The proposed work addresses GoMRI Research Theme 3: Environmental effects of the petroleum/dispersant system on the sea floor, water column, coastal waters, beach sediments, wetlands, marshes, and organisms; and the science of ecosystem recovery, with the overall objectives of elucidating the mechanism(s) by which exposure to DWH oil may be interfering with the marine vertebrate stress response and determining the trajectory of recovery. The central hypothesis of this proposal is that there are multiple pathways by which PAHs found in DWH oil may disrupt the marine vertebrate stress response, due to the complexity of both the stress response and the oil mixture, and that recovery will be pathway-dependent.
The central hypothesis is based on past and current research that suggests PAHs found in oil interfere with the typical vertebrate stress response, an adaptive response that serves to promote survival and restore physiological systems to homeostasis. In marine vertebrates, exposure to pollutants typically results in release of the steroid glucocorticoid hormone, cortisol, into the circulation. However, some studies have shown that circulating cortisol does not increase in fish chronically exposed to PAHs. Instead, fish in contaminated environments have reduced cortisol levels at capture compared to fish collected from clean environments, suggesting a disruption in the complicated endocrine axis that regulates cortisol biosynthesis. Exemplifying this issue is the recent finding that bottlenose dolphins captured in Barataria Bay, Louisiana, an area that received substantial oiling from DWH over an extended period of time, have significantly reduced circulating cortisol levels in response to capture stress compared to dolphins captured from Sarasota Bay, Florida, where no oil was observed following the DWH spill. While studies on fish and marine mammals support a disruption in cortisol biosynthesis, the effect of PAHs on the stress response is complicated with other studies showing significant increases in plasma cortisol in response to acute and chronic PAH exposure.
On this background, the ultimate goal of the proposed work is to develop a greater understanding of DWH oil-induced toxicity and ascertain the extent to which the combination of PAHs in DWH oil interferes with the vertebrate stress response. We have developed an Adverse Outcome Pathway (AOP), a mechanism-based model for ecological risk assessment, to inform the scientific questions that will be addressed in the present proposal. The AOP for this proposal links molecular initiating events (MIEs; processes that control cortisol biosynthesis and receptor levels) that may be used as sensitive indicators of DWH oil exposure and predictors of exposure consequences to apical endpoints at the level of the individual (effects on metabolism and behavior) and population (effects on abundance and diversity). Uncertainty in the proposed AOP linkages form the basis for the scientific questions that will be addressed.
To fully assess the impacts of DWH oil on the vertebrate stress response and the trajectory for recovery, the proposed activities integrate molecular, cellular, gland/organ and whole animal physiological and behavioral studies using a benthic marine teleost, the Gulf toadfish, a resident of the Gulf of Mexico. These studies will evaluate multiple pathways (e.g., pituitary fatigue, reduced receptor sensitivity, disruption or overstimulation of cortisol biosynthesis) and the consequence of these changes at the whole animal level (e.g., changes in carbohydrate metabolism, immune capacity and responses to natural stresses such as predation and social interaction). These pathways and endpoints will be evaluated in both short- and long-term exposures to DWH oil and individual PAH constituents. Each exposure will be followed by a complementary recovery period (i.e., no oil or PAH exposure) to assess the recovery trajectory.
The PI has experience with oil toxicity studies on toadfish from efforts during 2013-2015 associated with the Natural Resource Damage Assessment (NRDA). The proposed activities are based on findings from these NRDA related efforts and are an outgrowth of endpoints and AOPs that would not normally be examined in NRDA testing. Dr. McDonald and her team are well-positioned to carry out the proposed research as she has established facilities and extensive experience in marine fish molecular biology, neuroendocrinology, transport and binding kinetics, pharmacology, and whole animal physiology and behavior. In particular, Dr. McDonald is an expert in stress physiology and has authored >20 publications on the stress response and the role of cortisol in the control of fish physiology and behavior. The majority of the methodologies used in the proposed work have been applied successfully by McDonald and her team, ensuring that the proposed work can be completed successfully.
The proposed research is innovative as it will be the first to determine the effect of DWH oil on the many different and integrated components of the stress response. We expect that experimental outcomes will greatly contribute to our overall understanding of the mechanism(s) of DWH oil toxicity on the stress response of marine fish and will allow us to ascertain the trajectory of recovery. Given the conservation in the stress response between marine mammals and fish, studying the impact and mechanism of toxicity of DWH oil on the stress response of marine fish, which can be easily obtained and manipulated experimentally, will also contribute to our understanding of the mode of action in marine mammals, which are of great public concern.