Daniel D. Benetti

Deepwater Horizon crude oil impacts the developing hearts of large predatory pelagic fish

Significance The 2010 Deepwater Horizon (MC252) disaster in the northern Gulf of Mexico released more than 4 million barrels of crude oil. Oil rose from the ocean floor to the surface where many large pelagic fish spawn. Here we describe the impacts of field-collected oil samples on the rapidly developing embryos of warm-water predators, including bluefin and yellowfin tunas and an amberjack. For each species, environmentally relevant MC252 oil exposures caused serious defects in heart development. Moreover, abnormalities in cardiac function were highly consistent, indicating a broadly conserved developmental crude oil cardiotoxicity. Losses of early life stages were therefore likely for Gulf populations of tunas, amberjack, swordfish, billfish, and other large predators that spawned in oiled surface habitats. The Deepwater Horizon disaster released more than 636 million L of crude oil into the northern Gulf of Mexico. The spill oiled upper surface water spawning habitats for many commercially and ecologically important pelagic fish species. Consequently, the developing spawn (embryos and larvae) of tunas, swordfish, and other large predators were potentially exposed to crude oil-derived polycyclic aromatic hydrocarbons (PAHs). Fish embryos are generally very sensitive to PAH-induced cardiotoxicity, and adverse changes in heart physiology and morphology can cause both acute and delayed mortality. Cardiac function is particularly important for fast-swimming pelagic predators with high aerobic demand. Offspring for these species develop rapidly at relatively high temperatures, and their vulnerability to crude oil toxicity is unknown. We assessed the impacts of field-collected Deepwater Horizon (MC252) oil samples on embryos of three pelagic fish: bluefin tuna, yellowfin tuna, and an amberjack. We show that environmentally realistic exposures (1–15 µg/L total PAH) cause specific dose-dependent defects in cardiac function in all three species, with circulatory disruption culminating in pericardial edema and other secondary malformations. Each species displayed an irregular atrial arrhythmia following oil exposure, indicating a highly conserved response to oil toxicity. A considerable portion of Gulf water samples collected during the spill had PAH concentrations exceeding toxicity thresholds observed here, indicating the potential for losses of pelagic fish larvae. Vulnerability assessments in other ocean habitats, including the Arctic, should focus on the developing heart of resident fish species as an exceptionally sensitive and consistent indicator of crude oil impacts.

Acute embryonic or juvenile exposure to Deepwater Horizon crude oil impairs the swimming performance of mahi-mahi (Coryphaena hippurus).

The Deepwater Horizon incident likely resulted in exposure of commercially and ecologically important fish species to crude oil during the sensitive early life stages. We show that brief exposure of a water-accommodated fraction of oil from the spill to mahi-mahi as juveniles, or as embryos/larvae that were then raised for ∼25 days to juveniles, reduces their swimming performance. These physiological deficits, likely attributable to polycyclic aromatic hydrocarbons (PAHs), occurred at environmentally realistic exposure concentrations. Specifically, a 48 h exposure of 1.2 ± 0.6 μg L(-1) ΣPAHs (geometric mean ± SEM) to embryos/larvae that were then raised to juvenile stage or a 24 h exposure of 30 ± 7 μg L(-1) ΣPAHs (geometric mean ± SEM) directly to juveniles resulted in 37% and 22% decreases in critical swimming velocities (Ucrit), respectively. Oil-exposed larvae from the 48 h exposure showed a 4.5-fold increase in the incidence of pericardial and yolk sac edema relative to controls. However, this larval cardiotoxicity did not manifest in a reduced aerobic scope in the surviving juveniles. Instead, respirometric analyses point to a reduction in swimming efficiency as a potential alternative or contributing mechanism for the observed decreases in Ucrit.

Pigment abnormalities in flatfish

Abstract Pigment abnormalities have been reported to occur on both sides of flatfish. Hypomelanosis or pseudo-albinism, characterized by white patches or areas devoid of normal pigmentation on the ocular surface of the skin, is common in both wild and hatchery reared flatfish. The blind side may display hypermelanosis in the form of dark spots, known as ambicoloration of the skin. The etiology of these abnormalities is not well understood. Environmental, nutritional and neurological aspects which may be involved are reviewed and approaches for future research are identified.

The effects of weathering and chemical dispersion on Deepwater Horizon crude oil toxicity to mahi-mahi (Coryphaena hippurus) early life stages

To better understand the impact of the Deepwater Horizon (DWH) incident on commercially and ecologically important pelagic fish species, a mahi-mahi spawning program was developed to assess the effect of embryonic exposure to DWH crude oil with particular emphasis on the effects of weathering and dispersant on the magnitude of toxicity. Acute lethality (96 h LC50) ranged from 45.8 (28.4-63.1) μg l(-1) ΣPAH for wellhead (source) oil to 8.8 (7.4-10.3) μg l(-1) ΣPAH for samples collected from the surface slick, reinforcing previous work that weathered oil is more toxic on a ΣPAH basis. Differences in toxicity appear related to the amount of dissolved 3 ringed PAHs. The dispersant Corexit 9500 did not influence acute lethality of oil preparations. Embryonic oil exposure resulted in cardiotoxicity after 48 h, as evident from pericardial edema and reduced atrial contractility. Whereas pericardial edema appeared to correlate well with acute lethality at 96 h, atrial contractility did not. However, sub-lethal cardiotoxicity may impact long-term performance and survival. Dispersant did not affect the occurrence of pericardial edema; however, there was an apparent reduction in atrial contractility at 48 h of exposure. Pericardial edema at 48 h and lethality at 96 h were equally sensitive endpoints in mahi-mahi.

Spawning and larval husbandry of flounder (Paralichthys woolmani) and pacific yellowtail (Seriola mazatlana), new candidate species for aquaculture

Copyright (c) 1997 Elsevier Science B.V. All rights reserved. This paper describes the spawning and larval rearing of a new species of flounder (Paralichthys woolmani) and Pacific yellowtail (Seriola mazatlana) for aquaculture in Ecuador. Experimental production of these species has been conducted for the first time from eggs in captivity. Broodstock flounder were conditioned to spawn through temperature manipulation. Pacific yellowtail spawned under natural environmental conditions. Production of flounder fingerlings has been steady but survival rates remain low (3-8%). Survivals ranging from 0-70% were achieved throughout larval rearing of Seriola, however, high mortalities caused by diseases, cannibalism and weaning onto artificial diets during and after metamorphosis reduced the average survival rates through the juvenile stage to less than 1%. Epizootics of epitheliocystis and Vibrio alginolyticus have repeatedly occurred during the early developmental stages and remain the bottleneck to sustainable mass production of S. mazatlana and P. woolmani fingerlings.

Corresponding morphological and molecular indicators of crude oil toxicity to the developing hearts of mahi mahi.

Crude oils from distinct geological sources worldwide are toxic to developing fish hearts. When oil spills occur in fish spawning habitats, natural resource injury assessments often rely on conventional morphometric analyses of heart form and function. The extent to which visible indicators correspond to molecular markers for cardiovascular stress is unknown for pelagic predators from the Gulf of Mexico. Here we exposed mahi (Coryphaena hippurus) embryos to field-collected crude oil samples from the 2010 Deepwater Horizon disaster. We compared visible heart defects (edema, abnormal looping, reduced contractility) to changes in expression of cardiac-specific genes that are diagnostic of heart failure in humans or associated with loss-of-function zebrafish cardiac mutants. Mahi exposed to crude oil during embryogenesis displayed typical symptoms of cardiogenic syndrome as larvae. Contractility, looping, and circulatory defects were evident, but larval mahi did not exhibit downstream craniofacial and body axis abnormalities. A gradation of oil exposures yielded concentration-responsive changes in morphometric and molecular responses, with relative sensitivity being influenced by age. Our findings suggest that 1) morphometric analyses of cardiac function are more sensitive to proximal effects of crude oil-derived chemicals on the developing heart, and 2) molecular indicators reveal a longer-term adverse shift in cardiogenesis trajectory.

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.

From Fishing to the Sustainable Farming of Carnivorous Marine Finfish

Carnivorous marine finfish aquaculture has been the subject of intense criticism. Because the process consumes more fish biomass in the form of fishmeal and fish oil than it produces, critics argue carnivorous marine finfish aquaculture causes a net loss of living marine resources and is unsustainable given the continued expansion of the industry. While this “fish-in fish-out” critique is factually correct, it fails to capture all the costs and benefits of carnivorous marine finfish aquaculture. Accepted theories on energy and matter flow between trophic levels indicate that carnivorous marine finfish aquaculture appropriates less ocean primary production than commercial fishing and, as we show, it is generally less demanding of agricultural resources and inputs than terrestrial animal husbandry. The basic fish-in fish-out critique also neglects to consider the fishmeal industry with sufficient granularity. The amount of small pelagic fish harvested for reduction has remained stable despite increased carnivorous marine finfish production, largely due to research into alternative ingredients that has decreased fishmeal and fish oil inclusion rates and caused aggregate fishmeal and fish oil consumption by the aquaculture industry to plateau in recent years. Consideration of all the costs and benefits of carnivorous marine finfish aquaculture suggests that the industry is progressing toward sustainability.

Ultraviolet Radiation Enhances the Toxicity of Deepwater Horizon Oil to Mahi-mahi (Coryphaena hippurus) Embryos

The 2010 Deepwater Horizon oil spill resulted in the accidental release of millions barrels of crude oil into the Gulf of Mexico. Photoinduced toxicity following coexposure to ultraviolet (UV) radiation is one mechanism by which polycyclic aromatic hydrocarbons (PAHs) from oil spills may exert toxicity. Mahi-mahi (Coryphaena hippurus), an important fishery resource, have positively buoyant, transparent eggs. These characteristics may result in mahi-mahi embryos being at particular risk from photoinduced toxicity. The goal of this study was to determine whether exposure to ultraviolet radiation as natural sunlight enhances the toxicity of crude oil to embryonic mahi-mahi. Mahi-mahi embryos were exposed to several dilutions of water accommodated fractions (WAF) from slick oil collected during the 2010 spill and gradations of natural sunlight in a fully factorial design. Here, we report that coexposure to natural sunlight and WAF significantly reduced percent hatch in mahi-mahi embryos. Effect concentrations of PAH in WAF were within the range of surface PAH concentrations reported in the Gulf of Mexico during the Deepwater Horizon spill. These data suggest that laboratory toxicity tests that do not include UV may underestimate the toxicity of oil spills to early lifestage fish species.

Impacts of Deepwater Horizon crude oil exposure on adult mahi-mahi (Coryphaena hippurus) swim performance

The temporal and geographic attributes of the Deepwater Horizon incident in 2010 likely exposed pelagic game fish species, such as mahi-mahi, to crude oil. Although much of the research assessing the effects of the spill has focused on early life stages of fish, studies examining whole-animal physiological responses of adult marine fish species are lacking. Using swim chamber respirometry, the present study demonstrates that acute exposure to a sublethal concentration of the water accommodated fraction of Deepwater Horizon crude oil results in significant swim performance impacts on young adult mahi-mahi, representing the first report of acute sublethal toxicity on adult pelagic fish in the Gulf of Mexico following the spill. At an exposure concentration of 8.4 ± 0.6 µg L-1 sum of 50 selected polycyclic aromatic hydrocarbons (PAHs; mean of geometric means ± standard error of the mean), significant decreases in the critical and optimal swimming speeds of 14% and 10%, respectively (p < 0.05), were observed. In addition, a 20% reduction in the maximum metabolic rate and a 29% reduction in aerobic scope resulted from exposure to this level of ΣPAHs. Using environmentally relevant crude oil exposure concentrations and a commercially and ecologically valuable Gulf of Mexico fish species, the present results provide insight into the effects of the Deepwater Horizon oil spill on adult pelagic fish. Environ Toxicol Chem 2016;35:2613-2622.