A review of the toxicology of oil in vertebrates: what we have learned following the Deepwater Horizon oil spill.

In the wake of the Deepwater Horizon (DWH) oil spill, a number of government agencies, academic institutions, consultants, and nonprofit organizations conducted lab- and field-based research to understand the toxic effects of the oil. Lab testing was performed with a variety of fish, birds, turtles, and vertebrate cell lines (as well as invertebrates); field biologists conducted observations on fish, birds, turtles, and marine mammals; and epidemiologists carried out observational studies in humans. Eight years after the spill, scientists and resource managers held a workshop to summarize the similarities and differences in the effects of DWH oil on vertebrate taxa and to identify remaining gaps in our understanding of oil toxicity in wildlife and humans, building upon the cross-taxonomic synthesis initiated during the Natural Resource Damage Assessment. Across the studies, consistency was found in the types of toxic response observed in the different organisms. Impairment of stress responses and adrenal gland function, cardiotoxicity, immune system dysfunction, disruption of blood cells and their function, effects on locomotion, and oxidative damage were observed across taxa. This consistency suggests conservation in the mechanisms of action and disease pathogenesis. From a toxicological perspective, a logical progression of impacts was noted: from molecular and cellular effects that manifest as organ dysfunction, to systemic effects that compromise fitness, growth, reproductive potential, and survival. From a clinical perspective, adverse health effects from DWH oil spill exposure formed a suite of signs/symptomatic responses that at the highest doses/concentrations resulted in multi-organ system failure.

Crude oil cardiotoxicity to red drum embryos is independent of oil dispersion energy.

The potential bioavailability of toxic chemicals from oil spills to water column organisms such as fish embryos may be influenced by physical dispersion along an energy gradient. For example, a surface slick with minimal wave action (low energy) could potentially produce different toxic effects from high energy situations such as pressurized discharge from a blown wellhead. Here we directly compared the toxicity of water accommodated fractions (WAFs) of oil prepared with low and high mixing energy (LEWAFs and HEWAFs, respectively) using surface oil samples collected during the 2010 Deepwater Horizon spill, and embryos of a representative nearshore species, red drum (Sciaenops ocellatus). Biological effects of each WAF type was quantified with several functional and morphological indices of developmental cardiotoxicity, providing additional insight into species-specific responses to oil exposure. Although the two WAF preparations yielded different profiles of polycyclic aromatic hydrocarbons (PAHs), cardiotoxic phenotypes were essentially identical. Based on benchmark thresholds for both morphological and functional cardiotoxicity, in general LEWAFs had lower thresholds for these phenotypes than HEWAFs based on total PAH measures. However, HEWAF and LEWAF toxicity thresholds were more similar when calculated based on estimates of dissolved PAHs only. Differences in thresholds were attributable to the weathering state of the oil samples.

Estimating incident ultraviolet radiation exposure in the northern Gulf of Mexico during the Deepwater Horizon oil spill.

Millions of barrels of oil were released into the Gulf of Mexico following the 2010 explosion of the Deepwater Horizon oil rig. Polycyclic aromatic hydrocarbons (PAHs) are toxic components of crude oil, which may become more toxic in the presence of ultraviolet (UV) radiation, a phenomenon known as photo-induced toxicity. The Deepwater Horizon spill impacted offshore and estuarine sites, where biota may be co-exposed to UV and PAHs. Penetration of UV into the water column is affected by site-specific factors. Therefore, measurements and/or estimations of UV are necessary when one is assessing the risk to biota posed by photo-induced toxicity. We describe how estimates of incident UV were determined for the area impacted by the Deepwater Horizon oil spill, using monitoring data from radiometers near the spill, in conjunction with reference spectra characterizing the composition of solar radiation. Furthermore, we provide UV attenuation coefficients for both near- and offshore sites in the Gulf of Mexico. These estimates are specific to the time and location of the spill, and fall within the range of intensities utilized during photo-induced toxicity tests performed in support of the Deepwater Horizon Natural Resource Damage Assessment (NRDA). These data further validate the methodologies and findings of phototoxicity tests included in the Deepwater Horizon NRDA, while underscoring the importance of considering UV exposure when assessing possible risks following oil spills. Environ Toxicol Chem 2018;37:1679-1687. © 2018 SETAC.

Toxicity of weathered Deepwater Horizon oil to bay anchovy (Anchoa mitchilli) embryos.

The BP-contracted Deepwater Horizon Macondo well blowout occurred on 20 April 2010 and lasted nearly three months. The well released millions of barrels of crude oil into the northern Gulf of Mexico, causing extensive impacts on pelagic, benthic, and estuarine fish species. The bay anchovy (Anchoa mitchilli) is an important zooplanktivore in the Gulf, serving as an ecological link between lower trophic levels and pelagic predatory fish species. Bay anchovy spawn from May through November in shallow inshore and estuarine waters throughout the Gulf. Because their buoyant embryos are a dominant part of the inshore ichthyoplankton throughout the summer, it is likely bay anchovy embryos encountered oil in coastal estuaries during the summer and fall of 2010. Bay anchovy embryos were exposed to a range of concentrations of two field-collected Deepwater Horizon oils as high-energy and low-energy water accommodated fractions (HEWAFs and LEWAFs, respectively) for 48h. The median lethal concentrations (LC50) were lower in exposures with the more weathered oil (HEWAF, 1.48µg/L TPAH50; LEWAF, 1.58µg/L TPAH50) compared to the less weathered oil (HEWAF, 3.87µg/L TPAH50; LEWAF, 4.28µg/L TPAH50). To measure delayed mortality and life stage sensitivity between embryos and larvae, an additional 24h acute HEWAF exposure using the more weathered oil was run followed by a 24h grow-out period. Here the LC50 was 9.71µg/L TPAH50 after the grow-out phase, suggesting a toxic effect of oil at the embryonic or hatching stage. We also found that exposures prepared with the more weathered Slick B oil produced lower LC50 values compared to the exposures prepared with Slick A oil. Our results demonstrate that even relatively acute environmental exposure times can have a detrimental effect on bay anchovy embryos.

Crude oil impairs immune function and increases susceptibility to pathogenic bacteria in southern flounder.

Exposure to crude oil or its individual constituents can have detrimental impacts on fish species, including impairment of the immune response. Increased observations of skin lesions in northern Gulf of Mexico fish during the 2010 Deepwater Horizon oil spill indicated the possibility of oil-induced immunocompromisation resulting in bacterial or viral infection. This study used a full factorial design of oil exposure and bacterial challenge to examine how oil exposure impairs southern flounder (Paralichthys lethostigma) immune function and increases susceptibility to the bacteria Vibrio anguillarum, a causative agent of vibriosis. Fish exposed to oil prior to bacterial challenge exhibited 94.4% mortality within 48 hours of bacterial exposure. Flounder challenged with V. anguillarum without prior oil exposure had <10% mortality. Exposure resulted in taxonomically distinct gill and intestine bacterial communities. Mortality strongly correlated with V. anguillarum levels, where it comprised a significantly higher percentage of the microbiome in Oil/Pathogen challenged fish and was nearly non-existent in the No Oil/Pathogen challenged fish bacterial community. Elevated V. anguillarum levels were a direct result of oil exposure-induced immunosuppression. Oil-exposure reduced expression of immunoglobulin M, the major systemic fish antibody, and resulted in an overall downregulation in transcriptome response, particularly in genes related to immune function, response to stimulus and hemostasis. Ultimately, sediment-borne oil exposure impairs immune function, leading to increased incidences of bacterial infections. This type of sediment-borne exposure may result in long-term marine ecosystem effects, as oil-bound sediment in the northern Gulf of Mexico will likely remain a contamination source for years to come.

Co-exposure to sunlight enhances the toxicity of naturally weathered Deepwater Horizon oil to early lifestage red drum (Sciaenops ocellatus) and speckled seatrout (Cynoscion nebulosus).

The 2010 Deepwater Horizon oil spill resulted in the accidental release of millions of barrels of crude oil into the Gulf of Mexico. Photo-induced toxicity following co-exposure to ultraviolet (UV) radiation is 1 mechanism by which polycyclic aromatic hydrocarbons (PAHs) from oil spills may exert toxicity. Red drum and speckled seatrout are both important fishery resources in the Gulf of Mexico. They spawn near-shore and produce positively buoyant embryos that hatch into larvae in approximately 24 h. The goal of the present study was to determine whether exposure to UV as natural sunlight enhances the toxicity of crude oil to early lifestage red drum and speckled seatrout. Larval fish were exposed to several dilutions of high-energy water-accommodated fractions (HEWAFs) from 2 different oils collected in the field under chain of custody during the 2010 spill and 3 gradations of natural sunlight in a factorial design. Co-exposure to natural sunlight and oil significantly reduced larval survival compared with exposure to oil alone. Although both species were sensitive at PAH concentrations reported during the Deepwater Horizon spill, speckled seatrout demonstrated a greater sensitivity to photo-induced toxicity than red drum. These data demonstrate that even advanced weathering of slicks does not ameliorate the potential for photo-induced toxicity of oil to these species. Environ Toxicol Chem 2017;36:780-785. © 2016 SETAC.

A multiple endpoint analysis of the effects of chronic exposure to sediment contaminated with Deepwater Horizon oil on juvenile Southern flounder and their associated microbiomes.

Exposure to oiled sediments can negatively impact the health of fish species. Here, we examine the effects of chronic exposure of juvenile southern flounder, Paralichthys lethostigma, to a sediment-oil mixture. Oil:sediment mixtures are persistent over time and can become bioavailable following sediment perturbation or resuspension. Juvenile flounder were exposed for 32 days under controlled laboratory conditions to five concentrations of naturally weathered Macondo MC252 oil mixed into uncontaminated, field-collected sediments. The percent composition of individual polycyclic aromatic hydrocarbons (PAHs) of the weathered oil did not change after mixing with the sediment. Spiked exposure sediments contained 0.04-395mg/kg tPAH50 (sum of 50 individual PAH concentration measurements). Mortality increased with both exposure duration and concentration of sediment-associated PAHs, and flounder exposed to concentrations above 8mg/kg tPAH50 showed significantly reduced growth over the course of the experiment. Evident histopathologic changes were observed in liver and gill tissues of fish exposed to more than 8mg/kg tPAH50. All fish at these concentrations showed hepatic intravascular congestion, macrovesicular hepatic vacoulation, telangiectasia of secondary lamellae, and lamellar epithelial proliferation in gill tissues. Dose-dependent upregulation of Cyp1a expression in liver tissues was observed. Taxonomic analysis of gill and intestinal commensal bacterial assemblages showed that exposure to oiled sediments led to distinct shifts in commensal bacterial population structures. These data show that chronic exposure to environmentally-relevant concentrations of oiled sediments produces adverse effects in flounder at multiple biological levels.