Polycyclic Aromatic Hydrocarbon Exposure, Hepatic Accumulation, and Associated Health Impacts in Gulf of Mexico Tilefish (Lopholatilus chamaeleonticeps)

Following the 2010 Deepwater Horizon oil spill, systematic demersal longline surveys were conducted throughout the Gulf of Mexico (GoM) continental shelf to evaluate polycyclic aromatic hydrocarbon (PAH) exposure, hepatic accumulation, and health indices in demersal fishes. Tilefish (Lopholatilus chamaeleonticeps) were chosen as a target species due to high vulnerability to environmental disturbance, commercial importance, Gulf-wide distribution, and documented high exposure to PAHs post-Deepwater Horizon. Over 200 Tilefish were sampled in the north central GoM at repeat stations from 2012 to 2017, and from the northwest GoM, southwest GoM, Bay of Campeche, and Yucatán Shelf over years 2015 and 2016. Tilefish were sampled for biometrics, and bile and liver for contaminant analyses. Tilefish livers were also obtained from demersal longline surveys in the northwest Atlantic Ocean for comparison. Bile samples were analyzed via high performance liquid chromatography with fluorescence (HPLC-F) detection for PAH metabolites, a biomarker of short-term (e.g. days) exposure to PAHs. Longer-term accumulation of PAHs was assessed by analyzing liver samples for PAHs and alkylated homologs using the Quick, Easy, Cheap, Effective, Rugged, and Safe (QuEChERS) extraction method and gas chromatography tandem mass spectrometry (GC-MS/MS). Fish health indices including Fulton’s condition factor and total liver lipid were evaluated. Liver samples were also analyzed for microscopic hepatic changes (MHCs) by a board-certified veterinary pathologist. Over the six-year time series in the north central GoM, exposure to petrogenic PAHs increased by an average of 178%, correlating with an average 22% decline in Fulton’s condition factor. The decline in Fulton’s condition factor was positively correlated with a 53% decline in percent liver lipid. There was no accumulation of PAHs in liver tissue over time. Together, these results suggest that increasing and chronic PAH exposure and resultant elevated xenobiotic metabolism may be taxing the energy budgets of Tilefish, particularly adult females, with potentially negative effects on fitness. Gulf-wide spatial comparisons revealed the highest PAH exposure, and concentrations in liver tissue in the north central GoM, with decreasing concentrations from the north central Gulf counterclockwise, and an increase on the Yucatán Shelf. Total hepatic PAH concentrations were similar between the GoM 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 PAH exposure and measurable hepatic PAH concentrations observed in Tilefish from both the GoM and northwest Atlantic. Histological examinations identified 14 MHCs, ranging from mild to severe (i.e. neoplasia). 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. Ten MHCs including glycogen and lipid-type vacuolar change, biliary fibrosis, increased pigmented macrophage aggregates, granulomas, foci of cellular alteration, inflammation with lymphocytic aggregation, parasites, hepatocellular atrophy, and necrosis were associated with hepatic PAH accumulation. In the north central GoM, where Tilefish were sampled at repeat stations 2012 to 2015, inflammatory MHCs and glycogen-type vacuolar change increased over time, while lipid-type vacuolar change decreased, potentially indicating a switch from preferential storage of hepatic lipids to hepatic glycogen. 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 that were correlated to increasing PAH exposure, these data indicate concerning temporal trends and changes in hepatic energy metabolism. The results of this dissertation indicate chronic and increasing exposure of GoM Tilefish to petrogenic PAHs with significant effects on health indices. Specifically, in the north central GoM where PAH exposure and hepatic accumulation are highest Gulf-wide, the time series of PAH exposure and associated health effects indicates increasing exposure, alterations in hepatic energy storage, and decreasing Fulton’s condition factor. The implications are serious for individual health, reproductive capacity, and population productivity of GoM Tilefish. Due to their economic and ecological value, and signs of chronic PAH exposure and accumulating impact, the GoM Tilefish population, particularly individuals from north central Gulf, should be closely monitored until a new, stable baseline is achieved