Exposure to high concentrations of crude oil produces a lethal syndrome of heart failure in fish embryos. Mortality is caused by cardiotoxic polycyclic aromatic hydrocarbons (PAHs), ubiquitous components of petroleum. Here, we show that transient embryonic exposure to very low concentrations of oil causes toxicity that is sublethal, delayed, and not counteracted by the protective effects of cytochrome P450 induction. Nearly a year after embryonic oil exposure, adult zebrafish showed subtle changes in heart shape and a significant reduction in swimming performance, indicative of reduced cardiac output. These delayed physiological impacts on cardiovascular performance at later life stages provide a potential mechanism linking reduced individual survival to population-level ecosystem responses of fish species to chronic, low-level oil pollution.

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The 1989 Exxon Valdez disaster exposed embryos of pink salmon and Pacific herring to crude oil in shoreline spawning habitats throughout Prince William Sound, Alaska. The herring fishery collapsed four years later. The role of the spill, if any, in this decline remains one of the most controversial unanswered questions in modern natural resource injury assessment. Crude oil disrupts excitationcontraction coupling in fish heart muscle cells, and we show here that salmon and herring exposed as embryos to trace levels of crude oil grow into juveniles with abnormal hearts and reduced cardiorespiratory function, the latter a key determinant of individual survival and population recruitment. Oil exposure during cardiogenesis led to specific defects in the outflow tract and compact myocardium, and a hypertrophic response in spongy myocardium, evident in juveniles 7 to 9 months after exposure. The thresholds for developmental cardiotoxicity were remarkably low, suggesting the scale of the Exxon Valdez impact in shoreline spawning habitats was much greater than previously appreciated. Moreover, an irreversible loss of cardiac fitness and consequent increases in delayed mortality in oil-exposed cohorts may have been important contributors to the delayed decline of pink salmon and herring stocks in Prince William Sound.The year 2014 marked the 25 th anniversary of the 1989 Exxon Valdez oil spill in Prince William Sound, Alaska. At the time, the spill was the largest in U.S. history, with extensive oiling of shoreline spawning habitats for Pacific herring (Clupea pallasi) and pink salmon (Oncorhynchus gorbuscha), the two most important commercial fish species in the Sound. Herring larvae sampled in proximity to oil were visibly abnormal 1 , and mortality rates were higher for pink salmon embryos at oiled sites 2 . The herring fishery collapsed 3-4 years after the spill 3,4 when the cohort spawned in oiled areas would have reached reproductive maturity 5 . The contribution of the spill to the herring population collapse, if any, was never determined and remains controversial.In the early 1990s little was known about the effects of low-level crude oil exposures on fish early life stages. In the ensuing years, the syndrome of developmental defects and mortality documented in field-collected herring and salmon larvae was linked to polycyclic aromatic hydrocarbons (PAHs), an abundant fraction of most crude oils [6][7][8] . Subsequent research using the zebrafish model showed that the etiology of the syndrome was a disruption of embryonic cardiac function and morphogenesis 9,10 . This cardiotoxicity was specifically attributed to three-ringed PAHs 9,10 , and it was further shown that normal-appearing zebrafish embryos surviving trace crude oil exposures grow into adults with malformed hearts and reduced cardiorespiratory performance 11 . It is now established that crude oils from different geological sources disrupt heart development 12,13 in a diversity of fish species 14,15 , by a mechanism