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      Combined effects of elevated temperature and Deepwater Horizon oil exposure on the cardiac performance of larval mahi-mahi, Coryphaena hippurus

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          Abstract

          The 2010 Deepwater Horizon oil spill coincided with the spawning season of many pelagic fish species in the Gulf of Mexico. Yet, few studies have investigated physiological responses of larval fish to interactions between anthropogenic crude oil exposure and natural factors (e.g. temperature, oxygen levels). Consequently, mahi mahi ( Coryphaena hippurus) embryos were exposed for 24 hours to combinations of two temperatures (26 and 30°C) and six concentrations of oiled fractions of weathered oil (from 0 to 44.1 μg ∑50PAHs·L -1). In 56 hours post-fertilization larvae, heart rate, stroke volume and cardiac output were measured as indicators of functional cardiac phenotypes. Fluid accumulation and incidence of edema and hematomas were quantified as indicators of morphological impairments. At both 26 and 30°C, oil-exposed larvae suffered dose-dependent morphological impairments and functional heart failure. Elevation of temperature to 30°C appeared to induce greater physiological responses (bradycardia) at PAH concentrations in the range of 3.0–14.9 μg·L -1. Conversely, elevated temperature in oil-exposed larvae reduced edema severity and hematoma incidence. However, the apparent protective role of warmer temperature does not appear to protect against enhanced mortality. Collectively, our findings show that elevated temperature may slightly decrease larval resilience to concurrent oil exposure.

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

          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.
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            Crude oil impairs cardiac excitation-contraction coupling in fish.

            Crude oil is known to disrupt cardiac function in fish embryos. Large oil spills, such as the Deepwater Horizon (DWH) disaster that occurred in 2010 in the Gulf of Mexico, could severely affect fish at impacted spawning sites. The physiological mechanisms underlying such potential cardiotoxic effects remain unclear. Here, we show that crude oil samples collected from the DWH spill prolonged the action potential of isolated cardiomyocytes from juvenile bluefin and yellowfin tunas, through the blocking of the delayed rectifier potassium current (I(Kr)). Crude oil exposure also decreased calcium current (I(Ca)) and calcium cycling, which disrupted excitation-contraction coupling in cardiomyocytes. Our findings demonstrate a cardiotoxic mechanism by which crude oil affects the regulation of cellular excitability, with implications for life-threatening arrhythmias in vertebrates.
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              Characteristics of dispersions and water-soluble extracts of crude and refined oils and their toxicity to estuarine crustaceans and fish

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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: ResourcesRole: ValidationRole: Writing – review & editing
                Role: Funding acquisitionRole: ResourcesRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: Funding acquisitionRole: ResourcesRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: Funding acquisitionRole: ResourcesRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                17 October 2018
                2018
                : 13
                : 10
                : e0203949
                Affiliations
                [1 ] Department of Biological Sciences, University of North Texas, Denton, Texas, United States of America
                [2 ] Department of Marine Biology and Ecology, University of Miami, Rosenstiel School of Marine and Atmospheric Science, Miami, Florida, United States of America
                [3 ] Department of Marine Ecosystems and Society, University of Miami, Rosenstiel School of Marine and Atmospheric Science, Miami, Florida, United States of America
                University of Siena, ITALY
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                [¤]

                Current address: Institute of Marine Research, Austevoll Research Station, Storebø, Norway.

                Author information
                http://orcid.org/0000-0002-1410-878X
                Article
                PONE-D-18-05541
                10.1371/journal.pone.0203949
                6192557
                30332409
                264923dd-ca1a-4f29-a2b1-cf01622aadbe
                © 2018 Perrichon et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 20 February 2018
                : 30 August 2018
                Page count
                Figures: 4, Tables: 1, Pages: 19
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100007240, Gulf of Mexico Research Initiative;
                Award ID: SA-1520
                Award Recipient :
                This research was made possible by a grant from the Gulf of Mexico Research Initiative. Data are publicly available through the Gulf of Mexico Research Initiative Information and Data Cooperative (GRIIDC) at https://data.gulfresearchinitiative.org (doi:< 10.7266/N7PR7T17>; doi:< 10.7266/N7T151PG>; doi:< 10.7266/N7C53HX0). Grant N0; SA-1520; Name: Relationship of Effects of Cardiac Outcomes in fish for Validation of Ecological Risk (RECOVER) to MG, WWB and DB. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Larvae
                Medicine and Health Sciences
                Diagnostic Medicine
                Signs and Symptoms
                Edema
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Signs and Symptoms
                Edema
                Biology and Life Sciences
                Zoology
                Fish Biology
                Fish Physiology
                Biology and Life Sciences
                Zoology
                Animal Physiology
                Vertebrate Physiology
                Fish Physiology
                Medicine and Health Sciences
                Cardiology
                Cardiac Output
                Engineering and Technology
                Energy and Power
                Fuels
                Fossil Fuels
                Crude Oil
                Physical Sciences
                Materials Science
                Materials
                Fuels
                Fossil Fuels
                Crude Oil
                Medicine and Health Sciences
                Cardiology
                Heart Rate
                Biology and Life Sciences
                Developmental Biology
                Embryology
                Embryos
                Biology and Life Sciences
                Anatomy
                Cardiovascular Anatomy
                Heart
                Medicine and Health Sciences
                Anatomy
                Cardiovascular Anatomy
                Heart
                Custom metadata
                Data are publicly available through the Gulf of Mexico Research Initiative Information and Data Cooperative (GRIIDC) at https://data.gulfresearchinitiative.org (doi:< 10.7266/N7PR7T17>; doi:< 10.7266/N7T151PG>; doi:< 10.7266/N7C53HX0).

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