White perch health relative to urbanization and habitat degradation in Chesapeake Bay tributaries. I. Biliary neoplasms and hepatic lesions.

White perch Morone americana (Gmelin, 1789) from the Chesapeake Bay (USA) watershed have a high incidence of liver disease, including neoplasms of bile duct origin. Fish collected seasonally from spring 2019 to winter 2020 from the urban Severn River and the more rural Choptank River were evaluated for hepatic lesions. Biliary hyperplasia (64.1%), neoplasms (cholangioma and cholangiocarcinoma, 27%), and dysplasia (24.9%) were significantly higher in Severn River fish compared to Choptank River fish (52.9, 16.2, and 15.8%, respectively). Hepatocellular lesions were less common, including foci of hepatocellular alteration (FHA, 13.3%) and hepatocellular neoplasms (1%). There was also a progressive age-related increase in copper-laden granules in hepatocytes, which was a significant risk factor for FHA and could be a source of oxidative stress in the liver. Significant risk factors for biliary neoplasms included age, bile duct fibrosis, and infections by the myxozoan parasite Myxidium murchelanoi, but the prevalence and relative intensity of M. murchelanoi infections did not differ significantly between fish populations. Hepatic disease in this species appears to be chronic and may stem from an age-related accumulation of damage, possibly from parasitic infections and contaminants such as polychlorinated biphenyls (PCBs), polycyclic aromatic hydrocarbons (PAHs), and copper. Watershed development and exposures to PCBs and PAHs were generally higher for white perch in the Severn River, but similar suites of chemical contaminants were detected in the Choptank River. A broader survey of white perch within and outside Chesapeake Bay may allow determination of the extent of biliary neoplasia in this species.

White perch health relative to urbanization and habitat degradation in Chesapeake Bay tributaries. II. Hepatic and splenic macrophage aggregates.

Macrophage aggregate (MA) abundance in fish is a useful general biomarker of contaminant exposures and environmental stress. Hepatic and splenic MAs were evaluated in semi-anadromous white perch Morone americana (Gmelin, 1789) from the urbanized Severn River (S) and the more rural Choptank River (C), Chesapeake Bay. Fish were collected from different sites in the annual migratory circuit in each river that corresponded to active spawning in late winter-early spring, summer regenerating, autumn developing, and winter spawning-capable phases. An age-associated progressive increase in the total volume of MAs (MAV) was evident in the liver and spleen. Mean hepatic MAV (range in seasonal means, C: 6.4-23.1 mm3; S: 15.7-48.7 mm3) and mean splenic MAV (C: 7.3-12.6 mm3; S: 16.0-33.0 mm3) differed significantly among seasons and were significantly greater in females and in Severn River fish. Age and river were the most influential factors, suggesting that increased MAV in Severn River fish resulted from chronic exposures to higher concentrations of environmental contaminants. Hepatic MAV was directly related to the relative volume of copper granules in the liver. Less influential factors on splenic MAV included fish condition, trematode infections, and granulomas, indicating possible functional differences in MAs by organ. While organ volumes were strongly linked to gonadosomatic index (GSI) and reproductive phase, the reason for seasonal differences in MAV was less clear. Water temperature, salinity, and dissolved oxygen were not significantly related to MAV, and indicators of reproductive phase (hepatosomatic index and GSI) were significant but less important in explaining variation in MAV.

Spatiotemporal patterns in the prevalence of microscopic hepatic changes in Gulf of Mexico Tilefish (Lopholatilus chamaeleonticeps) and associations with hepatic PAHs.

Following the 2010 Deepwater Horizon blowout, demersal longline surveys were conducted across the Gulf of Mexico (GoM) continental shelf to evaluate polycyclic aromatic hydrocarbon (PAH) exposure, tissue accumulation, and health indices in demersal fishes. Tilefish (Lopholatilus chamaeleonticeps), a target species due to Gulf-wide distribution with documented high exposure to PAHs, were collected in the north central GoM at repeat stations 2012 to 2015, and from the northwest GoM, Bay of Campeche, and Yucatán Shelf in 2015 and 2016. Liver samples (n = 239) were analyzed for microscopic hepatic changes (MHCs) by a board-certified veterinary pathologist. Histological analyzes identified 14 MHCs. Prevalence of MHCs was generally uniform throughout the GoM, except for low prevalence on the Yucatán Shelf. Inflammatory and vacuolar changes were most prevalent, while pre-neoplasia and neoplasia were rare. Tilefish sampled annually in the north central GoM showed increases in inflammatory MHCs and glycogen-type vacuolar change over time, while lipid-type vacuolar change decreased over time. Short-term exposure to PAHs was assessed by measuring PAH metabolites in bile (n = 100) using high performance liquid chromatography with fluorescence detection. Longer-term accumulation of PAHs in tissue was assessed by analyzing liver (n = 111) for PAHs and alkylated homologs using QuEChERS extractions and gas chromatography tandem mass spectrometry. Six MHCs including glycogen-type vacuolar change, biliary fibrosis, foci of cellular alteration, parasites, hepatocellular atrophy, and necrosis were significantly associated with hepatic PAH accumulation in Tilefish from the northern central GoM; however, no MHCs were associated with biliary PAH metabolites. Combined with previous studies of PAH exposure and health indices in north central GoM Tilefish post-Deepwater Horizon, which also identified decreases in hepatic lipid storage and Fulton's condition factor that were correlated to increasing PAH exposure, these data indicate concerning temporal trends and changes in hepatic energy storage.

Biological and anthropogenic influences on macrophage aggregates in white perch Morone americana from Chesapeake Bay, USA.

The response of macrophage aggregates in fish to a variety of environmental stressors has been useful as a biomarker of exposure to habitat degradation. Total volume of macrophage aggregates (MAV) was estimated in the liver and spleen of white perch Morone americana from Chesapeake Bay using stereological approaches. Hepatic and splenic MAV were compared between fish populations from the rural Choptank River (n = 122) and the highly urbanized Severn River (n = 131). Hepatic and splenic MAV increased with fish age, were greater in females from the Severn River only, and were significantly greater in fish from the more polluted Severn River (higher concentrations of polycyclic aromatic hydrocarbons, organochlorine pesticides, and brominated diphenyl ethers). Water temperature and dissolved oxygen had a significant effect on organ volumes, but not on MAV. Age and river were most influential on hepatic and splenic MAV, suggesting that increased MAV in Severn River fish resulted from chronic exposures to higher concentrations of environmental contaminants and other stressors. Hemosiderin was abundant in 97% of spleens and was inversely related to fish condition and positively related to fish age and trematode infections. Minor amounts of hemosiderin were detected in 30% of livers and positively related to concentrations of benzo[a]pyrene metabolite equivalents in the bile. This study demonstrated that hepatic and splenic MAV were useful indicators in fish from the 2 tributaries with different land use characteristics and concentrations of environmental contaminants. More data are needed from additional tributaries with a wider gradient of environmental impacts to validate our results in this species.

Towards integrated modeling of the long-term impacts of oil spills.

Although great progress has been made to advance the scientific understanding of oil spills, tools for integrated assessment modeling of the long-term impacts on ecosystems, socioeconomics and human health are lacking. The objective of this study was to develop a conceptual framework that could be used to answer stakeholder questions about oil spill impacts and to identify knowledge gaps and future integration priorities. The framework was initially separated into four knowledge domains (ocean environment, biological ecosystems, socioeconomics, and human health) whose interactions were explored by gathering stakeholder questions through public engagement, assimilating expert input about existing models, and consolidating information through a system dynamics approach. This synthesis resulted in a causal loop diagram from which the interconnectivity of the system could be visualized. Results of this analysis indicate that the system naturally separates into two tiers, ocean environment and biological ecosystems versus socioeconomics and human health. As a result, ocean environment and ecosystem models could be used to provide input to explore human health and socioeconomic variables in hypothetical scenarios. At decadal-plus time scales, the analysis emphasized that human domains influence the natural domains through changes in oil-spill related laws and regulations. Although data gaps were identified in all four model domains, the socioeconomics and human health domains are the least established. Considerable future work is needed to address research gaps and to create fully coupled quantitative integrative assessment models that can be used in strategic decision-making that will optimize recoveries from future large oil spills.

Hepatobiliary PAHs and prevalence of pathological changes in Red Snapper.

Red Snapper (Lutjanus campechanus) were collected throughout the Gulf of Mexico (GoM) from 2011 to 2017 and analyzed for biliary (n = 496) fluorescent aromatic compounds (FACs), hepatic (n = 297) polycyclic aromatic hydrocarbons (PAHs) and microscopic hepatobiliary changes (MHC, n = 152). Gross and histological evaluations were conducted with liver tissues to identify and characterize pathological changes. This is the first report to interrelate hepatobiliary PAH concentrations and MHCs in Red Snapper. Hepatic PAHs measured in GoM Red Snapper ranged from 192 to 8530 ng g-1 w.w. and biliary FACs ranged from 480 to 1,100,000 ng FAC g-1 bile. Biliary FACs in Red Snapper collected along the west Florida Shelf and north central region declined after 2011 and were relatively stable until a sharp increase was noted in 2017. Increases in the PAH exposures are likely due to a number of sources including leaking infrastructure, annual spills, riverine input and the resuspension of contaminated sediments. In contrast, hepatic PAH concentrations were relatively stable indicating Red Snapper are able to maintain metabolic clearance however this energetic cost may be manifesting as microscopic hepatic changes (MHCs). Virtually all (99 %) of the evaluated Red Snapper had one to nine MHCs with an average of five coinciding changes in an individual fish. The observed changes were broadly classified as inflammatory responses, metabolic responses, degenerative lesions, nonneoplastic proliferation and neoplastic lesions. Biliary FACs were associated with parasitic infection and intracellular breakdown product accumulation such as intra-macrophage hemosiderin, lipofuscin and ceroid laden prevalence. Whereas, hepatic PAHs were associated with increased myxozoan plasmodia prevalence. This study evaluates relationships between hepatobiliary PAH concentrations and biometrics, somatic indices, condition factors and microscopic hepatic changes in Red Snapper located in the north central GoM. Together, these results may be signaling increased disease progression in Gulf of Mexico Red Snapper more than likely resulting from chronic environmental stressors including elevated PAH exposures and concentrations.

High prevalence of biliary neoplasia in white perch Morone americana: potential roles of bile duct parasites and environmental contaminants.

Recent surveys of white perch Morone americana from Chesapeake Bay, USA, revealed a high prevalence of hepatic and biliary lesions, including neoplasia, and bile duct parasites. Here, we describe lesions in the liver and gallbladder and evaluate for statistical associations among lesions, parasites, and biomarkers of chemical exposure in fish from 2 tributaries of Chesapeake Bay. Fish were collected from an estuarine site in the Choptank River (n = 122, ages 3-11), a tributary with extensive agriculture within the watershed, and the Severn River (n = 131, ages 2-16), a tributary with extensive urban development. Passive integrative samplers were deployed at the fish collection site and an upstream, non-tidal site in each river for 30 d. Intrahepatic biliary lesions observed in fish from both rivers included neoplasia (23.3%), dysplasia (16.2%), hyperplasia (46.6%), cholangitis (24.9%), and dilated ducts containing plasmodia of Myxidium sp. (24.9%). Hepatocellular lesions included foci of hepatocellular alteration (FHA, 15.8%) and neoplasia in 4 Severn River fish (2.3%). Age of fish and Myxidium sp. infections were significant risk factors for proliferative and neoplastic biliary lesions, age alone was a risk factor for FHA, and Goussia bayae infections were associated with cholangitis and cholecystitis. Lesion prevalence was higher in fish from the Severn River, which contained higher concentrations of PAHs, organochlorine pesticides, and brominated diphenyl ethers. Metabolite biomarkers indicated higher PAH exposures in Severn River fish. This study suggests Myxidium sp. as a promoter of bile duct tumors, but more data are needed to evaluate the biological effects of environmental contaminants in this species.

Spatial contrasts in hepatic and biliary PAHs in Tilefish (Lopholatilus chamaeleonticeps) throughout the Gulf of Mexico, with comparison to the Northwest Atlantic.

A multinational demersal longline survey was conducted on the Gulf of Mexico continental shelf over the years 2015 and 2016 to generate a Gulf-wide baseline of polycyclic aromatic hydrocarbon (PAH) concentrations in demersal fishes. Tilefish (Lopholatilus chamaeleonticeps) were sampled in all regions of the Gulf of Mexico for biometrics, bile, and liver. Tilefish liver was also obtained from surveys in the northwest Atlantic Ocean for comparison. Liver tissues (n = 305) were analyzed for PAHs and select alkylated homologs using QuEChERS extractions and gas chromatography tandem mass spectrometry. Bile samples (n = 225) were analyzed for biliary PAH metabolites using high-performance liquid chromatography with fluorescence detection. Spatial comparisons indicate the highest levels of PAH exposure and hepatic accumulation in the north central Gulf of Mexico, with decreasing concentrations moving from the north central Gulf counterclockwise, and an increase on the Yucatán Shelf. Hepatic PAH concentrations were similar between the Gulf of Mexico and the northwest Atlantic, however, Tilefish from the northwest Atlantic had higher concentrations and more frequent detection of carcinogenic high molecular weight PAHs. Overall, results demonstrate that PAH pollution was ubiquitous within the study regions, with recent exposure and hepatic accumulation observed in Tilefish from both the Gulf of Mexico and northwest Atlantic.

Hepatobiliary Analyses Suggest Chronic PAH Exposure in Hakes (Urophycis spp.) Following the Deepwater Horizon Oil Spill.

Prior to the Deepwater Horizon oil spill, we lacked a comprehensive baseline of oil contamination in the Gulf of Mexico's sediments, water column, and biota. Gaps in prespill knowledge limit our ability to determine the aftereffects of the Deepwater Horizon blowout or prepare to mitigate similar impacts during future oil spill disasters. We examined spatiotemporal differences in exposure to and metabolism of polycyclic aromatic hydrocarbons (PAHs) in 2 hake species (Urophycis spp.) to establish a current baseline for these ecologically important, abundant, and at-risk demersal fishes. Gulf hake (Urophycis cirrata) and southern hake (Urophycis floridana) were collected throughout the Gulf of Mexico during extensive longline surveys from 2012 to 2015. Analyses of biliary PAH metabolites and liver PAH concentrations provided evidence of exposures to di- and tricyclic compounds, with the highest concentrations measured in the northern Gulf of Mexico. Species-specific differences were not detected, but temporal trends observed in biliary PAHs suggest a decrease in acute exposures, whereas increasing liver PAHs suggest chronic exposures marked by greater assimilation than metabolism rates. To our knowledge, the present study provides the first multitissue contaminant analyses, as well as the most exhaustive biometric analyses, for both gulf and southern hakes. Though sources of exposure are complex because of multiple natural and anthropogenic PAH inputs, these results will facilitate the development of much needed health metrics for Gulf of Mexico benthos. Environ Toxicol Chem 2019;38:2740-2749. © 2019 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals, Inc. on behalf of SETAC.

Species-specific metabolism of naphthalene and phenanthrene in 3 species of marine teleosts exposed to Deepwater Horizon crude oil.

The 2 most abundant polycyclic aromatic hydrocarbons (PAHs) measured in Deepwater Horizon crude oil, naphthalene and phenanthrene, and their associated homologs have both been shown to be acutely toxic in fish. Although fish have a relatively high metabolic capacity for PAHs, hydroxylated PAH (OH-PAH) derivatives formed during the initial metabolic response can negatively impact the health of fish. Species-specific metabolism of naphthalene and phenanthrene was evaluated in 3 marine teleosts, red drum (Scianops ocellatus), Florida pompano (Trachinotus carolinus), and southern flounder (Paralichthys lethostigma). Fish were exposed to Deepwater Horizon crude oil by intraperitoneal injections at time 0 and 48 h, with bile sampling events at 24 and 72 h post injection. The data suggested metabolic induction in Florida pompano and red drum, whereas southern flounder may have demonstrated metabolic fatigue. By 24 h post injection, overall profiles of red drum and southern flounder were dominated by hydroxylated phenanthrene metabolites; conversely, the Florida pompano profiles were dominated by monohydroxylated naphthalenes. In addition, Florida pompano had faster overall relative biotransformation rates, suggesting their potential decreased susceptibility to adverse effects. Red drum and southern flounder had much lower relative biotransformation rates, indicating their probable susceptibility to adverse outcomes after naphthalene and phenanthrene exposures. To our knowledge, the present study is the first to investigate monohydroxylated PAHs in fish exposed to Deepwater Horizon oil. Environ Toxicol Chem 2017;36:3168-3176. © 2017 © 2017 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals, Inc. on behalf of SETAC.

Significant spatial variability of bioavailable PAHs in water column and sediment porewater in the Gulf of Mexico 1 year after the Deepwater Horizon oil spill.

One year after the Deepwater Horizon oil spill accident, semipermeable membrane devices (SPMDs) and polyethylene devices (PEDs) were deployed in wetland areas and coastal areas of the Gulf of Mexico (GOM) to monitor polycyclic aromatic hydrocarbons (PAHs). The measured PAH levels with the PEDs in coastal areas were 0.05-1.9 ng/L in water and 0.03-9.7 ng/L in sediment porewater. With the SPMDs, the measured PAH levels in wetlands (Barataria Bay) were 1.4-73 ng/L in water and 3.3-107 ng/L in porewater. The total PAH concentrations in the coastal areas were close to the reported baseline PAH concentrations in GOM; however, the total PAH concentrations in the wetland areas were one or two orders of magnitude higher than those reported in the coastal areas. In light of the significant spatial variability of PAHs in the Gulf's environments, baseline information on PAHs should be obtained in specific areas periodically.

Geographic specificity of Aroclor 1268 in bottlenose dolphins (Tursiops truncatus) frequenting the Turtle/Brunswick River Estuary, Georgia (USA).

Coastal marine resources are at risk from anthropogenic contaminants, including legacy persistent organic pollutants (POPs) with half-lives of decades or more. To determine if polychlorinated biphenyl (PCB) signatures can be used to distinguish among local populations of inshore bottlenose dolphins (Tursiops truncatus) along the southeastern U.S. coast, blubber from free-ranging and stranded animals were collected along the Georgia coast in 2004 and analyzed for PCB congeners using gas chromatography with electron capture and negative chemical ionization mass spectrometric detection (GC-ECD and GC-NCI-MS). Mean total PCB concentrations (77+/-34 microg/g lipid) were more than 10 fold higher and congener distributions were highly enriched in Cl(7)-Cl(10) homologs in free-ranging animals from the Turtle/Brunswick River estuary (TBRE) compared with strandings samples from Savannah area estuaries 90 km to the north. Using principal components analysis (PCA), the Aroclor 1268 signature associated with TBRE animals was distinct from that observed in Savannah area animals, and also from those in animals biopsied in other southeastern U.S estuaries. Moreover, PCB signatures in dolphin blubber closely resembled those in local preferred prey fish species, strengthening the hypothesis that inshore T. truncatus populations exhibit long-term fidelity to specific estuaries and making them excellent sentinels for assessing the impact of stressors on coastal ecosystem health.