exposure and uptake of PAH pollution.

Subjects

Introduction

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The Deepwater Horizon (DWH) blowout in the Gulf of Mexico (GoM) released 4.9 million barrels of crude oil between April 20th and July 15th, 2010. (1) Through multiple mechanisms, 4–31% of the oil residue settled on the northern GoM seafloor and its effects are apparent in sediment cores taken at sites polluted by the spill with negative impacts on the benthos. (2-5) Given the persistence of DWH oil in the environment, there is a need to understand the interactions with, and impacts on fish and other biota, particularly demersal fishes living in contact with sediments that may contain residual DWH oil. (2, 6-8)

Polycyclic aromatic hydrocarbons (PAHs) are considered the most toxic component of crude oil to marine life and are ubiquitous pollutants in the marine environment. (9, 10) Hydrocarbon analysis of DWH oil collected from the wellhead documented 3.8–4.0% PAHs by weight. (11, 12) With 4.9 million barrels of oil released during the DWH blowout, there was a large episodic pulse of PAHs associated with DWH into the GoM in 2010, with the potential to negatively impact fishes. Exposure to PAHs has been linked with a variety of sublethal effects in fish, including DNA damage, hepatic lesions and neoplasia, epidermal lesions, immunosuppression, cardiotoxicity, reduced adult fitness, altered and reduced growth, “toxicant-induced starvation”, disrupted cell membranes, gill abnormalities, osmoregulatory imbalance, endocrine disruption, decreased fecundity and reduced survival to maturity. (10, 13-17)

Routes of exposure to PAHs in demersal fishes include ingestion, ventilation over the gills and dermal uptake and may act simultaneously. (10, 18, 19) However, the relative importance of each route of exposure will change with physicochemical properties of each PAH, such as the octanol–water partition coefficient (K_ow). (20) Direct exposure to PAH-contaminated sediment and a diet of benthic prey is suspected to be an important source of exposure for demersal organisms. (21-24) Following uptake, the hepato-biliary system in fishes works to metabolize and eliminate PAHs. (25) The metabolites are accumulated in the bile which is stored in the gall bladder. In fish, metabolism rapidly converts up to 99% of PAH molecules into a more hydrophilic PAH metabolite leading to rapid excretion. Therefore, the concentration of parent PAHs in routinely monitored tissues, such as muscle and liver, often reveal only trace levels of contamination and are not necessarily good quantitative indicators of PAH exposure. (20, 26-30) The presence of biliary PAH metabolites represents an early marker of relatively short-term exposure to PAHs from all routes of exposure and has been associated with known sublethal effects in fish. (22, 28, 31, 32)

We studied three demersal fish species, the burrow-forming golden tilefish (Lopholatilus chamaeleonticeps), the mud-dwelling king snake eel (Ophichthus rex) and the reef fish, red snapper (Lutjanus campechanus). These species represent a gradient of likely sediment associations, with golden tilefish being heavily associated with sediments, king snake eel likely being moderately/heavily associated with the sediments, and red snapper being more distantly associated with sediments. (33-35) Studying differential PAH exposure between fish with varying levels of association with the sediment, including fishes that ingest sediment, has shown that the level of direct contact with contaminated sediment leads to differential body burdens of PAHs. (36)

Golden tilefish are demersal, nonmigratory and relatively long-lived fish that are commercially important in the GoM. (37-39) Golden tilefish have been observed living in a variety of shelter habitats, however, their primary habitat is a large funnel-shaped burrow. (38, 40) Living in depositional environments, the filling-in of a burrow is rapid, therefore, substantial maintenance of a burrow is required, consequently, golden tilefish frequently bioturbate sediments with their mouths and bodies. (34, 37, 40) This incidental sediment ingestion could potentially be a key route of exposure to PAH pollution for the species. In addition, golden tilefish are a species of interest due to the highest frequency of external skin lesions (7%), observed during a 2011 disease survey. (13) While cause and effect have not been established, it has neither been rejected. (13)

Little information is available about king snake eel life history. They are described as “mud eels” and “obligate mud dwellers” that are associated with soft-bottom habitat and are often concentrated near oil rigs. (35, 41) The limited literature does not suggest king snake eel form permanent burrows comparable to those of golden tilefish but they may burrow into sediments to hide or to search for food as is similar to the behavior of other Ophichthid eels. (42) Additionally, 82% of king snake eel habitat overlaps with the area that received some oil following DWH blowout, making it a species of high interest relative to oil pollution effects. (43) Red snapper are a commercially and recreationally important demersal reef fish associated more with vertical structure (e.g., natural and artificial reefs, offshore oil infrastructure) than the bottom sediments. (33, 44) All three study species are known to eat benthic prey during parts of their life cycle. (41, 44, 45)

The objective of this study was to estimate equivalent concentrations of metabolites of three common PAHs found in DWH crude oil, naphthalene (NPH), phenanthrene (PHN), and benzo[a]pyrene (BaP) as a biomarker of recent PAH exposure in three demersal fish species in the GoM following the DWH blowout and primarily designed to monitor relative concentrations over time. This research is part of a much larger study of fish disease and contamination in the GoM and ongoing analyses include quantifying PAHs and alkylated homologues in muscle and liver tissue, exposure studies to assess sublethal effects, sediment analysis, and risk assessment. Knowing the relative level of PAH exposure is important in understanding the link between PAH exposure, accumulation in edible tissues and resulting sublethal effects measured, particularly since PAHs exert their toxic effects after metabolism. (22, 46, 47) In addition, this study provides ample baseline data, which can be used to measure future environmental impacts in the GoM.

In three years following the DWH blowout (2011–2013), we collected bile from the three species to screen bile samples for relative concentrations of biliary PAH metabolites and fluorescent aromatic compounds (FACs). This study used a widely accepted semiquantitative method, high performance liquid chromatography with fluorescence detection (HPLC-F), to estimate concentrations of biliary PAH metabolites. (29, 48, 49) This methodology estimates the concentration of parent PAHs, their metabolites, alkylated derivatives of PAHs, their metabolites and N-, S-, and O-containing compounds with the same aromatic structure. (29) The HPLC-F bile screening method has been validated by comparison to quantitative GC/MS methodology following oil spills and in environmental monitoring, demonstrating strong correlation between the two methods for NPH equivalents (r = 0.94, p < 0.0001), PHN equivalents (r = 0.93, p < 0.0001) and BaP equivalents. (29, 30, 50, 51) The method is routinely used in a number of biomonitoring studies to estimate PAH exposure in fish and is frequently the preferred method over the more rigorous analytical approaches following an oil spill where there is a need to test large numbers of samples for exposure in a timely and cost-effective manner. (29, 30, 47, 49, 51-53)

Materials and Methods

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Collection of Samples

During 2011–2013, extensive demersal longline surveys evaluating fish disease were conducted in the GoM, from the West Florida Shelf (WFS) to west of the Mississippi River. (13) In 2011, fish were caught via demersal longlining on chartered commercial fishing vessels between June and August at depths ranging from 38–180 m (Figure 1). From 2012, all fish were caught via demersal longlining in the month of August, onboard the R/V Weatherbird II, at depths ranging from 34–389 m. Additionally, red snapper samples were obtained from the Madison-Swanson fishery closed area, by rod and reel in June of 2013 and 2014, at a depth of 85 m (Figure 1).

Figure 1. Location of sampling stations conducted in the northern Gulf of Mexico in 2011 (white), 2012–2013 (red, gray, yellow) and the *Deepwater Horizon* (DWH) blowout. Red markers denote red snapper stations grouped as northern Gulf of Mexico (nGoM) stations. Yellow markers denote red snapper stations grouped as West Florida Shelf (WFS) stations. Adapted by permission. Copyright © 2015 Esri, DeLorme, GEBCO, NOAA, NGDC. All rights reserved.

At each longline sampling station, an average of 495 baited #13 circle hooks were attached to 91-kg-test leaders and to 3.2 mm galvanized steel (2011, 2012), or 544-kg-test monofilament main line (2013). Bait used was cut fish (Atlantic mackerel (Scomber scombrus)) or various squid. Temperature–time-depth recorders (Star: Oddi CDST Centi) were deployed at the beginning and end of each longline set. Latitude, longitude, depth, and weather conditions were also recorded at the beginning and end of each set. Average soak time was 2 h.

Target fish for the longline surveys included the three species analyzed in this study. The target fish species were processed at time of capture for standard and total lengths, weight, sex and a subsample of the catch were selected to be sampled for bile, liver, muscle, otoliths and other tissues. Bile was collected by dissecting the gall bladder away from the liver, cutting the bile duct, and draining the fluid via the duct into 8 mL combusted amber vials. The samples were immediately frozen. In the laboratory, bile samples were stored at −40 °C until analysis.

Laboratory Analysis

All 2011 bile samples (n = 30) were analyzed at the Northwest Fisheries Science Center (NWFSC), Seattle, WA. The 2012 (n = 62) and 2013 (n = 179) bile samples were analyzed at Mote Marine Laboratory (MML), Sarasota, FL. Prior to analysis of the 2012 and 2013 samples, an interlaboratory comparison was completed to validate methods, precision and accuracy between the two laboratories. The interlab comparison used three bile samples from 2011, from different species (cobia (Rachycentron canadum), greater amberjack (Seriola dumerili), red snapper) and over a wide range of concentrations (for NPH: 41–240 μg g^–1; for PHN: 6.3–46 μg g^–1, for BaP: 97–310 ng g^–1). Prior to the interlab comparison, accuracy was monitored as part of the quality assurance plan at the NWFSC using a fish bile control sample (bile of Atlantic salmon (Salmo salar) exposed to 25 μg mL^–1 of Monterey Crude oil for 48 h). There was successful interlaboratory agreement for the three bile samples, with a CV of less than 15%, for PAH equivalents for NPH, PHN, and BaP. Bile samples were then analyzed using the semiquantitative bile screening HPLC-F method following NWFSC Environmental Chemistry program protocols described below. (29, 48, 49)

Untreated bile samples (3 μL) were injected directly onto the HPLC-F system (MML: Agilent Technologies, Series 1100, Santa Clara, CA; NWFSC: Waters, Milford, MA) equipped with a C-18 reverse-phase column (Synergi 4 μm Hydro-RP 80A, Phenomenex, Torrence, CA), with the column temperature held at 50 °C. Fluorescent aromatic compounds were eluted at 1 mL/min using a linear gradient from 100% solvent A (0.5% acetic acid in water) to 100% solvent B (methanol). Chromatograms were recorded at representative wavelength pairs of 292/335 nm for the NPH equivalents (2–3 ring FACs), 260/380 nm for the PHN equivalents (3–4 ring FACs) and 380/430 nm for the BaP equivalents (4–5 ring FACs). All peaks within the portion of the chromatogram where metabolites elute (6–19 min), were integrated for each wavelength pair, summed and FACs were calculated using external standards of the respective parent compounds, NPH, PHN, and BaP, to convert sample area (fluorescence response) to PAH equivalents (ng g^–1) bile wet weight using the following calculation: (48)

where the density of bile is 1.03 g mL^–1. (21) All equivalent concentrations were reported to two significant figures.

Quality Assurance/Control

Quality assurance was monitored in four ways. (1) An interlaboratory comparison of three 2011 bile samples was performed between MML and the NWFSC discussed above. (2) A methanol solvent blank was run prior to every field sample. The area of the methanol blank was subtracted from the area of the field sample that was subsequently analyzed. (3) Each field sample was run in duplicate, with a CV of less than 15%. If the CV between duplicates was greater than 15%, the sample was run again in triplicate until the CV reached less than 15%. (4) A continuing calibration was used to monitor instrument stability throughout the entire analysis by running the quantifying standards of parent PAHs of NPH (2.5 μg mL^–1), PHN (1 μg mL^–1) and BaP (250 ng mL^–1) every 12 field samples, making sure the CV remained less than 15%.

Data Analysis

Nonparametric, or permutation-based, hypothesis tests were run as it is unrealistic that biological data meet the assumptions (e.g., normal distribution, random sampling) of traditional parametric analyses, such as analysis of variance. (54, 55) If a potential explanatory variable was categorical (e.g., year), a nonparametric multivariate analysis of variance (npMANOVA), also known as a permutation-based analysis of variance when used on univariate data, was run using α = 0.05 to reject the null hypothesis. Between-group dispersion was checked for homogeneity prior to each npMANOVA and if dispersions were nonhomogenous, the data were transformed to minimize heterogeneity. If the npMANOVA was significant, a pairwise npMANOVA was run to assess subset’s significant differences. An adjusted p-value, using the Holms–Bonferroni transformation, was used to test the null hypothesis for a pairwise npMANOVA, using α = 0.05.

Results and Discussion

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Biliary PAH Metabolite Concentrations

This study examined 271 bile samples, from 26 longline stations, collected over the three years following the DWH blowout, including 96 golden tilefish, 67 king snake eel, and 108 red snapper (Table 1). The concentrations of biliary NPH and PHN equivalents varied linearly within individuals (r = 0.92, p = 0.001), for all three species, and within sites, therefore, only results for NPH equivalents are analyzed and discussed to avoid redundant information. The strong correlation between NPH and PHN metabolite concentration has been found in other studies suggesting a common petrogenic PAH source. (51, 56, 57) The correlation between NPH and BaP metabolites was also significant (r = 0.30, p = 0.001), although much weaker than the correlation between NPH and PHN, therefore, results for BaP metabolite concentration are analyzed and presented separately. The low molecular weight (LMW) PAHs, specifically NPH and PHN, are present in relatively high concentrations in DWH crude oil while BaP is found in much smaller concentrations, or not quantified above the detection limits of the instrument. (11, 12)

Table 1. Summary Statistics for Biliary Naphthalene (μg g^–1) and Benz[a]pyrene (ng g^–1) Metabolite Equivalent Concentrations for Red Snapper, Golden Tilefish and King Snake Eel Caught in the Northern Gulf of Mexico, Separated by Year of Catch^a

year		naphthalene equivalents (μg g^–1)
	species	mean	median	range	SD	n	mean length (cm)	% female : % male
2011	red snapper	120	110	41–470	78	30	65	60:40
2012	red snapper	61	54	20–130	27	15	58	60:40
	golden tilefish	240	230	110–340	61	24	67	n/a
	king snake eel	38	24	11–88	27	23	151	n/a
2013	red snapper	51	48	13–140	27	63	65	47:53
	golden tilefish	220	230	22–480	110	72	65	63:37
	king snake eel	24	16	3.6–210	34	44	140	n/a

year		benzo[a]pyrene equivalents (ng g^–1)
2011	species	mean	median	range	SD	n
	red snapper	280	260	94–590	140	30
2012	red snapper	220	170	68–540	150	15
	golden tilefish	170	140	51–470	110	24
	king snake eel	260	160	46–850	150	23
2013	red snapper	380	300	310–1500	330	63
	golden tilefish	370	220	71–3030	450	72
	king snake eel	160	130	34–880	150	44

SD, standard deviation, n, number of samples analyzed. Mean length (cm) and sex ratio (% female: % male) is also provided, and are the same for individuals measured for naphthalene and benzo[a]pyrene equivalents. Sex ratio is not provided for king snake eel (n/a = not applicable), as sex is difficult to determine, and sex is not provided for 2012 golden tilefish catch.

Species-Specific Differences in Biliary PAH Metabolite Concentration

For both 2012 and 2013 data, there is a significant difference in NPH metabolite concentrations between all three study organisms, with golden tilefish having significantly higher concentrations of biliary NPH metabolites than king snake eel or red snapper (Figure 2; p = 0.001, p = 0.001 respectively). Mean NPH metabolite concentration in golden tilefish was, on average, four times higher than red snapper for both 2012 (p = 0.003) and 2013 (p = 0.003), six times higher than king snake eel in 2012 (p = 0.003) and nine times higher than king snake eel in 2013 (p = 0.003). This difference persists overall and at the four longline stations where golden tilefish and king snake eel co-occurred. Golden tilefish and red snapper have never been caught at the same station on our longlining cruises due to differences in habitat and depth range. Red snapper mean NPH metabolite concentration is consistently higher than king snake eel concentrations, with mean concentrations five times higher in 2012 (p = 0.012) and two times higher in 2013 (p = 0.003). This pattern also occurred at two of three longline stations where red snapper and king snake eel co-occurred.

Figure 2. Biliary naphthalene metabolite concentrations (μg g^–1) for golden tilefish (2012: n = 24; 2013: n = 72), red snapper (2011: n = 30; 2012: n = 15; 2013: n = 63) and king snake eel (2012: n = 23; 2013: n = 44), sampled in 2011, 2012, and 2013 in the northern Gulf of Mexico.

In contrast to results for NPH, no significant differences in BaP metabolite concentration were found among the three species for 2012 (Figure 3; p = 0.265). However, for 2013, average BaP metabolite concentration is two times higher in golden tilefish and red snapper compared to king snake eel (Figure 3; p = 0.003, p = 0.003 respectively), while golden tilefish and red snapper concentrations are statistically similar (p = 0.751).

Figure 3. Biliary benzo[a]pyrene metabolite concentrations (ng g^–1) for golden tilefish (2012: n = 24; 2013: n = 72), red snapper (2011: n = 30; 2012: n = 15; 2013: n = 63) and king snake eel (2012: n = 23; 2013: n = 44), sampled in 2011, 2012, and 2013 in the northern Gulf of Mexico.

The uptake of PAHs by organisms is generally governed by a number of complex mechanisms including chemical bioavailability, species-specific metabolism, and biotransformation, diet, trophic level, and habitat use. Bioavailability is a function of both species-specific metabolic processes and uptake, as well as physicochemical properties. Molecular weight and K_ow have been found to be negatively correlated with bioavailability of individual PAHs. (58) The less hydrophobic LMW PAHs (log K_ow < 4) tend to dissolve more rapidly than high molecular weight (HMW) compounds (low K_ow > 4), thereby increasing their bioavailability to marine organisms. Preferential uptake of LMW PAHs, by two species of benthic fish, has been documented and attributed to both the bioavailability of the compounds, as well as biotransformation mechanisms, such as higher biotransformation rates of HMW compounds compared to LMW PAHs. (59-61) However, in contrast, higher rate of metabolism of LMW PAHs has also been found and attributed to differences in K_ow. (62, 63) In addition, research suggests that the use of chemical dispersants, such as Corexit 9500, increases the uptake, bioavailability and bioconcentration of PAHs by exposed fish. (64-66) The use of chemical dispersants following the DWH blowout, therefore, could have influenced both the bioavailability and potentially the toxicity of PAH to exposed fishes.

The significant difference in NPH metabolite concentrations among the three fish species, which persists even when species are sampled at the same station, indicates these differences are not a sampling artifact or due to spatial heterogeneity of exposure. The much higher concentrations of NPH metabolites in golden tilefish as compared to the other two species is likely due to their burrowing lifestyle, incidental sediment ingestion, and their diet of benthic prey (e.g., benthic invertebrates and demersal fishes), which may result in additional routes of exposure to sedimented PAH contamination. As the solubility of PAHs decreases with increasing molecular weight, the bioaccumulation potential for LMW compounds from sediment tends to be greater than the HMW compounds. (59) Previous studies on organic contaminants also demonstrated negative correlations between biota-sediment accumulation factors (BSAF) and log K_ow, suggesting decreasing bioavailability with increasing log K_ow. (67) Furthermore, HMW compounds can be physically bulky limiting their ability to pass through lipid membrane barriers, resulting in lower body burdens. The more hydrophobic HMW PAHs bind more readily with particulates, dissolved organic material (DOM) and oil droplets, also hindering their bioavailability to marine organisms. Recent studies of the DWH blowout document a hydrocarbon-contaminated marine snow event and found evidence of rapid deposition of associated oil-particle aggregates and degraded oil to the seabed. (3, 5, 68) When dissecting golden tilefish, it is evident that they ingest large volumes of sediment, seen in the digestive tract, buccal cavity and gills, while obvious sediment ingestion is not observed in the king snake eel or red snapper digestive tracts (personal observation). Together the observed hydrocarbon-contaminated marine snow and degraded oil deposition on the seafloor, differences in bioavailability, and species-specific metabolism and uptake help to explain the higher levels of NPH observed in golden tilefish.

We hypothesize king snake eel may have lower biliary PAH metabolite concentrations than the other species analyzed due to their inordinate epidermal mucus production, inefficiency of metabolism or peculiarities of their life history. King snake eel may eliminate LMW PAHs through mucus, as they produce prodigious amounts relative to the other species (personal observation). Exposure studies have documented high levels of NPH and metabolites in the epidermal mucus of both rainbow trout (Oncorhynchus mykiss) and starry flounder (Platichthys stellatus), exposed to [³H]naphthalene, suggesting epidermal mucus is an important pathway of LMW PAH excretion from the body. (69, 70) Alternatively, mucus may provide a physical barrier against dermal uptake. King snake eel may also be less efficient at metabolizing PAHs, although, hepatic ethoxyresorufin-O-deethylase (EROD) activity, a biomarker of exposure to organic contaminants, in eel of another family, the European eel (Anguilla anguilla), was found to be comparable to a teleost, European flounder (Platichthys flesus), suggesting that eels can metabolize PAHs. (71) King snake eel life history, although unknown, may play a role in contaminant exposure and metabolism, as other Ophichthid eels (Myrophis punctatus) have complex life history and sexual maturation, which may influence enzymatic activity. (71, 72)

Fish length, weight, and sex have been previously correlated with biliary PAH concentrations. (52, 53) In this study, fish sex and length were examined as factors influencing biliary PAH metabolite concentration. Male red snapper were found to have higher biliary NPH metabolite concentrations than females (p = 0.021) with the mean concentrations of 61 μg g^–1 and 44 μg g^–1, respectively. Differences in biliary PAH metabolite concentration between sex has been documented and hypothesized to be due to sex hormone differences in PAH metabolism (e.g., enzyme induction and activity), and regulation of monooxygenase activity by estrogens, leading to male fish having higher concentrations of biliary FACs. (10, 53, 73) Larger king snake eel were found to have lower concentrations of both biliary NPH and BaP metabolites (NPH: r = −0.40, p = 0.001; BaP: r = −0.60, p = 0.002). A similar trend with length was seen for golden tilefish for BaP metabolites (r = −0.33, p = 0.004). The weak but significant negative relationship between biliary BaP and fish length for golden tilefish suggests diet may play a larger role in exposure. Golden tilefish exhibit an ontogenetic shift in diet, from benthic invertebrates, to a higher proportion of fish, which may be a mechanism of changing PAH exposure with fish length, as invertebrates have lower metabolism and elimination efficiencies for PAHs compared to vertebrates. Very little is known about king snake eel, therefore, their life history, physiology or possibly the same ontogenetic shift in diet may explain the similar trend, however, no diet studies have been published for the species.

Temporal Variation in Biliary PAH Metabolite Concentration

Between 2012 and 2013, there was no significant change in golden tilefish NPH metabolite concentration (Figure 2; p = 0.367), with the mean concentration declining 8% from 240 μg g^–1 to 220 μg g^–1. However, there was a significant increase in golden tilefish BaP metabolite concentration over the two years (Figure 3; p = 0.025), with the mean concentration increasing from 170 ng g^–1 to 370 ng g^–1. Between 2012 and 2013, the mean concentration of NPH metabolites in king snake eel declined by 37%, from 38 μg g^–1 to 24 μg g^–1, although this difference was not significant (Figure 2; p = 0.063). There was, however, a significant decrease in king snake eel BaP metabolite concentration over the two years (Figure 3; p = 0.025), decreasing 38% (260 ng g^–1 to 160 ng g^–1).

Over the three-year period following the DWH event, there was a significant decrease in mean red snapper NPH metabolite concentration (Figure 2; p = 0.001). Between 2011 and 2012, there was a significant 49% decrease from a mean concentration of 120 μg g^–1 to 61 μg g^–1 (p = 0.003). Between 2012 and 2013, there was a continued decrease in the mean concentration, from 61 μg g^–1 to 51 μg g^–1, although the difference between 2012 and 2013 was nonsignificant (p = 0.194). Red snapper BaP metabolites remained at similar concentrations over the three years (Figure 3; p = 0.282).

The significant declines in NPH metabolite concentration in red snapper is indicative of an episodic exposure event to NPH prior to 2011. (13) A similar, although nonsignificant, decrease in king snake eel NPH metabolite concentration between 2012 and 2013 also suggests episodic exposure to elevated PAHs. For both species, these data support a scenario of increased NPH contamination in the environment coincident with the DWH blowout and a decrease in exposure reflected in decreasing biliary NPH metabolite concentration in following years. In comparison, the persistent, and significantly higher, concentrations of biliary NPH metabolites in golden tilefish suggests that the source of NPH for golden tilefish did not decrease over time, since biliary PAH metabolites indicate short-term exposure to PAHs. (28, 31) If PAHs exist in sediments associated with golden tilefish burrows and are being sequestered by continued sedimentation, the digging behavior of golden tilefish may re-expose these animals to PAHs, while other co-occurring species may not be exposed to the same routes and thus the same effective exposure levels. Crescent gunnel (Pholis laeta), a demersal fish, collected from sites polluted by the Exxon Valdez oil spill, showed elevated concentrations of LMW biliary PAH metabolites 10 years after the event, indicating that oil can persist in the environment resulting in persistently elevated levels of biliary PAH metabolites. (74) The combination of sediment enrichment from the hydrocarbon-contaminated marine snow event following the DWH and the slow dissolution rates of HMW PAHs from oil droplets, particulates and DOM, help to explain the increasing concentration of biliary BaP metabolites for golden tilefish, as the bioavailability of PAHs in oil droplets or DOM increases over time. (75)

Spatial Variation in Biliary PAH Metabolite Concentration

Spatial variability in biliary PAH metabolite concentration was evaluated by comparing results for the northern GoM to the WFS for red snapper sampled in 2013 (Figure 1). Red snapper caught on the WFS had significantly lower biliary PAH metabolites, for both NPH (p = 0.001) and BaP (p = 0.001), compared to red snapper caught in the northern GoM, closer to the Mississippi River, extant oil infrastructure and the DWH event (Figure 4). Additionally, the northern GoM stations showed a decrease in biliary PAH concentration over time, for both NPH and BaP metabolites, suggesting episodic exposure to an elevated source of PAHs, whereas biliary PAH concentrations from the Madison–Swanson fishery closed area on the WFS have not decreased between years. Therefore, these stations on the WFS may represent baseline biliary PAH metabolite concentration for red snapper in the GoM. No significant spatial trends existed for golden tilefish and king snake eel biliary PAH data, as these species were not caught in large numbers on the WFS.

Figure 4. Comparison of red snapper biliary polycyclic aromatic hydrocarbon metabolite concentration for naphthalene (μg g^–1) and benzo[a]pyrene (ng g^–1) from two regional groups sampled in 2013, West Florida Shelf (WFS, n = 14) and northern Gulf of Mexico (nGoM, n = 49). For both NPH and BaP metabolite concentrations, p = 0.001.

Comparison to Historical Biliary PAH Data

We conducted a metadata analysis of previous studies that used similar HPLC-F methods to quantify biliary PAH metabolite concentrations in fish, including studies of three other oil spills, three previous GoM studies, six polluted estuaries, and one “pristine” site upstream of the 1984 Columbia River oil spill (51, 56, 57, 76-80) (Figure 5). In comparison to all of these, golden tilefish biliary NPH metabolite concentrations (240 μg g^–1), collected two years hence of the DWH blowout, were among the most contaminated fish, only falling below pink salmon (Oncorhynchus gorbuscha, 480 μg g^–1) sampled immediately after the Exxon Valdez oil spill and an assortment of species from a polluted channel (São Sebastião channel, 290 μg g^–1) in São Paulo, Brazil, that serves as the largest petroleum terminal in that country, frequently experiencing oil spills and discharge. (56, 76) Golden tilefish NPH metabolite concentrations are about 1.5 times higher than those reported from inshore fish (primarily Atlantic croaker (Micropogonias undulatus)) caught in the northern GoM both before and after Hurricane Katrina (190 μg g^–1, 150 μg g^–1, respectively) and 6.5 times higher than white sturgeon (Ancipenser transmontanus, 32 μg g^–1) caught downstream of the Columbia River oil spill. (76, 77) Red snapper and king snake eel biliary NPH metabolite concentrations (120 μg g^–1 (from 2011), 38 μg g^–1 (from 2012), respectively) comparatively rank much lower, closer to previous GoM data sampled from an assortment of species offshore of Texas in 1993 (110 μg g^–1), with king snake eel concentrations being similar to the relatively unpolluted site in the Columbia River. (77, 80) For biliary BaP metabolites, all three species have comparatively low concentrations (170–280 ng g^–1), which are very similar to the 1993 GoM data (200 ng g^–1), and much lower than the highly polluted estuaries (580–2900 ng g^–1) and inshore fish samples taken before and after Hurricane Katrina (1400–1600 ng g^–1). (76, 77, 79, 80)

Figure 5. Comparison of biliary naphthalene (left, thin white bars), phenanthrene (left, thin black bars) and benzo[a]pyrene (right) metabolite concentration between post-*Deepwater Horizon* golden tilefish (n = 24) sampled in the northern Gulf of Mexico (GoM) in 2012, red snapper (n = 30) sampled in 2011 and king snake eel (n = 23) sampled in 2012, to other oil spills, polluted estuaries and one pristine site on the Columbia River. Data from this study are denoted with stars.

Comparisons of PAH data from these three species post-DWH reveal that the level of LMW PAH exposure was extensive, particularly for golden tilefish, even two years and more following the event. While the levels of LMW PAHs in golden tilefish prior to the DWH are unknown, the 1993 study off of Texas, which included anchor tilefish (Caulolatilus intermedius), had a much lower average of LMW PAHs (116 μg g^–1 for NPH), and perhaps indicated the residual pollution levels in areas where oil and gas rigs are located. (80) In contrast, the BaP metabolite concentrations in our study were lower than most other studies. Benzo[a]pyrene is primarily derived of from combusted hydrocarbons (e.g., from urban and industrial pollution), thus, the relatively high levels of BaP in studies of polluted estuaries, and inshore GoM, serve more a function of depth and distance from shore, compared to the offshore locations sampled in this study. (76, 78) While large quantities of DWH oil were burned at sea, it is unknown what portion of the oil resulted in BaP contamination, although the quantity of BaP in DWH source oil was very low, if present at all. (11, 12)

The data synthesized in this study constitute one of the largest biliary PAH data sets for fishes and the largest for the GoM. Nearly 300 bile samples were analyzed from three GoM demersal fish species over three years following the DWH blowout. Significant interspecies differences exist between the three species in concentrations of LMW biliary PAH metabolites. Golden tilefish exhibit the highest known concentrations of biliary NPH metabolites of data available on GoM fishes, and were among the highest concentrations in comparable studies globally. Differences in habitat, physiology, and diet most likely account for the observed differences in LMW PAH exposure, however, differences in bioavailability, and species-specific rates of uptake, metabolism, and elimination, all play a role. While king snake eel may directly encounter polluted sediments as well, their physiology may result in avoidance (e.g., mucus barrier) and elimination of ingested PAHs, although, this is conjecture. Red snapper, in contrast, are not as intimately coupled with sediments, leading to respiration and diet as the more likely exposure routes, with species-specific metabolism and excretion most likely lending to the lower biliary PAH concentrations. To definitively understand these species-specific differences, further analysis of muscle and liver tissue from the field-caught individuals in this study, will be analyzed for PAHs and alkylated homologues to better understand the distribution of PAHs between bile, liver, and muscle, and to better understand PAH source. Controlled exposure studies could also assist in understanding these mechanisms.

Temporal trends were observed for interspecies variation of biliary NPH metabolite concentrations. The high concentrations of biliary NPH persisted over time in golden tilefish, whereas they declined in red snapper and king snake eel. The statistically significant, exponential decrease over time of biliary NPH metabolites in red snapper suggests exposure to LMW PAH pollution from an episodic event likely occurred in the GoM prior to 2011. (13) The same, albeit lower, decrease over time was seen in NPH and BaP biliary PAH metabolite concentration for king snake eel samples. It is possible (likely) that the episodic event was the DWH blowout, since it is unlikely that the other sources of PAHs to the GoM would decrease substantially (e.g., 50%) in the same region at the same time. (13) Concentrations of biliary PAH metabolites were significant higher in the northern GoM, closer to the DWH event and Mississippi River, compared to the WFS, for 2013 red snapper samples. The declining concentrations of PAHs with distance from the DWH well site is consistent with this event being the source of elevated PAHs in red snapper observed.

While the collection and analysis of biliary PAHs in fish to evaluate temporal trends in contamination reveals much about the source and magnitude of pollution in the GoM, these studies would have been aided by the availability of pre-DWH baseline data. The lack of such baseline complicates but does not obviate the assessment of PAH pollution source and magnitude. Spatially relevant, precise and replicated baseline data would have been useful in detecting the levels of exposure of GoM fishes. Nevertheless, temporal changes in contaminant levels reveal much about the ephemeral and more persistent levels of contamination, as suggested by long-term studies of the Exxon Valdez oil spill. Continued monitoring of GoM fishes should document return to baseline conditions in areas not subjected to persistent levels of PAH contamination.

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Author Information

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Corresponding Author
- Susan M. Snyder - University of South Florida, College of Marine Science, St. Petersburg, Florida 33701, United States; Email: [email protected]
Authors
- Erin L. Pulster - Mote Marine Laboratory, Sarasota, Florida 34236, United States
- Dana L. Wetzel - Mote Marine Laboratory, Sarasota, Florida 34236, United States
- Steven A. Murawski - University of South Florida, College of Marine Science, St. Petersburg, Florida 33701, United States
Author Contributions
The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript.
Notes
The authors declare no competing financial interest.

Acknowledgment

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We thank the owners, captains and crew of the F/V Pisces and the R/V Weatherbird II; the field team, including E. Herdter, A. Wallace, K. Deak, S. Gilbert, S. Grasty, and the fishermen; the Murawski Lab, G. Ylitalo and B. Anulacion for their guidance and the 2011 bile analysis at the NOAA Northwest Fisheries Science Center; and I. Romero, P. Schwing, D. Hollander and K. Able for their collaboration. This research was made possible in part by grants from BP/The Gulf of Mexico Research Initiative, through its Center for Integrated Modeling and Analysis of Gulf Ecosystems (C-IMAGE), the State of Louisiana, and NOAA Grant NA11NMF4720151-Systematic Survey of Finfish Disease Prevalence in the Gulf of Mexico.

ABBREVIATIONS

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DWH	Deepwater Horizon
GoM	Gulf of Mexico
PAH	polycyclic aromatic hydrocarbons
NPH	naphthalene
PHN	phenanthrene
BaP	benzo[a]pyrene
FAC	fluorescent aromatic hydrocarbons
HPLC-F	high performance liquid chromatography with fluorescence detection
WFS	West Florida Shelf
NWFSC	Northwest Fisheries Science Center
MML	Mote Marine Laboratory
LMW	low molecular weight
HMW	high molecular weight
BSAF	biota-sediment accumulation factor
K_ow	octanol–water partition coefficient
DOM	dissolved organic matter

References

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Journal of Chromatography (1993), 642 (1-2), 15-32CODEN: JOCRAM; ISSN:0021-9673.
A review, with 42 refs., covers rapid HPLC methods to screen arom. compds. in aquatic sediment, bile, and tissue samples of aquatic biota to est. pollutant concns. that can be confirmed in selected samples by gas chromatog.-mass spectrometry.
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Assessment of the exposure of subsistence fish to aromatic compounds after the Exxon Valdez oil spill
Hom, Tom; Varanasi, Usha; Stein, John E.; Sloan, Catherine A.; Tilbury, Karen L.; Chan, Sin-Lam
American Fisheries Society Symposium (1996), 18 (Proceedings of the Exxon Valdez Oil Spill Symposium, 1993), 856-866CODEN: AFSSEF; ISSN:0892-2284. (American Fisheries Society)
Previous research has shown that fish have the capacity to biotransform many arom. compds. (ACs) to polar metabolites that are readily accumulated in the gall bladder for excretion and to greatly limit the deposition of ACs or their metabolites in edible muscle tissue. Accordingly, a rapid and sensitive method, developed in our lab. for screening bile for fluorescent arom. compds. (FACs) that are components of petroleum was used to assess exposure of fish to ACs after the Exxon Valdez oil spill. The results of anal. of bile from nearly 500 fish provided evidence that many fish were exposed to ACs after the oil spill. Edible flesh samples from fishes showing a range of biliary FACs were analyzed for the presence of ACs by gas chromatog.-mass spectrometry. Concns. of FACs in bile of bottom fishes and salmon from areas affected by oil ranged from 10 to 17,000 ng phenanthrene equiv./mg bile protein; however, no appreciable concns. of ACs were detected in muscle of bottom fishes (<1 ng/g wet wt., ppb), and, although concns. of ACs in muscle of salmon were somewhat higher (most samples ranged from 0 to 20 ppb), they rarely exceeded 100 ppb. These findings were used by the Alaskan Oil Spill Health Task Force in arriving at an advisory opinion that consumption of the flesh of fish from areas affected by the oil spill posed minimal risk to native Alaskans. Furthermore, these results were used to verify findings of earlier lab. studies on the pathways of metab. and disposition of ACs in fish that were important in formulating a focused, scientific basis for the present investigation of oil-impacted subsistence fisheries.
58
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Varanasi, U.; Gmur, D. J. Hydrocarbons and metabolites in English sole (Parophrys vetulus) exposed simultaneously to [3H]benzo[a]pyrene and [14C]naphthalene in oil-contaminated sediment Aquat. Toxicol. 1981, 1 (1) 49– 67
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Hydrocarbons and metabolites in english sole (Parophrys vetulus) exposed simultaneously to [3H]benzo[a]pyrene and [14C]-naphthalene in oil-contaminated sediment
Varanasi, Usha; Gmur, Dennis J.
Aquatic Toxicology (1981), 1 (1), 49-67CODEN: AQTODG; ISSN:0166-445X.
English sole were exposed to 3H-labeled benzo[a]pyrene (I) [50-32-8] and 14C-labeled naphthalene (II) [91-20-3] in sediment contg. 1% Prudhoe Bay crude oil (PBCO). Bioconcn. values [pmoles of hydrocarbon equiv. in g of dry tissue/pmoles of hydrocarbon equiv. in g of sediment-assocd. water (SAW)] for II were greater than corresponding values for I in tissues of fish exposed for 24 h. However, from 24 to 168 h of the exposure, a substantial decline in II-derived radioactivity and a significant increase in I-derived radioactivity occurred in most of the tissues examd. When fish were transferred for 24 h to sediment free of radioactivity and PBCO, the retention of I-derived radioactivity in the tissues of fish was considerably greater than II. Metabolites of I and II in sediment, SAW, liver, and bile of fish were characterized by TLC. For liver, a 2-dimensional TLC was devised to sep. I and its metabolites from liver lipids. An important finding was that liver of English sole metabolized I to a far greater extent than II; at 24 h after the exposure, the concn. ratio of I to its metabolites was 1:49, whereas II was 6:1. Larger proportions of glucuronide conjugates than sulfate conjugates of I and II were present in bile of English sole. II was largely converted into a glucuronide conjugate of 1,2-dihydro-1,2-dihydroxynaphthalene. A no. of metabolites of I known to be toxic to mammals were detected in the liver and bile including the 7,8-dihydro-7,8-dihydroxy deriv. [13345-25-0] and its conjugates. These findings of extensive metab. of I by fish liver very probably explain why I is usually not detected in liver of fish even when considerable concns. of I are detected in the environment of the fish.
61
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Hepatic Clearance of 6 Polycyclic Aromatic Hydrocarbons by Isolated Perfused Trout Livers: Prediction From In Vitro Clearance by Liver S9 Fractions
Nichols, John W.; Hoffman, Alex D.; ter Laak, Thomas L.; Fitzsimmons, Patrick N.
Toxicological Sciences (2013), 136 (2), 359-372CODEN: TOSCF2; ISSN:1096-0929. (Oxford University Press)
Isolated perfused trout livers were used to evaluate in vitro-in vivo metab. extrapolation procedures for fish. In vitro depletion rates for 6 polycyclic arom. hydrocarbons (PAHs) were measured using liver S9 fractions and extrapolated to the intact tissue. Predicted hepatic clearance (CLH) values were then compared with values exhibited by intact livers. Binding in liver perfusates was manipulated using bovine serum albumin (BSA) and was characterized by solid-phase microextn. Addnl. studies were conducted to develop binding terms (fU; calcd. as the ratio of unbound fractions in liver perfusate [fU,PERF] and the S9 system [fU,S9]) used as inputs to a well-stirred liver model. Hepatic clearance values for pyrene and benzo[a]pyrene, predicted by extrapolating in vitro data to the intact tissue, were in good agreement with measured values (<2-fold difference). This can be partly attributed to the rapid rate at which both compds. were metabolized by S9 fractions, resulting in perfusion-limited clearance. Predicted levels of CLH for the other PAHs underestimated obsd. values although these differences were generally small (<3-fold, except for naphthalene). Setting fU = 1.0 improved clearance predictions at the highest tested BSA concn. (10 mg/mL), suggesting that trout S9 fractions exhibit lower levels of intrinsic activity than the intact tissue or that the full binding assumption (ie, fU = fU,PERF/fU,S9) underestimates the availability of hydrophobic substrates to hepatic metabolizing enzymes. These findings provide qualified support for procedures currently being used to predict metab. impacts on chem. accumulation by fish based on measured rates of in vitro activity.
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Uptake and release of naphthalene and its metabolites in skin and epidermal mucus of salmonids
Varanasi, Usha; Uhler, Michael; Stranahan, Susan I.
Toxicology and Applied Pharmacology (1978), 44 (2), 277-89CODEN: TXAPA9; ISSN:0041-008X.
Rainbow trout (Salmo gairdneri) exposed to 1, 4, 5, 8-3H-labeled naphthalene (I) [91-20-3] through force feeding, via i.p. injection, or in flowing water, accumulated significant concns. of both I and its metabolic products in skin, regardless of the mode of exposure. Concns. of I and its metabolites in skin increased with time initially and subsequently declined. Concns. of I decreased more rapidly than the metabolites in all 3 expts.: as much as 17.6 (force-feeding study), 15.1 (injection study), and 52.0% (water-immersion study) of the total radioactivity in the skin was attributable to the metabolites at the end of each expt. This tendency of skin to retain metabolites preferentially was also exhibited by the liver. Based on 1 g of dry tissue, skin contained 34-84% of the I and 13-26% of the metabolites present in the liver 24 h after the initiation of I exposure; activity of skin with respect to liver was the highest for the water-immersion study, as may be expected, and lowest for the injection study. Epidermal mucus of the test fish in the injection and force-feeding expts. contained small concns. of I and considerably larger concns. of metabolites for several days after the initial treatment. Because epidermal mucus of fish exists in a state of continuous flux (i.e., a small amt. of mucus is continuously sloughed off and renewed), these results imply that epidermal mucus is involved in the excretion of hydrocarbons and their metabolites.
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Sublethal detoxification responses to contaminant exposure associated with offshore production platforms
Mcdonald, Susanne J.; Willett, Kristine L.; Thomsen, Jane; Beatty, Karla B.; Connor, Kevin; Narasimhan, Tumkur R.; Erickson, Cynthia M.; Safe, Stephen H.
Canadian Journal of Fisheries and Aquatic Sciences (1996), 53 (11), 2606-2617CODEN: CJFSDX; ISSN:0706-652X. (National Research Council of Canada)
Several biomarkers of arom. hydrocarbon exposure were used to evaluate contamination assocd. with petroleum and gas development and prodn. in the Gulf of Mexico. Several species of fish and invertebrates were sampled at stations <100 m (near) and >3000 m (far) from the center of three platforms. No significant near/far station differences were obsd. in aryl hydrocarbon hydroxylase (AHH) activity for any invertebrate species. The only significant induction of ethoxyresorufin O-deethylase (EROD) activity in H4IIE cell bioassays was obsd. in cells dosed with exts. of brown shrimp (Penaeus aztecus) sampled at MAI-686 near station. However, a sediment contaminant gradient was not detected at this platform. No significant near/far station differences in EROD and AHH activities, CYPIA mRNA levels, and biliary polynuclear arom. hydrocarbon (PAH) metabolite concns. were detected in 16 species of fish. However, species-dependent differences in EROD activity and biliary PAH metabolite levels were detected. Addnl., a radiolabeled nuclear aryl hydrocarbon receptor complex was characterized for two fish species.

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Cite this: Environ. Sci. Technol. 2015, 49, 14, 8786–8795

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Abstract
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Figure 1
Figure 1. Location of sampling stations conducted in the northern Gulf of Mexico in 2011 (white), 2012–2013 (red, gray, yellow) and the Deepwater Horizon (DWH) blowout. Red markers denote red snapper stations grouped as northern Gulf of Mexico (nGoM) stations. Yellow markers denote red snapper stations grouped as West Florida Shelf (WFS) stations. Adapted by permission. Copyright © 2015 Esri, DeLorme, GEBCO, NOAA, NGDC. All rights reserved.
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Figure 2
Figure 2. Biliary naphthalene metabolite concentrations (μg g^–1) for golden tilefish (2012: n = 24; 2013: n = 72), red snapper (2011: n = 30; 2012: n = 15; 2013: n = 63) and king snake eel (2012: n = 23; 2013: n = 44), sampled in 2011, 2012, and 2013 in the northern Gulf of Mexico.
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Figure 3
Figure 3. Biliary benzo[a]pyrene metabolite concentrations (ng g^–1) for golden tilefish (2012: n = 24; 2013: n = 72), red snapper (2011: n = 30; 2012: n = 15; 2013: n = 63) and king snake eel (2012: n = 23; 2013: n = 44), sampled in 2011, 2012, and 2013 in the northern Gulf of Mexico.
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Figure 4
Figure 4. Comparison of red snapper biliary polycyclic aromatic hydrocarbon metabolite concentration for naphthalene (μg g^–1) and benzo[a]pyrene (ng g^–1) from two regional groups sampled in 2013, West Florida Shelf (WFS, n = 14) and northern Gulf of Mexico (nGoM, n = 49). For both NPH and BaP metabolite concentrations, p = 0.001.
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Figure 5
Figure 5. Comparison of biliary naphthalene (left, thin white bars), phenanthrene (left, thin black bars) and benzo[a]pyrene (right) metabolite concentration between post-Deepwater Horizon golden tilefish (n = 24) sampled in the northern Gulf of Mexico (GoM) in 2012, red snapper (n = 30) sampled in 2011 and king snake eel (n = 23) sampled in 2012, to other oil spills, polluted estuaries and one pristine site on the Columbia River. Data from this study are denoted with stars.
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References
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  There is no corresponding record for this reference.
4. 4
  Valentine, D. L.; Fisher, G. B.; Bagby, S. C.; Nelson, R. K.; Reddy, C. M.; Sylva, S. P.; Woo, M. A. Fallout plume of submerged oil from Deepwater Horizon Proc. Natl. Acad. Sci. U.S.A. 2014, 111 (45) 15906– 15911
  There is no corresponding record for this reference.
5. 5
  Romero, I. C.; Schwing, P. T.; Brooks, G. R.; Larson, R. A.; Hastings, D. W.; Ellis, G.; Goddard, E. A.; Hollander, D. J. Hydrocarbons in deep-sea sediments following the 2010 Deepwater Horizon blowout in the northeast Gulf of Mexico PLoS One 2015, 10 (5) e0128371
  There is no corresponding record for this reference.
6. 6
  Lin, Q.; Mendelssohn, I. A. Impacts and recovery of the Deepwater Horizon oil spill on vegetation structure and function of coastal salt marshes in the northern Gulf of Mexico Environ. Sci. Technol. 2012, 46 (7) 3737– 3743
  There is no corresponding record for this reference.
7. 7
  Michel, J.; Owens, E. H.; Zengel, S.; Graham, A.; Nixon, Z.; Allard, T.; Holton, W.; Reimer, P. D.; Lamarche, A.; White, M.; Rutherford, N.; Childs, C.; Mauseth, G.; Challenger, G.; Taylor, E. Extent and degree of shoreline oiling: Deepwater Horizon Oil Spill, Gulf of Mexico, USA PLoS One 2013, 8 (6) e65087
  7
  Extent and degree of shoreline oiling: Deepwater Horizon oil spill, Gulf of Mexico, USA
  Michel, Jacqueline; Owens, Edward H.; Zengel, Scott; Graham, Andrew; Nixon, Zachary; Allard, Teresa; Holton, William; Reimer, P. Doug; Lamarche, Alain; White, Mark; Rutherford, Nicolle; Childs, Carl; Mauseth, Gary; Challenger, Greg; Taylor, Elliott
  PLoS One (2013), 8 (6), e65087CODEN: POLNCL; ISSN:1932-6203. (Public Library of Science)
  The oil from the 2010 Deepwater Horizon spill in the Gulf of Mexico was documented by shoreline assessment teams as stranding on 1,773 km of shoreline. Beaches comprised 50.8%, marshes 44.9%, and other shoreline types 4.3% of the oiled shoreline. Shoreline cleanup activities were authorized on 660 km, or 73.3% of oiled beaches and up to 71 km, or 8.9% of oiled marshes and assocd. habitats. One year after the spill began, oil remained on 847 km; two years later, oil remained on 687 km, though at much lesser degrees of oiling. For example, shorelines characterized as heavily oiled went from a max. of 360 km, to 22.4 km one year later, and to 6.4 km two years later. Shoreline cleanup has been conducted to meet habitat-specific cleanup endpoints and will continue until all oiled shoreline segments meet endpoints. The entire shoreline cleanup program has been managed under the Shoreline Cleanup Assessment Technique (SCAT) Program, which is a systematic, objective, and inclusive process to collect data on shoreline oiling conditions and support decision making on appropriate cleanup methods and endpoints. It was a particularly valuable and effective process during such a complex spill.
8. 8
  Silliman, B. R.; van de Koppel, J.; McCoy, M. W.; Diller, J.; Kasozi, G. N.; Earl, K.; Adams, P. N.; Zimmerman, A. R. Degradation and resilience in Louisiana salt marshes after the BP–Deepwater Horizon oil spill Proc. Natl. Acad. Sci. U. S. A. 2012, 109 (28) 11234– 11239
  There is no corresponding record for this reference.
9. 9
  Hylland, K. Polycyclic aromatic hydrocarbon (PAH) ecotoxicology in marine ecosystems J. Toxicol. Environ. Health, Part A 2006, 69 (1–2) 109– 123
  There is no corresponding record for this reference.
10. 10
  Tuvikene, A. Responses of fish to polycyclic aromatic hydrocarbons (PAHs) Ann. Zool. Fenn. 1995, 32 (3) 295– 309
  There is no corresponding record for this reference.
11. 11
  BP Gulf Coast Restoration Organization: Gulf Science Data, 2014. http://gulfsciencedata.bp.com/.
  There is no corresponding record for this reference.
12. 12
  Reddy, C. M.; Arey, J. S.; Seewald, J. S.; Sylva, S. P.; Lemkau, K. L.; Nelson, R. K.; Carmichael, C. A.; McIntyre, C. P.; Fenwick, J.; Ventura, G. T.; Van Mooy, B. A. S.; Camilli, R. Composition and fate of gas and oil released to the water column during the Deepwater Horizon oil spill Proc. Natl. Acad. Sci. U.S.A. 2012, 109 (50) 20229– 20234
  There is no corresponding record for this reference.
13. 13
  Murawski, S. A.; Hogarth, W. T.; Peebles, E. B.; Barbeiri, L. Prevalence of external skin lesions and polycyclic aromatic hydrocarbon concentrations in Gulf of Mexico Fishes, post-Deepwater Horizon Trans. Am. Fish. Soc. 2014, 143 (4) 1084– 1097
  13
  Prevalence of External Skin Lesions and Polycyclic Aromatic Hydrocarbon Concentrations in Gulf of Mexico Fishes, Post-Deepwater Horizon
  Murawski, Steven A.; Hogarth, William T.; Peebles, Ernst B.; Barbeiri, Luiz
  Transactions of the American Fisheries Society (2014), 143 (4), 1084-1097CODEN: TAFSAI; ISSN:0002-8487. (Taylor & Francis Ltd.)
  We surveyed offshore fish populations in the Gulf of Mexico in 2011 and 2012, following persistent reports of abnormal skin lesions and other pathologies in the aftermath of the Deepwater Horizon oil spill. The incidence of skin lesions in 2011 sampling was most frequent in some bottom-dwelling species along the continental shelf edge north of the Deepwater Horizon site. Longline surveys revealed that by 2012 the overall frequency of lesions in northern Gulf of Mexico (NGM) fishes in the vicinity of the Deepwater Horizon had declined 53%, with severity also declining. Relatively high concns. of polycyclic arom. hydrocarbon (PAH) metabolites (up to 470,000 ng naphthalene equiv./g bile wet wt.), indicative of oil-related pollution, were found in fish bile in 2011; concns. of summed PAHs measured in fish liver and muscle were relatively low (<35 ng/g) due to the efficient metab. of these compds. by teleost fish. Significant declines in bile concns. of naphthalene and phenanthrene metabolites in Red Snapper Lutjanus campechanus between 2011 and 2012 indicate an episodic exposure to elevated levels of hydrocarbons of petrogenic origin. The compn. of PAH parent compds. and alkylated homologs in Red Snapper liver samples was highly correlated with oil collected at the Deepwater Horizon wellhead but was less coherent with other PAH sources in the NGM. The elevated 2011 prevalence of skin lesions in some NGM species was unrelated to surface salinity or temp. anomalies and was not the result of an epizootic observable in our histopathol. samples but was pos. correlated with PAH concn. Thus, we fail to reject the null hypothesis that elevated skin lesion frequency is unrelated to PAH exposure from the Deepwater Horizon oil spill. Received August 14, 2013; accepted March 26, 2014.
14. 14
  Hicken, C. E.; Linbo, T. L.; Baldwin, D. H.; Willis, M. L.; Myers, M. S.; Holland, L.; Larsen, M.; Stekoll, M. S.; Rice, S. D.; Collier, T. K.; Scholz, N. L.; Incardona, J. P. Sublethal exposure to crude oil during embryonic development alters cardiac morphology and reduces aerobic capacity in adult fish Proc. Natl. Acad. Sci. U.S.A. 2011, 108 (17) 7086– 7090
  14
  Sublethal exposure to crude oil during embryonic development alters cardiac morphology and reduces aerobic capacity in adult fish
  Hicken, Corinne E.; Linbo, Tiffany L.; Baldwin, David H.; Willis, Maryjean L.; Myers, Mark S.; Holland, Larry; Larsen, Marie; Stekoll, Michael S.; Rice, Stanley D.; Collier, Tracy K.; Scholz, Nathaniel L.; Incardona, John P.
  Proceedings of the National Academy of Sciences of the United States of America (2011), 108 (17), 7086-7090, S7086/1-S7086/3CODEN: PNASA6; ISSN:0027-8424. (National Academy of Sciences)
  Exposure to high concns. of crude oil produces a lethal syndrome of heart failure in fish embryos. Mortality is caused by cardiotoxic polycyclic arom. hydrocarbons (PAHs), ubiquitous components of petroleum. Here, we show that transient embryonic exposure to very low concns. of oil causes toxicity that is sublethal, delayed, and not counteracted by the protective effects of cytochrome P 450 induction. Nearly a year after embryonic oil exposure, adult zebrafish showed subtle changes in heart shape and a significant redn. in swimming performance, indicative of reduced cardiac output. These delayed physiol. impacts on cardiovascular performance at later life stages provide a potential mechanism linking reduced individual survival to population-level ecosystem responses of fish species to chronic, low-level oil pollution.
15. 15
  Heintz, R. A. Chronic exposure to polynuclear aromatic hydrocarbons in natal habitats leads to decreased equilibrium size, growth, and stability of pink salmon populations Integr. Environ. Assess. Manage. 2007, 3 (3) 351– 363
  There is no corresponding record for this reference.
16. 16
  White, P. A.; Robitaille, S.; Rasmussen, J. B. Heritable reproductive effects of benzo a pyrene on the fathead minnow (Pimephales promelas) Environ. Toxicol. Chem. 1999, 18 (8) 1843– 1847
  There is no corresponding record for this reference.
17. 17
  Brette, F.; Machado, B.; Cros, C.; Incardona, J. P.; Scholz, N. L.; Block, B. A. Crude oil impairs cardiac excitation-contraction coupling in fish Science 2014, 343 (6172) 772– 776
  17
  Crude Oil Impairs Cardiac Excitation-Contraction Coupling in Fish
  Brette, Fabien; Machado, Ben; Cros, Caroline; Incardona, John P.; Scholz, Nathaniel L.; Block, Barbara A.
  Science (Washington, DC, United States) (2014), 343 (6172), 772-776CODEN: SCIEAS; ISSN:0036-8075. (American Association for the Advancement of Science)
  Crude oil is known to disrupt cardiac function in fish embryos. Large oil spills, such as the Deepwater Horizon (DWH) disaster that occurred in 2010 in the Gulf of Mexico, could severely affect fish at impacted spawning sites. The physiol. mechanisms underlying such potential cardiotoxic effects remain unclear. Here, we show that crude oil samples collected from the DWH spill prolonged the action potential of isolated cardiomyocytes from juvenile bluefin and yellowfin tunas, through the blocking of the delayed rectifier potassium current (IKr). Crude oil exposure also decreased calcium current (ICa) and calcium cycling, which disrupted excitation-contraction coupling in cardiomyocytes. Our findings demonstrate a cardiotoxic mechanism by which crude oil affects the regulation of cellular excitability, with implications for life-threatening arrhythmias in vertebrates.
18. 18
  Collier, T. K.; Stein, J. E.; Goksoyr, A.; Myers, M. S.; Gooch, J. W.; Huggett, R. J.; Varanasi, U. Biomarkers of PAH exposure in oyster toadfish (Opsanus tau) from the Elizabeth River, Virginia Environ. Sci. 1993, 2 (3) 161– 177
  18
  Biomarkers of PAH exposure in oyster toadfish (Opsanis tau) from the Elizabeth River, Virginia
  Collier, Tracy K.; Stein, John E.; Goksoeyr, Anders; Myers, Mark S.; Gooch, Jay W.; Huggett, Robert J.; Varanasi, Usha
  Environmental Sciences (Tokyo, Japan) (1993), 2 (3), 161-77CODEN: ESCIE6; ISSN:0915-955X.
  Surficial sediments of the Elizabeth River, Virginia, USA show a pronounced gradient of polycyclic arom. hydrocarbon (PAH) contamination. Oyster toadfish (Opsanis tau), which live in the Elizabeth River, are bottom-dwelling fish with limited migratory movement. This presents an opportunity to evaluate biomarkers of PAH exposure in a feral fish. The biomarkers measured in the present study were levels of fluorescent arom. compds. (FACs) in bile, which arise largely from metab. of PAHs; hepatic levels of hydrophobic xenobiotic-DNA adducts, detected by 32P-postlabeling; and hepatic monooxygenase activities catalyzed by cytochrome P 450 1A (CYP1A), an enzyme known to be readily induced in fish exposed to PAHs and many other org. xenobiotic compds. Toadfish were sampled from six sites in and adjacent to the Elizabeth River, with levels of PAHs in the sediments at the capture sites ranging from less than 10 to almost 100,000 ppb on a dry wt. basis. Levels of biliary FACs and hepatic xenobiotic-DNA adducts were highly correlated with levels of PAHs in sediments, showing the usefulness of these measures for assessing PAH exposure in feral fish. Hepatic CYP1A-assocd. monooxygenase activities, however, were near or below limits of detection and showed no differences with respect to site of capture. Immunochem. assay of hepatic CYP1A, whether by Western blot or immunohistochem. localization, corroborated the finding of weak expression of CYP1A in the fish sampled in this study. An interesting finding was the inability to detect any expression of CYP1A in normal liver parenchyma (hepatocytes), which is in contrast to other fish species studied thus far.
19. 19
  Nichols, J. W.; McKim, J. M.; Lien, G. J.; Hoffman, A. D.; Bertelsen, S. L.; Elonen, C. M. A physiologically based toxicokinetic model for dermal absorption of organic chemicals by fish Fund. Appl. Toxicol. 1996, 31 (2) 229– 242
  19
  A physiologically based toxicokinetic model for dermal absorption of organic chemicals by fish
  Nichols, John W.; McKim, James M.; Lien, Gregory J.; Hoffman, Alex D.; Bertelsen, Sharon L.; Elonen, Colleen M.
  Fundamental and Applied Toxicology (1996), 31 (2), 229-242CODEN: FAATDF; ISSN:0272-0590. (Academic)
  A physiol. based toxicokinetic model was developed to describe dermal absorption of waterborne org. chems. by fish. The skin was modeled as a discrete compartment into which compds. diffuse as a function of chem. permeability and the concn. gradient. The model includes a countercurrent description of chem. flux at fish gills and was used to simulate dermal-only exposures, during which the gills act as a route of elimination. The model was evaluated by exposing adult rainbow trout and channel catfish to hexachloroethane (HCE), pentachloroethane (PCE), and 1,1,2,2-tetrachloroethane (TCE). Skin permeability coeffs. were obtained by fitting model simulations to measured arterial blood data. Permeability coeffs. increased with the no. of chlorine substituent groups, but not in the manner expected from a directly proportional relation between dermal permeability and skin:water chem. partitioning. An evaluation of rate limitations on dermal flux in both trout and catfish suggested that chem. absorption was limited more by diffusion across the skin than by blood flow to the skin. Modeling results from a hypothetical combined dermal and branchial exposure indicate that dermal uptake could contribute from 1.6% (TCE) to 3.5% (HCE) of initial uptake in trout. Dermal uptake rates in catfish are even higher than those in trout and could contribute from 7.1% (TCE) to 8.3% (PCE) of initial uptake in a combined exposure.
20. 20
  Law, R. J.; Hellou, J. Contamination of fish and shellfish following oil spill incidents Environ. Geosci. 1999, 6 (2) 90– 98
  There is no corresponding record for this reference.
21. 21
  Krahn, M. M.; Rhodes, L. D.; Myers, M. S.; Moore, L. K.; Macleod, W. D.; Malins, D. C. Associations between metabolites of aromatic compounds in bile and the occurence of hepatic lesions in English sole (Parophrys vetulus) from Puget Sound, Washington Arch. Environ. Contam. Toxicol. 1986, 15 (1) 61– 67
  There is no corresponding record for this reference.
22. 22
  Myers, M. S.; Johnson, L. L.; Collier, T. K. Establishing the causal relationship between polycyclic aromatic hydrocarbon (PAH) exposure and hepatic neoplasms and neoplasia-related liver lesions in English sole (Pleuronectes vetulus) Hum. Ecol. Risk Assess. 2003, 9 (1) 67– 94
  22
  Establishing the causal relationship between polycyclic aromatic hydrocarbon (PAH) exposure and hepatic neoplasms and neoplasia-related liver lesions in English sole (Pleuronectes vetulus)
  Myers, Mark S.; Johnson, Lyndal L.; Collier, Tracy K.
  Human and Ecological Risk Assessment (2003), 9 (1), 67-94CODEN: HERAFR; ISSN:1080-7039. (CRC Press LLC)
  A review on establishing the causal relationship between polycyclic arom. hydrocarbon (PAH) exposure and hepatic neoplasms and neoplasia-related liver lesions in english sole (Pleuronectes vetulus). For almost 25 yr the authors' lab. has studied the impact of PAHs and related industrial contaminants on benthic fish, following an interdisciplinary approach involving chem. exposure assessment linked to synoptic detection of various effects at several levels of biol. organization. These data demonstrate a cause-and-effect relationship between neoplastic and neoplasia-related liver lesions in English sole, and exposure to PAHs, and to a lesser degree, chlorinated hydrocarbons such as PCBs. In statistical analyses of data from multiple field studies conducted since 1978, exposure to PAHs measured in various compartments has consistently been identified as a highly significant, major risk factor for neoplasms and related lesions in this species, with PCB exposure shown to be a significant, but less consistent and less strong risk factor for these lesions. A cause-and-effect relationship between PAHs and toxicopathic liver lesions in this species is further supported by the exptl. induction of toxicopathic lesions identical to those obsd. in field-collected fish, in sole exposed in the lab. to model carcinogenic PAHs such as BaP or to PAH-rich exts. of sediments from Eagle Harbor, a severely PAH-contaminated site in Puget Sound. More recent field studies have identified significant assocns. between hepatic cytochrome P 4501A (CYP1A) induction and xenobiotic-DNA adduct formation, and hepatic lesion prevalences in wild subadult English sole. Field studies in Eagle Harbor subsequent to capping of. The most PAH-contaminated region of this harbor with clean dredge spoils have shown a decline in exposure to PAHs as assessed by biliary fluorescent arom. compds. (FACs) and hepatic xenobiotic-DNA adducts. This decline in PAH exposure has been accompanied by a dramatic decline in risk of occurrence of toxicopathic hepatic lesions in English sole from Eagle Harbor. Further, lab. studies have induced lesions in English sole by injections of exts. from PAH-contaminated sediments. Overall, these findings relating to exposure to PAHs and chlorinated hydrocarbons and the occurrence of hepatic neoplasms and neoplasia-related lesions in English sole fulfill the classic criteria for causality in epizootiol. or ecol. risk assessment studies, including:. (1) Strength of assocn.,. (2) Consistency of assocn.,. (3) Specificity of assocn.,. (4) Toxicol. and biol. plausibility,. (5) Temporal sequence/timing (i.e., exposure precedes disease, effect decreases when the cause is decreased or removed),. (6) Dose-response or biol. gradient, and. (7) Supportive exptl. evidence.
23. 23
  Malins, D. C.; McCain, B. B.; Brown, D. W.; Chan, S. L.; Myers, M. S.; Landahl, J. T.; Prohaska, P. G.; Friedman, A. J.; Rhodes, L. D.; Burrows, D. G.; Gronlund, W. D.; Hodgins, H. O. Chemical pollutants in sediments and diseases of bottom-dwelling fish in Puget Sound, Washington Environ. Sci. Technol. 1984, 18 (9) 705– 713
  There is no corresponding record for this reference.
24. 24
  Malins, D. C.; McCain, B. B.; Brown, D. W.; Varanasi, U.; Krahn, M. M.; Myers, M. S.; Chan, S. L. Sediment associated contaminants and liver diseases in bottom-dwelling fish Hydrobiologia 1987, 149, 67– 74
  There is no corresponding record for this reference.
25. 25
  Lee, R. F.; Sauerheb, R.; Dobbs, G. H. Uptake, metabolism and discharge of polycyclic aromatic hydrocarbons by marine fish Mar. Biol. 1972, 17 (3) 201– &
  There is no corresponding record for this reference.
26. 26
  Varanasi, U.; Stein, J. E.; Nishimoto, M., Biotransformation and disposition of polycyclic aromatic hydrocarbons (PAH) in fish. In Metabolism of Polycylic Aromatic Hydrocarbons in the Aquatic Environment; Varanasi, U., Ed.; CRC Press, Inc.: Boca Raton, FL, 1989; pp 94– 143.
  There is no corresponding record for this reference.
27. 27
  Ylitalo, G. M.; Krahn, M. M.; Dickhoff, W. W.; Stein, J. E.; Walker, C. C.; Lassitter, C. L.; Garrett, E. S.; Desfosse, L. L.; Mitchell, K. M.; Noble, B. T.; Wilson, S.; Beck, N. B.; Benner, R. A.; Koufopoulos, P. N.; Dickey, R. W. Federal seafood safety response to the Deepwater Horizon oil spill Proc. Natl. Acad. Sci. U.S.A. 2012, 109 (50) 20274– 20279
  There is no corresponding record for this reference.
28. 28
  Beyer, J.; Jonsson, G.; Porte, C.; Krahn, M. M.; Ariese, F. Analytical methods for determining metabolites of polycyclic aromatic hydrocarbon (PAH) pollutants in fish bile: A review Environ. Toxicol. Pharmacol. 2010, 30 (3) 224– 244
  There is no corresponding record for this reference.
29. 29
  Krahn, M. M.; Myers, M. S.; Burrows, D. G.; Malins, D. C. Determination of metabolites of xenobiotics in the bile of fish from polluted waterways Xenobiotica 1984, 14 (8) 633– 646
  There is no corresponding record for this reference.
30. 30
  Krahn, M. M.; Burrows, D. G.; Ylitalo, G. M.; Brown, D. W.; Wigren, C. A.; Collier, T. K.; Chan, S. L.; Varanasi, U. Mass spectrometric analysis for aromatic compounds in bile of fish sampled after the Exxon Valdez oil spill Environ. Sci. Technol. 1992, 26 (1) 116– 126
  There is no corresponding record for this reference.
31. 31
  Le Du-Lacoste, M.; Akcha, F.; Devier, M.-H.; Morin, B.; Burgeot, T.; Budzinski, H. Comparative study of different exposure routes on the biotransformation and genotoxicity of PAHs in the flatfish species, Scophthalmus maximus Environ. Sci. Pollut. Res. 2013, 20 (2) 690– 707
  There is no corresponding record for this reference.
32. 32
  Meador, J. P.; Buzitis, J.; Bravo, C. F. Using fluorescent aromatic compounds in bile from juvenile salmonids to predict exposure to polycyclic aromatic hydrocarbons Environ. Toxicol. Chem. 2008, 27 (4) 845– 853
  There is no corresponding record for this reference.
33. 33
  Gallaway, B. J.; Szedlmayer, S. T.; Gazey, W. J. A life history review for red snapper in the Gulf of Mexico with an evaluation of the importance of offshore petroleum platforms and other artificial reefs Rev. Fish. Sci. 2009, 17 (1) 48– 67
  There is no corresponding record for this reference.
34. 34
  Able, K. W.; Grimes, C. B.; Cooper, R. A.; Uzmann, J. R. Burrow construction and behavior of tilefish, Lopholatilus chamaeleonticeps, in Hudson Submarine Canyon Environ. Biol. Fishes 1982, 7 (3) 199– 205
  There is no corresponding record for this reference.
35. 35
  Clark, S. T. Age, growth, and distributions of the giant snake eel, Ophichthus rex, in the Gulf of Mexico Bull. Mar. Sci. 2000, 67 (3) 911– 922
  There is no corresponding record for this reference.
36. 36
  Levengood, J. M.; Schaeffer, D. J. Polycyclic aromatic hydrocarbons in fish and crayfish from the Calumet region of southwestern Lake Michigan Ecotoxicology 2011, 20 (6) 1411– 1421
  There is no corresponding record for this reference.
37. 37
  Twichell, D. C.; Grimes, C. B.; Jones, R. S.; Able, K. W. The role of erosion by fish in shaping topography around Hudson Submarine Canyon J. Sediment. Petrol. 1985, 55 (5) 712– 719
  There is no corresponding record for this reference.
38. 38
  Grimes, C. B.; Turner, S. C. The complex life history of tilefish Lopholatilus chamaeleonticeps and vulnerability to exploitation Am. Fish. Soc. Symp. 1999, 23, 17– 26
  There is no corresponding record for this reference.
39. 39
  Katz, S. J.; Grimes, C. B.; Able, K. W. Delineation of tilefish, Lopholatilus chamaeleonticeps, stocks along the United States east coast and in the Gulf of Mexico U.S. Fish Wildl. Serv. Fish. Bull. 1983, 81 (1) 41– 50
  There is no corresponding record for this reference.
40. 40
  Grimes, C. B.; Able, K. W.; Jones, R. S. Tilefish, Lopholatilus chamaeleonticeps, habitat, behaviro and community structure in Mid-Atlantic and Southern New England waters Environ. Bio. Fishes. 1986, 15 (4) 273– 292
  There is no corresponding record for this reference.
41. 41
  Burgess, G. H. Biological, Fishery, and Product Assessments of the Keoghfish, an Underutilized and Unmanaged Gulf of Mexico Resource; University of Florida: Floirda Museum of Natural History.
  There is no corresponding record for this reference.
42. 42
  Bozzano, A. Vision in the rufus snake eel, Ophichthus rufus: Adaptive mechanisms for a burrowing life-style Marine Biology 2003, 143 (1) 167– 174
  There is no corresponding record for this reference.
43. 43
  Chakrabarty, P.; Lam, C.; Hardman, J.; Aaronson, J.; House, P. H.; Janies, D. A. SM: A web-based application for visualizing the overlap of distributions and pollution events, with a list of fishes put at risk by the 2010 Gulf of Mexico oil spill Biodiversity Conserv. 2012, 21 (7) 1865– 1876
  There is no corresponding record for this reference.
44. 44
  McCawley, J. R.; Cowan, J. H., Jr., Seasonal and size specific diet and prey demand of red snapper on Alabama artificial reefs. In American Fisheries Society Symposium; Patterson, W. F.; Cowan, J. H.; Fitzhugh, G. R.; Nieland, D. L., Eds. ; 2007; Vol. 60, pp 77– 104.
  There is no corresponding record for this reference.
45. 45
  Steimle, F. W. Essential fish habitat source document. Tilefish, Lopholatilus chamaeleonticeps, life history and habitat characteristics. U.S. Dept. of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Northeast Region, Northeast Fisheries Science Center ; Available from the National Technical Information Service: Woods Hole, MA, 1999.
  There is no corresponding record for this reference.
46. 46
  Hellou, J.; Leonard, J.; Collier, T. K.; Ariese, F. Assessing PAH exposure in feral finfish from the Northwest Atlantic Mar. Pollut. Bull. 2006, 52 (4) 433– 441
  There is no corresponding record for this reference.
47. 47
  Krahn, M. M.; Ylitalo, G. M.; Buzitis, J.; Chan, S. L.; Varanasi, U. Rapid high-performance liquid chromatographic methods that screen for aromatic compounds in environmental samples J. Chromatogr. 1993, 642 (1–2) 15– 32
  47
  Rapid high-performance liquid chromatographic methods that screen for aromatic compounds in environmental samples
  Krahn, Margaret M.; Ylitalo, Gina M.; Buzitis, Jon; Chan, Sin Lam; Varanasi, Usha
  Journal of Chromatography (1993), 642 (1-2), 15-32CODEN: JOCRAM; ISSN:0021-9673.
  A review, with 42 refs., covers rapid HPLC methods to screen arom. compds. in aquatic sediment, bile, and tissue samples of aquatic biota to est. pollutant concns. that can be confirmed in selected samples by gas chromatog.-mass spectrometry.
48. 48
  Krahn, M. M.; Moore, L. K.; Macleod, W. D.Standard Analytical Procedures of the NOAA National Analytical Facility, 1986: Metabolites of Aromatic Compounds in Fish Bile, NMFS-NWC-102; U.S. Department of Commerce, N. O. a. A. A., National Marine Fisheries Service, Northeast Region, Northwest Fisheries Science Center, 1986; pp 1– 25.
  There is no corresponding record for this reference.
49. 49
  Johnson, L. L.; Ylitalo, G. M.; Myers, M. S.; Anulacion, B. F.; Buzitis, J.; Collier, T. K. Aluminum smelter-derived polycyclic aromatic hydrocarbons and flatfish health in the Kitimat marine ecosystem, British Columbia, Canada Sci. Total Environ. 2015, 512, 227– 239
  There is no corresponding record for this reference.
50. 50
  Krahn, M. M.; Burrows, D. G.; Macleod, W. D.; Malins, D. C. Determination of individual metabolites of aromatic compounds in hydrolyzed bile of English sole (Parophrys vetulus) from polluted sites in Puget Sound, Washington Arch. Environ. Contam. Toxicol. 1987, 16 (5) 511– 522
  There is no corresponding record for this reference.
51. 51
  Krahn, M. M.; Ylitalo, G. M.; Buzitis, J.; Bolton, J. L.; Wigren, C. A.; Chan, S. L.; Varanasi, U. Analyses for petroleum related contaminants in marine fish and sediments following the Gulf oil spill Mar. Pollut. Bull. 1993, 27, 285– 292
  There is no corresponding record for this reference.
52. 52
  Tomy, G. T.; Halldorson, T.; Chemomas, G.; Bestvater, L.; Danegerfield, K.; Ward, T.; Pleskach, K.; Stern, G.; Atchison, S.; Majewski, A.; Reist, J. D.; Palace, V. P. Polycyclic aromatic hydrocarbon metabolites in Arctic Cod (Boreogadus saida) from the Beaufort Sea and associative fish health effects Environ. Sci. Technol. 2014, 48 (19) 11629– 11636
  There is no corresponding record for this reference.
53. 53
  Vuorinen, P. J.; Keinanen, M.; Vuontisjarvi, H.; Barsiene, J.; Broeg, K.; Forlin, L.; Gercken, J.; Kopecka, J.; Koehler, A.; Parkkonen, J.; Pempkowiak, J.; Schiedek, D. Use of biliary PAH metabolites as a biomarker of pollution in fish from the Baltic Sea Mar. Pollut. Bull. 2006, 53 (8–9) 479– 487
  There is no corresponding record for this reference.
54. 54
  Anderson, M. J. A new method for non-parametric multivariate analysis of variance Austral Ecol. 2001, 26 (1) 32– 46
  There is no corresponding record for this reference.
55. 55
  Manly, B. F. J.; Manly, B. F. J.Randomization and Monte Carlo Methods in Biology, 1991; Vol. i-xiii, pp 1– 281.
  There is no corresponding record for this reference.
56. 56
  da Silva, D. A. M.; Buzitis, J.; Krahn, M. M.; Bicego, M. C.; Pires-Vanin, A. M. S. Metabolites in bile of fish from Sao Sebastiao Channel, Sao Paulo, Brazil as biomarkers of exposure to petrogenic polycyclic aromatic compounds Mar. Pollut. Bull. 2006, 52 (2) 175– 183
  There is no corresponding record for this reference.
57. 57
  Hom, T.; Varanasi, U.; Stein, J. E.; Sloan, C. A.; Tilbury, K. L.; Chan, S.-L. Assessment of the exposure of subsistence fish to aromatic compounds after the Exxon Valdez oil spill Am. Fish. Soc. Symp. 1996, 18, 856– 866
  57
  Assessment of the exposure of subsistence fish to aromatic compounds after the Exxon Valdez oil spill
  Hom, Tom; Varanasi, Usha; Stein, John E.; Sloan, Catherine A.; Tilbury, Karen L.; Chan, Sin-Lam
  American Fisheries Society Symposium (1996), 18 (Proceedings of the Exxon Valdez Oil Spill Symposium, 1993), 856-866CODEN: AFSSEF; ISSN:0892-2284. (American Fisheries Society)
  Previous research has shown that fish have the capacity to biotransform many arom. compds. (ACs) to polar metabolites that are readily accumulated in the gall bladder for excretion and to greatly limit the deposition of ACs or their metabolites in edible muscle tissue. Accordingly, a rapid and sensitive method, developed in our lab. for screening bile for fluorescent arom. compds. (FACs) that are components of petroleum was used to assess exposure of fish to ACs after the Exxon Valdez oil spill. The results of anal. of bile from nearly 500 fish provided evidence that many fish were exposed to ACs after the oil spill. Edible flesh samples from fishes showing a range of biliary FACs were analyzed for the presence of ACs by gas chromatog.-mass spectrometry. Concns. of FACs in bile of bottom fishes and salmon from areas affected by oil ranged from 10 to 17,000 ng phenanthrene equiv./mg bile protein; however, no appreciable concns. of ACs were detected in muscle of bottom fishes (<1 ng/g wet wt., ppb), and, although concns. of ACs in muscle of salmon were somewhat higher (most samples ranged from 0 to 20 ppb), they rarely exceeded 100 ppb. These findings were used by the Alaskan Oil Spill Health Task Force in arriving at an advisory opinion that consumption of the flesh of fish from areas affected by the oil spill posed minimal risk to native Alaskans. Furthermore, these results were used to verify findings of earlier lab. studies on the pathways of metab. and disposition of ACs in fish that were important in formulating a focused, scientific basis for the present investigation of oil-impacted subsistence fisheries.
58. 58
  Wang, H.-S.; Man, Y.-B.; Wu, F.-Y.; Zhao, Y.-G.; Wong, C. K. C.; Wong, M.-H. Oral bioaccessibility of polycyclic aromatic hydrocarbons (PAHs) through fish consumption, based on an in vitro digestion model J. Agric. Food Chem. 2010, 58 (21) 11517– 11524
  There is no corresponding record for this reference.
59. 59
  Baumard, P.; Budzinski, H.; Garrigues, P.; Sorbe, J. C.; Burgeot, T.; Bellocq, J. Concentrations of PAHs (polycyclic aromatic hydrocarbons) in various marine organisms in relation to those in sediments and to trophic level Mar. Pollut. Bull. 1998, 36 (12) 951– 960
  There is no corresponding record for this reference.
60. 60
  Varanasi, U.; Gmur, D. J. Hydrocarbons and metabolites in English sole (Parophrys vetulus) exposed simultaneously to [3H]benzo[a]pyrene and [14C]naphthalene in oil-contaminated sediment Aquat. Toxicol. 1981, 1 (1) 49– 67
  60
  Hydrocarbons and metabolites in english sole (Parophrys vetulus) exposed simultaneously to [3H]benzo[a]pyrene and [14C]-naphthalene in oil-contaminated sediment
  Varanasi, Usha; Gmur, Dennis J.
  Aquatic Toxicology (1981), 1 (1), 49-67CODEN: AQTODG; ISSN:0166-445X.
  English sole were exposed to 3H-labeled benzo[a]pyrene (I) [50-32-8] and 14C-labeled naphthalene (II) [91-20-3] in sediment contg. 1% Prudhoe Bay crude oil (PBCO). Bioconcn. values [pmoles of hydrocarbon equiv. in g of dry tissue/pmoles of hydrocarbon equiv. in g of sediment-assocd. water (SAW)] for II were greater than corresponding values for I in tissues of fish exposed for 24 h. However, from 24 to 168 h of the exposure, a substantial decline in II-derived radioactivity and a significant increase in I-derived radioactivity occurred in most of the tissues examd. When fish were transferred for 24 h to sediment free of radioactivity and PBCO, the retention of I-derived radioactivity in the tissues of fish was considerably greater than II. Metabolites of I and II in sediment, SAW, liver, and bile of fish were characterized by TLC. For liver, a 2-dimensional TLC was devised to sep. I and its metabolites from liver lipids. An important finding was that liver of English sole metabolized I to a far greater extent than II; at 24 h after the exposure, the concn. ratio of I to its metabolites was 1:49, whereas II was 6:1. Larger proportions of glucuronide conjugates than sulfate conjugates of I and II were present in bile of English sole. II was largely converted into a glucuronide conjugate of 1,2-dihydro-1,2-dihydroxynaphthalene. A no. of metabolites of I known to be toxic to mammals were detected in the liver and bile including the 7,8-dihydro-7,8-dihydroxy deriv. [13345-25-0] and its conjugates. These findings of extensive metab. of I by fish liver very probably explain why I is usually not detected in liver of fish even when considerable concns. of I are detected in the environment of the fish.
61. 61
  Nichols, J. W.; Hoffman, A. D.; ter Laak, T. L.; Fitzsimmons, P. N. Hepatic clearance of 6 polycyclic aromatic hydrocarbons by isolated perfused trout livers: Prediction from in vitro clearance by liver s9 fractions Toxicol. Sci. 2013, 136 (2) 359– 372
  61
  Hepatic Clearance of 6 Polycyclic Aromatic Hydrocarbons by Isolated Perfused Trout Livers: Prediction From In Vitro Clearance by Liver S9 Fractions
  Nichols, John W.; Hoffman, Alex D.; ter Laak, Thomas L.; Fitzsimmons, Patrick N.
  Toxicological Sciences (2013), 136 (2), 359-372CODEN: TOSCF2; ISSN:1096-0929. (Oxford University Press)
  Isolated perfused trout livers were used to evaluate in vitro-in vivo metab. extrapolation procedures for fish. In vitro depletion rates for 6 polycyclic arom. hydrocarbons (PAHs) were measured using liver S9 fractions and extrapolated to the intact tissue. Predicted hepatic clearance (CLH) values were then compared with values exhibited by intact livers. Binding in liver perfusates was manipulated using bovine serum albumin (BSA) and was characterized by solid-phase microextn. Addnl. studies were conducted to develop binding terms (fU; calcd. as the ratio of unbound fractions in liver perfusate [fU,PERF] and the S9 system [fU,S9]) used as inputs to a well-stirred liver model. Hepatic clearance values for pyrene and benzo[a]pyrene, predicted by extrapolating in vitro data to the intact tissue, were in good agreement with measured values (<2-fold difference). This can be partly attributed to the rapid rate at which both compds. were metabolized by S9 fractions, resulting in perfusion-limited clearance. Predicted levels of CLH for the other PAHs underestimated obsd. values although these differences were generally small (<3-fold, except for naphthalene). Setting fU = 1.0 improved clearance predictions at the highest tested BSA concn. (10 mg/mL), suggesting that trout S9 fractions exhibit lower levels of intrinsic activity than the intact tissue or that the full binding assumption (ie, fU = fU,PERF/fU,S9) underestimates the availability of hydrophobic substrates to hepatic metabolizing enzymes. These findings provide qualified support for procedures currently being used to predict metab. impacts on chem. accumulation by fish based on measured rates of in vitro activity.
62. 62
  Burkhard, L. P.; Lukasewycz, M. T. Some bioaccumulation factors and biota-sediment accumulation factors for polycyclic aromatic hydrocarbons in lake trout Environ. Toxicol. Chem. 2000, 19 (5) 1427– 1429
  There is no corresponding record for this reference.
63. 63
  Jonsson, G.; Bechmann, R. K.; Bamber, S. D.; Baussant, T. Bioconcentration, biotransformation, and elimination of polycyclic aromatic hydrocarbons in sheepshead minnows (Cyprinodon variegatus) exposed to contaminated seawater Environ. Toxicol. Chem. 2004, 23 (6) 1538– 1548
  There is no corresponding record for this reference.
64. 64
  Ramachandran, S. D.; Hodson, P. V.; Khan, C. W.; Lee, K. Oil dispersant increases PAH uptake by fish exposed to crude oil Ecotoxicol. Environ. Saf. 2004, 59 (3) 300– 308
  There is no corresponding record for this reference.
65. 65
  Couillard, C. M.; Lee, K.; Legare, B.; King, T. L. Effect of dispersant on the composition of the water-accommodated fraction of crude oil and its toxicity to larval marine fish Environ. Toxicol. Chem. 2005, 24 (6) 1496– 1504
  There is no corresponding record for this reference.
66. 66
  Milinkovitch, T.; Kanan, R.; Thomas-Guyon, H.; Le Floch, S. Effects of dispersed oil exposure on the bioaccumulation of polycyclic aromatic hydrocarbons and the mortality of juvenile Liza ramada Sci. Total Environ. 2011, 409 (9) 1643– 1650
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67. 67
  Maruya, K. A.; Lee, R. E. Biota-sediment accumulation and trophic transfer factors for extremely hydrophobic polychlorinated biphenyls Environ. Toxicol. Chem. 1998, 17 (12) 2463– 2469
  There is no corresponding record for this reference.
68. 68
  Passow, U.; Ziervogel, K.; Asper, V.; Diercks, A., Marine snow formation in the aftermath of the Deepwater Horizon oil spill in the Gulf of Mexico. Environ. Res. Lett. 2012, 7, (3).
  There is no corresponding record for this reference.
69. 69
  Varanasi, U.; Gmur, D. J. Metabolisms and disposition of naphthalene in Starry flounder (Platichthys stellatus) Fed. Proc. 1978, 37 (3) 813– 813
  There is no corresponding record for this reference.
70. 70
  Varanasi, U.; Uhler, M.; Stranahan, S. I. Uptake and release of napthalene and its metabolites in skin and epidermal mucus of salmonids Toxicol. Appl. Pharmacol. 1978, 44 (2) 277– 289
  70
  Uptake and release of naphthalene and its metabolites in skin and epidermal mucus of salmonids
  Varanasi, Usha; Uhler, Michael; Stranahan, Susan I.
  Toxicology and Applied Pharmacology (1978), 44 (2), 277-89CODEN: TXAPA9; ISSN:0041-008X.
  Rainbow trout (Salmo gairdneri) exposed to 1, 4, 5, 8-3H-labeled naphthalene (I) [91-20-3] through force feeding, via i.p. injection, or in flowing water, accumulated significant concns. of both I and its metabolic products in skin, regardless of the mode of exposure. Concns. of I and its metabolites in skin increased with time initially and subsequently declined. Concns. of I decreased more rapidly than the metabolites in all 3 expts.: as much as 17.6 (force-feeding study), 15.1 (injection study), and 52.0% (water-immersion study) of the total radioactivity in the skin was attributable to the metabolites at the end of each expt. This tendency of skin to retain metabolites preferentially was also exhibited by the liver. Based on 1 g of dry tissue, skin contained 34-84% of the I and 13-26% of the metabolites present in the liver 24 h after the initiation of I exposure; activity of skin with respect to liver was the highest for the water-immersion study, as may be expected, and lowest for the injection study. Epidermal mucus of the test fish in the injection and force-feeding expts. contained small concns. of I and considerably larger concns. of metabolites for several days after the initial treatment. Because epidermal mucus of fish exists in a state of continuous flux (i.e., a small amt. of mucus is continuously sloughed off and renewed), these results imply that epidermal mucus is involved in the excretion of hydrocarbons and their metabolites.
71. 71
  Rotchell, J. M.; Bird, D. J.; Newton, L. C. Seasonal variation in ethoxyresorufin O-deethylase (EROD) activity in European eels Anguilla anguilla and flounders Pleuronectes flesus from the Severn Estuary and Bristol Channel Mar. Ecol.: Prog. Ser. 1999, 190, 263– 270
  There is no corresponding record for this reference.
72. 72
  Able, K. W.; Allen, D. M.; Bath-Martin, G.; Hare, J. A.; Hoss, D. E.; Marancik, K. E.; Powles, P. M.; Richardson, D. E.; Taylor, J. C.; Walsh, H. J.; Warlen, S. M.; Wenner, C. Life history and habitat use of the speckled worm eel, Myrophis punctatus, along the east coast of the United States Environ. Biol. Fishes 2011, 92 (2) 237– 259
  There is no corresponding record for this reference.
73. 73
  Navas, J. M.; Segner, H. Modulation of trout 7-ethoxyresorufin-O-deethylase (EROD) activity by estradiol and octylphenol Mar. Environ. Res. 2000, 50 (1–5) 157– 162
  There is no corresponding record for this reference.
74. 74
  Jewett, S. C.; Dean, T. A.; Woodin, B. R.; Hoberg, M. K.; Stegeman, J. J. Exposure to hydrocarbons 10 years after the Exxon Valdez oil spill: Evidence from cytochrome P4501A expression and biliary FACs in nearshore demersal fishes Mar. Environ. Res. 2002, 54 (1) 21– 48
  There is no corresponding record for this reference.
75. 75
  Baussant, T.; Sanni, S.; Jonsson, G.; Skadsheim, A.; Borseth, J. F. Bioaccumulation of polycyclic aromatic compounds: 1. Bioconcentration in two marine species and in semipermeable membrane devices during chronic exposure to dispersed crude oil Environ. Toxicol. Chem. 2001, 20 (6) 1175– 1184
  There is no corresponding record for this reference.
76. 76
  Hom, T.; Collier, T. K.; Krahn, M. M.; Strom, M. S.; Ylitalo, G. M.; Nilsson, W. B.; Papunjpye, R. N.; Varanasi, U., Assessing seafood safety, in the aftermath of Hurricane Katrina. In American Fisheries Society Symposium; McLaughlin, K. D., Ed., 2008; Vol. 64, pp 73– 93.
  There is no corresponding record for this reference.
77. 77
  Krahn, M. M.; Kittle, L. J.; Macleod, W. D. Evidence for exposure of fish to oil spilled into the Columbia River Mar. Environ. Res. 1986, 20 (4) 291– 298
  There is no corresponding record for this reference.
78. 78
  Myers, M. S.; Stehr, C. M.; Olson, O. P.; Johnson, L. L.; McCain, B. B.; Chan, S. L.; Varanasi, U. Relationships between toxicopathic hepatic lesions and exposure to chemical contaminants in English sole (Pleuronectes vetulus), Starry flounder (Platichthys stellatus), and White croaker (Genyonemus lineatus) from selected marine sites on the Pacific Coast, USA Environ. Health Perspect. 1994, 102 (2) 200– 215
  There is no corresponding record for this reference.
79. 79
  Johnson, L. L.; Ylitalo, G. M.; Arkoosh, M. R.; Kagley, A. N.; Stafford, C.; Bolton, J. L.; Buzitis, J.; Anulacion, B. F.; Collier, T. K. Contaminant exposure in outmigrant juvenile salmon from Pacific Northwest estuaries of the United States Environ. Monit. Assess. 2007, 124 (1–3) 167– 194
  There is no corresponding record for this reference.
80. 80
  McDonald, S. J.; Willett, K. L.; Thomsen, J.; Beatty, K. B.; Connor, K.; Narasimhan, T. R.; Erickson, C. M.; Safe, S. H. Sublethal detoxification responses to contaminant exposure associated with offshore production platforms Can. J. Fish. Aquat. Sci. 1996, 53 (11) 2606– 2617
  80
  Sublethal detoxification responses to contaminant exposure associated with offshore production platforms
  Mcdonald, Susanne J.; Willett, Kristine L.; Thomsen, Jane; Beatty, Karla B.; Connor, Kevin; Narasimhan, Tumkur R.; Erickson, Cynthia M.; Safe, Stephen H.
  Canadian Journal of Fisheries and Aquatic Sciences (1996), 53 (11), 2606-2617CODEN: CJFSDX; ISSN:0706-652X. (National Research Council of Canada)
  Several biomarkers of arom. hydrocarbon exposure were used to evaluate contamination assocd. with petroleum and gas development and prodn. in the Gulf of Mexico. Several species of fish and invertebrates were sampled at stations <100 m (near) and >3000 m (far) from the center of three platforms. No significant near/far station differences were obsd. in aryl hydrocarbon hydroxylase (AHH) activity for any invertebrate species. The only significant induction of ethoxyresorufin O-deethylase (EROD) activity in H4IIE cell bioassays was obsd. in cells dosed with exts. of brown shrimp (Penaeus aztecus) sampled at MAI-686 near station. However, a sediment contaminant gradient was not detected at this platform. No significant near/far station differences in EROD and AHH activities, CYPIA mRNA levels, and biliary polynuclear arom. hydrocarbon (PAH) metabolite concns. were detected in 16 species of fish. However, species-dependent differences in EROD activity and biliary PAH metabolite levels were detected. Addnl., a radiolabeled nuclear aryl hydrocarbon receptor complex was characterized for two fish species.
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Environmental Science & Technology

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Introduction

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Biliary PAH Metabolite Concentrations

Species-Specific Differences in Biliary PAH Metabolite Concentration

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Temporal Variation in Biliary PAH Metabolite Concentration

Spatial Variation in Biliary PAH Metabolite Concentration

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Comparison to Historical Biliary PAH Data

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PAH Exposure in Gulf of Mexico Demersal Fishes, Post-Deepwater Horizon
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