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.

Exposure to Crude Oil from the Deepwater Horizon Oil Spill Impairs Oil Avoidance Behavior without Affecting Olfactory Physiology in Juvenile Mahi-Mahi (Coryphaena hippurus).

The understanding of the detection threshold and behavioral response of fishes in response to crude oil is critical to predicting the effects of oil spills on wild fish populations. The Deepwater Horizon oil spill released approximately 4.9 million barrels of crude oil into the northern Gulf of Mexico in 2010, overlapping spatially and temporally with the habitat of many pelagic fish species. Yet, it is unknown whether highly migratory species, such as mahi-mahi (Coryphaena hippurus), might detect and avoid oil contaminated waters. We tested the ability of control and oil-exposed juvenile mahi-mahi (15-45 mm) to avoid two dilutions of crude oil in a two-channel flume. Control fish avoided the higher concentration (27.1 µg/L Σ50PAH), while oil-exposed (24 h, 18.0 µg/L Σ50PAH) conspecifics did not. Electro-olfactogram (EOG) data demonstrated that both control and oil-exposed (24 h, 14.5 µg/L Σ50PAH) juvenile mahi-mahi (27-85 mm) could detect crude oil as an olfactory cue and that oil-exposure did not affect the EOG amplitude or duration in response to oil or other cues. These results show that a brief oil exposure impairs the ability of mahi-mahi to avoid oil and suggests that this alteration likely results from injury to higher order central nervous system processing rather than impaired olfactory physiology.

Damsels in Distress: Oil Exposure Modifies Behavior and Olfaction in Bicolor Damselfish (Stegastes partitus).

In fishes, olfactory cues evoke behavioral responses that are crucial to survival; however, the receptors, olfactory sensory neurons, are directly exposed to the environment and are susceptible to damage from aquatic contaminants. In 2010, 4.9 million barrels of crude oil were released into the northern Gulf of Mexico from the Deepwater Horizon disaster, exposing marine organisms to this environmental contaminant. We examined the ability of bicolor damselfish (Stegastes partitus), exposed to the water accommodated fraction (WAF) of crude oil, to respond to chemical alarm cue (CAC) using a two-channel flume. Control bicolor damselfish avoided CAC in the flume choice test, whereas WAF-exposed conspecifics did not. This lack of avoidance persisted following 8 days of control water conditions. We then examined the physiological response to CAC, brine shrimp rinse, bile salt, and amino acid cues using the electro-olfactogram (EOG) technique and found that WAF-exposed bicolor damselfish were less likely to detect CAC as an olfactory cue but showed no difference in EOG amplitude or duration compared to controls. These data indicate that a sublethal WAF exposure directly modifies detection and avoidance of CAC beyond the exposure period and may suggest reduced predator avoidance behavior in oil-exposed fish in the wild.

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.

Environmental and climate variability drive population size of annual penaeid shrimp in a large lagoonal estuary.

Species with short life spans frequently show a close relationship between population abundance and environmental variation making these organisms potential indicator species of climatic variability. White (Penaeus setiferus), brown (P. aztecus), and pink (P. duorarum) penaeid shrimp typically have an annual life history and are of enormous ecological, cultural, and economic value to the southeastern United States and Gulf of Mexico. Within North Carolina, all three species rely on the Pamlico Sound, a large estuarine system that straddles Cape Hatteras, one of the most significant climate and biogeographic breaks in the world, as a nursery area. These characteristics make penaeid species within the Pamlico Sound a critical species-habitat complex for assessing climate impacts on fisheries. However, a comprehensive analysis of the influence of the environmental conditions that influence penaeid shrimp populations has been lacking in North Carolina. In this study, we used more than 30 years of data from two fishery-independent trawl surveys in the Pamlico Sound to examine the spatial distribution and abundance of adult brown, white, and pink shrimp and the environmental drivers associated with adult shrimp abundance and juvenile brown shrimp recruitment using numerical models. Brown shrimp recruitment models demonstrate that years with higher temperature, salinity, offshore windstress, and North Atlantic Oscillation phase predict increased abundance of juveniles. Additionally, models predicting adult brown, white, and pink shrimp abundance illustrate the importance of winter temperatures, windstress, salinity, the North Atlantic Oscillation index, and the abundance of spawning adult populations from the previous year on shrimp abundance. Our findings show a high degree of variability in shrimp abundance is explained by climate and environmental variation and indicate the importance of understanding these relationships in order to predict the impact of climate variability within ecosystems and develop climate-based adaptive management strategies for marine populations.

Seasonal variations in the physiological stress response to discrete bouts of aerial exposure in the little skate, Leucoraja erinacea.

Aerial exposure and acute thermal stress have been shown to elicit profound physiological disruptions in obligate water-breathing teleosts. However, no study has investigated these responses in an elasmobranch. To address this, venous blood samples were collected and evaluated from little skates (Leucoraja erinacea) subjected to discrete aerial exposure durations (0, 15, and 50 min) coupled with differing abrupt thermal changes (gradient between seawater and air; winter: ΔT=-3 °C; summer: ΔT=+9 °C) in two distinct laboratory studies. In general, blood acid-base properties (e.g. decline in pH; elevation in PCO(2)) and select metabolites (elevated whole-blood lactate) and electrolytes (elevated plasma K(+)) were significantly disrupted by aerial exposure, and were most disturbed after skates were exposed to air for 50 min. However, the magnitude of the blood acid-base perturbations, metabolic contribution to the resulting blood acidosis, elevations to ionic and metabolic parameters, and delayed mortality were more extreme during the summer study, suggesting that acute thermal stress exacerbates the physiological impairments associated with aerial exposure in little skates. Conversely, a reduced thermal gradient (from seawater to air) may attenuate the magnitude of metabolic and ionic perturbations, resulting in a high physiological threshold for coping with extended aerial exposure.

Magnesium transport in the aglomerular kidney of the Gulf toadfish (Opsanus beta).

Despite having an aglomerular kidney, Gulf toadfish can survive in water ranging from nearly fresh up to 70 parts per thousand salinity. In hyperosmotic environments, the major renal function is to balance the passive Mg2+ load from the environment with an equal excretion. However, the molecular transporters involved in Mg2+ secretion are poorly understood. We investigated whether environmental MgCl2 alone or in combination with elevated salinity affected transcriptional regulation of genes classically involved in renal Mg2+ secretion (slc41a1, slc41a3, cnnm3) together with three novel genes (trpm6, trpm7, claudin-19) and two isoforms of the Na+/K+-ATPase α-subunit (nka-α1a, nka-α1b). First, toadfish were acclimated to 5, 9, 35, or 60 ppt water (corresponding to ~ 7, 13, 50 and 108 mmol L-1 ambient [Mg2+], respectively) and sampled at 24 h or 9 days. Next, the impact of elevated ambient [Mg2+] was explored by exposing toadfish to control (50 mmol L-1 Mg2+), or elevated [Mg2+] (100 mmol L-1) at a constant salinity for 7 days. Mg2+ levels in this experiment corresponded with levels in control and hypersaline conditions in the first experiment. A salinity increase from 5 to 60 ppt stimulated the level of all investigated transcripts in the kidney. In Mg2+-exposed fish, we observed a 14-fold increase in the volume of intestinal fluids and elevated plasma osmolality and [Mg2+], suggesting osmoregulatory challenges. However, none of the renal gene targets changed expression compared with the control group. We conclude that transcriptional regulation of renal Mg2+ transporters is induced by elevated [Mg2+] in combination with salinity rather than elevated ambient [Mg2+] alone.

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.

Physiological stress and post-release mortality of white marlin (Kajikia albida) caught in the United States recreational fishery.

White marlin, a highly migratory pelagic marine fish, support important commercial and recreational fisheries throughout their range in the tropical and subtropical Atlantic Ocean. More than 10 000 individuals can be caught annually in the United States recreational fishery, of which the vast majority are captured on circle hooks and released alive. The probability of post-release mortality of white marlin released from circle hooks has been documented to be <0.02, but the associated physiological stress resulting from capture and handling techniques has not been characterized despite its importance for understanding the health of released fish. We examined the physiological response of 68 white marlin caught on circle hooks in the recreational fishery and followed the fate of 22 of these fish with pop-up satellite archival tags programmed to release after 30 days. Measures of plasma sodium, chloride, glucose and lactate concentrations taken from fish that were briefly and consistently (mean = 120 s, standard deviation = 40 s) removed from the water increased with angling time, but post-release mortality was inversely related to angling time. The probability of post-release mortality was predicted by elevated plasma potassium concentrations and was more than 10 times greater than has been previously reported for white marlin caught on circle hooks that were not removed from the water. This disparity in estimates of post-release mortality suggests that removal of fish from the water for physiological sampling greatly heightens stress, disrupts homeostasis and thus increases the probability of post-release mortality. Our results demonstrate that elevated concentrations of plasma potassium predict mortality in white marlin and that the probability of post-release mortality is highly dependent on post-capture handling procedures.