Brief Oil Exposure Reduces Fitness in Wild Gulf of Mexico Mahi-Mahi (Coryphaena hippurus).

The Deepwater Horizon (DWH) disaster released 3.19 million barrels of crude oil into the Gulf of Mexico (GOM) in 2010, overlapping the habitat of pelagic fish populations. Using mahi-mahi (Coryphaena hippurus)─a highly migratory marine teleost present in the GOM during the spill─as a model species, laboratory experiments demonstrate injuries to physiology and behavior following oil exposure. However, more than a decade postspill, impacts on wild populations remain unknown. To address this gap, we exposed wild mahi-mahi to crude oil or control conditions onboard a research vessel, collected fin clip samples, and tagged them with electronic tags prior to release into the GOM. We demonstrate profound effects on survival and reproduction in the wild. In addition to significant changes in gene expression profiles and predation mortality, we documented altered acceleration and habitat use in the first 8 days oil-exposed individuals were at liberty as well as a cessation of apparent spawning activity for at least 37 days. These data reveal that even a brief and low-dose exposure to crude oil impairs fitness in wild mahi-mahi. These findings offer new perspectives on the lasting impacts of the DWH blowout and provide insight about the impacts of future deep-sea oil spills.

Ultraviolet avoidance by embryonic buoyancy control in three species of marine fish.

Pelagic fish embryos are thought to float in or near surface waters for the majority of their development and are presumed to have little to no control over their mobility, rendering these embryos at high risk for damages associated with surface stressors such as ultraviolet radiation (UVR). We recently challenged these long-standing paradigms by characterizing a potential mechanism of stressor avoidance in early-life stage mahi-mahi (Coryphaena hippurus) in which embryos sense external cues, such as UVR, and modify their buoyancy to reduce further exposure. It is unknown whether embryos of other marine fish with pelagic spawning strategies have similar capabilities. To fill this knowledge gap, we investigated buoyancy change in response to UVR in three additional species of marine fish that utilize a pelagic spawning strategy: yellowfin tuna (Thunnus albacares), red snapper (Lutjanus campechanus), and cobia (Rachycentron canadum). Embryos of all three species displayed increased specific gravity and loss of buoyancy after exposures to environmentally relevant doses of UVR, a response that may be ubiquitous to fish with pelagic embryos. To gain further insight into this response, we investigated recovery of buoyancy, oxygen consumption, energy depletion, and photolyase induction in response to UVR exposures in at least one of the three species listed above.

Physiological Responses of Fish to Oil Spills.

Millions of tons of oil are spilled in aquatic environments every decade, and this oil has the potential to greatly impact fish populations. Here, we review available information on the physiological effects of oil and polycyclic aromatic hydrocarbons on fish. Oil toxicity affects multiple biological systems, including cardiac function, cholesterol biosynthesis, peripheral and central nervous system function, the stress response, and osmoregulatory and acid-base balance processes. We propose that cholesterol depletion may be a significant contributor to impacts on cardiac, neuronal, and synaptic function as well as reduced cortisol production and release. Furthermore, it is possible that intracellular calcium homeostasis-a part of cardiotoxic and neuronal function that is affected by oil exposure-may be related to cholesterol depletion. A detailed understanding of oil impacts and affected physiological processes is emerging, but knowledge of their combined effects on fish in natural habitats is largely lacking. We identify key areas deserving attention in future research.

Impacts of deepwater horizon oil on fish.

An explosion on the Deepwater Horizon (DWH) oil rig in 2010 lead to the largest marine oil spill to occur in US history, resulting in significant impacts to the ecosystems and organisms in the Northern Gulf of Mexico (GoM). The present review sought to summarize and discuss findings from the 50+ peer-reviewed publications reporting effects of DWH oil exposure on teleost fish, and concludes that oil toxicity is a multi-target, multi-organ syndrome with substantial species-specific sensitivity differences. Of the 15 species tested with characterized exposures, 20% show effects at concentrations <1 µg l-1 while 50% display effects at <8.6 µg l-1 ΣPAH50, concentrations well within the range of reported environmental levels during the spill. Cardiotoxic effects are among the most frequently reported endpoints in DWH oil exposure studies and are thought to have significant downstream effects on fitness and survival. However, additional and possibly cardio-toxic independent impacts on sensory function and behavior are reported at very low exposure concentrations (< 1 µg l-1 ∑PAH50) and are clearly deserving of further study. Available information about modes of action leading to different categories of effects are summarized in the present review. An overview of the literature illustrates that early life stages (ELS) are approximately 1-order of magnitude more sensitive than corresponding later life stages, but also illustrates that adults can be impacted at concentrations as low as 4 µg l-1 ΣPAH50. The majority of studies exploring DWH oil toxicity in fish are performed using acute exposures (1-2 days), mid-range test temperatures (26-28 °C) and measure effects at the molecular to organismal levels, leaving a pressing need for more long-term exposures, exposures at the upper and lower levels of GoM relevant temperatures, and studies investigating population level impacts.

Effects of corexit 9500A and Corexit-crude oil mixtures on transcriptomic pathways and developmental toxicity in early life stage mahi-mahi (Coryphaena hippurus).

Crude oil and polycyclic aromatic hydrocarbon (PAH) exposure in early life stage fish has been well-characterized to induce phenotypic malformations such as altered heart development and other morphological impacts. The effects of chemical oil dispersants on toxicity are more controversial. To better understand how chemical dispersion of oil can impact toxicity in pelagic fish, embryos of mahi-mahi (Coryphaena hippurus) were exposed to three concentrations of the chemical dispersant Corexit 9500A, or Corexit 9500A-oil mixtures (chemically enhanced water accommodated fractions: CEWAF) of Deepwater Horizon crude oil for 48 h. RNA sequencing, gene ontology enrichment, and phenotypic measurements were conducted to assess toxicity. Exposure to Corexit 9500A altered expression of less than 50 genes at all concentrations (2.5, 5, and 10 mg/L nominal concentration) and did not induce acute mortality or phenotypic malformations, corroborating other studies showing minimal effects of Corexit 9500A on developing mahi-mahi embryos. CEWAF preparations contained environmentally relevant ∑PAH concentrations ranging from 1.4 to 3.1 µg/L and similarly did not alter larval morphology. Differentially expressed genes and significantly altered pathways related to cardiotoxicity, visual impairments, and Ca2+ homeostasis reinforced previous work that expression of genes associated with the heart and eye are highly sensitive molecular endpoints in oil-exposed early life stage fish. Differential expression and gene ontology pathways were similar across the three CEWAF treatments, indicating that increased chemical dispersion did not alter molecular outcomes within the range tested here. In addition, significant sublethal molecular responses occurred in the absence of observable phenotypic changes to the heart, indicating that effects of oil on early life stage fish may not be completely dependent on cardiac function.

Deepwater Horizon crude oil exposure alters cholesterol biosynthesis with implications for developmental cardiotoxicity in larval mahi-mahi (Coryphaena hippurus).

During the spring and summer of 2010, the Deepwater Horizon (DWH) oil well released over three million barrels of crude oil into the Gulf of Mexico. As the oil dispersed it contaminated ecosystems that support numerous Gulf species including mahi-mahi (Coryphaena hippurus). The timing of the spill, and location of the surface slick, coincided with the spawning of many species in the region, raising concerns over embryonic and larval exposure. Numerous abnormalities due to crude oil exposure have been documented in fish early life stages, including cardiotoxicity; however, knowledge of the molecular mechanisms that cause these phenotypes is still limited. Several transcriptomic studies have presented cholesterol biosynthesis as one of the top enriched pathways following PAH exposure. In this study we exposed mahi-mahi embryos to DWH oil collected from the surface slick. At exposures ranging from ∑PAH 1.69 µg/L to ∑PAH 5.99 µg/L, the resulting larvae demonstrated significant increases in farnesyl-diphosphate farnesyltransferase 1 (fdft1) and an upward trend in 3-Hydroxy-3-Methylglutaryl-CoA Reductase (hmgcr) expression, genes that encode key enzymes in the cholesterol biosynthetic pathway. In addition to the increased expression of genes in cholesterol biosynthetic pathway, a significant decrease in total cholesterol was observed in larval homogenates, at ∑PAH 8.3 µg/L. These data confirm earlier transcriptomic studies and show that oil may diminish cholesterol and adversely impact numerous cellular functions due to altered membrane stability.

Changes in microRNA-mRNA Signatures Agree with Morphological, Physiological, and Behavioral Changes in Larval Mahi-Mahi Treated with Deepwater Horizon Oil.

In this study, we performed a systematic evaluation of global microRNA-mRNA interactions associated with the developmental toxicity of Deepwater Horizon oil using a combination of integrated mRNA and microRNA deep sequencing, expression profiling, gene ontology enrichment, and functional predictions by a series of advanced bioinformatic tools. After exposure to water accommodated fraction (WAF) of both weathered slick oil (0.5%, 1%, and 2%) and source oil (0.125%, 0.25%, and 0.5%) from the Deep Water Horizon oil spill, four dose-dependent miRNAs were identified, including three up-regulated (miR-23b, miR-34b, and miR-181b) and one down-regulated miRNAs (miR-203a) in mahi-mahi hatchings exposed from 6 h postfertilization (hpf) to 48 hpf. Consistent with morphological, physiological, and behavioral changes, the target genes of these miRNAs were largely involved in the development of the cardiovascular, visual, nervous system and associated toxicity pathways, suggesting that miRNAs play an essential role in regulating the responses to oil exposure. The results obtained from this study improve our understanding of the role of miRNAs and their target genes in relation to dose-dependent oil toxicity and provide the potential of using miRNAs as novel biomarkers in future oil studies.

Combined effects of hypoxia or elevated temperature and Deepwater Horizon crude oil exposure on juvenile mahi-mahi swimming performance.

This study examined potential interactive effects of co-exposure to Deepwater Horizon (DWH) crude oil (∼30 µg L-1 ΣPAHs) for 24 h and either hypoxia (2.5 mg O2 L-1; 40% O2 saturation) or elevated temperature (30 °C) on the swimming performance of juvenile mahi-mahi (Coryphaena hippurus). Additionally, effects of shorter duration exposures to equal or higher doses of oil alone either prior to swimming or during the actual swim trial itself were examined. Only exposure to hypoxia alone or combined with crude oil elicited significant decreases in critical swimming speed (Ucrit) and to a similar extent (∼20%). In contrast, results indicate that elevated temperature might ameliorate some effects of oil exposure on swimming performance and that effects of shorter duration exposures are either reduced or delayed.

Combined effects of oil exposure, temperature and ultraviolet radiation on buoyancy and oxygen consumption of embryonic mahi-mahi, Coryphaena hippurus.

The Deepwater Horizon oil spill occurred in the summer of 2010 and coincided with the spawning window of the ecologically and economically important pelagic fish mahi-mahi (Coryphaena hippurus). During summer months, early life stage mahi-mahi were likely also exposed to other naturally occurring stressors such as increased temperature and ultraviolet radiation (UV). Previous research has shown that co-exposure to oil and additional natural stressors can affect the timing and duration of negative buoyancy in mahi-mahi embryos. The current study aimed to elucidate the factors affecting the onset of negative buoyancy and to also explore possible mechanisms behind buoyancy change. Embryos co-exposed to oil and/or increased temperature and UV radiation displayed early onset of negative buoyancy with concurrent increases in oxygen consumption and sinking rates, which are normally only seen during the period directly preceding hatch. Results also suggest a behavioral response in which embryos avoid UV radiation by sinking down the water column but reestablish positive buoyancy once the UV radiation is removed. These findings imply that embryos can dynamically change their position in the water column in response to external cues and thus may have much greater control over buoyancy than previously thought.

Assessment of early life stage mahi-mahi windows of sensitivity during acute exposures to Deepwater Horizon crude oil.

Windows of exposure to a weathered Deepwater Horizon oil sample (slick A) were examined for early life stage mahi-mahi (Coryphaena hippurus) to determine whether there are developmental periods of enhanced sensitivity during the course of a standard 96-h bioassay. Survival was assessed at 96 h following oil exposures ranging from 2 h to 96 h and targeting 3 general periods of development, namely the prehatch phase, the period surrounding hatch, and the posthatch phase. In addition, 3 different oil preparations were used: high- and low-energy water accommodated fractions of oil and very thin surface slicks of oil (∼1 µm). The latter 2 were used to distinguish between effects due to direct contact with the slick itself and the water underlying the slick. Considering the data from all 3 exposure regimes, it was determined that the period near or including hatch was likely the most sensitive. Furthermore, toxicity was not enhanced by direct contact with slick oil. These findings are environmentally relevant given that the concentrations of polycyclic aromatic hydrocarbons eliciting mortality from exposures during the sensitive periods of development were below or near concentrations measured during the active spill phase. Environ Toxicol Chem 2017;36:1887-1895. © 2016 SETAC.

Effects of Deepwater Horizon crude oil exposure, temperature and developmental stage on oxygen consumption of embryonic and larval mahi-mahi (Coryphaena hippurus).

The timing and location of the 2010 Deepwater Horizon (DWH) incident within the Gulf of Mexico resulted in crude oil exposure of many commercially and ecologically important fish species, such as mahi-mahi (Coryphaena hippurus), during the sensitive early life stages. Previous research has shown that oil exposure during the embryonic stage of predatory pelagic fish reduces cardiac function - a particularly important trait for fast-swimming predators with high aerobic demands. However, it is unclear whether reductions in cardiac function translate to impacts on oxygen consumption in these developing embryos and larvae. A 24-channel optical-fluorescence oxygen-sensing system for high-throughput respiration measurements was used to investigate the effects of oil exposure, temperature and developmental stage on oxygen consumption rates in embryonic and larval mahi-mahi. Oil-exposed developing mahi-mahi displayed increased oxygen consumption, despite clear cardiac deformities and bradycardia, confirming oxygen uptake and delivery from a source other than the circulatory system. In addition to metabolic rate measurements, nitrogenous waste excretion was measured to test the hypothesis that increased energy demand was fueled by protein catabolism. This is the first study to our knowledge that demonstrates increased energy demand and energy depletion in oil-exposed developing mahi-mahi.

Time- and Oil-Dependent Transcriptomic and Physiological Responses to Deepwater Horizon Oil in Mahi-Mahi (Coryphaena hippurus) Embryos and Larvae.

The Deepwater Horizon (DWH) oil spill contaminated the spawning habitats for numerous commercially and ecologically important fishes. Exposure to the water accommodated fraction (WAF) of oil from the spill has been shown to cause cardiac toxicity during early developmental stages across fishes. To better understand the molecular events and explore new pathways responsible for toxicity, RNA sequencing was performed in conjunction with physiological and morphological assessments to analyze the time-course (24, 48, and 96 h post fertilization (hpf)) of transcriptional and developmental responses in embryos/larvae of mahi-mahi exposed to WAF of weathered (slick) and source DWH oils. Slick oil exposure induced more pronounced changes in gene expression over time than source oil exposure. Predominant transcriptomic responses included alteration of EIF2 signaling, steroid biosynthesis, ribosome biogenesis and activation of the cytochrome P450 pathway. At 96 hpf, slick oil exposure resulted in significant perturbations in eye development and peripheral nervous system, suggesting novel targets in addition to the heart may be involved in the developmental toxicity of DHW oil. Comparisons of changes of cardiac genes with phenotypic responses were consistent with reduced heart rate and increased pericardial edema in larvae exposed to slick oil but not source oil.