Very low embryonic crude oil exposures cause lasting cardiac defects in salmon and herring

Abstract

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

Evaluating signals of oil spill impacts, climate, and species interactions in Pacific herring and Pacific salmon populations in Prince William Sound and Copper River, Alaska

“…Chinook salmon supported the inclusion of the EVOS covariate in explaining variation in productivity relative to the models that only included density dependence (Table 1), but the estimated impact of EVOS was slightly positive and opposite of what we might expect from other studies [16]. Coefficients for these impacts and all hypotheses are included online, https://github.com/NCEAS/pfx-covariation-pws.…”

“…Incardona et al [16] suggested a mechanism by which detrimental effects could result from low toxicity 7–9 months after exposure, fine scale sampling of individual exposure rates immediately following a spill could be combined with intensive spatiotemporal histology sampling in the years that follow.…”

Application of gas chromatography/tandem mass spectrometry to determine a wide range of petrogenic alkylated polycyclic aromatic hydrocarbons in biotic samples

“…The identification of alkylated PAHs in crude oil‐exposed marine organisms is critical for evaluation of the toxicity observed in these species. Several studies report alkyl homologue cluster concentration in different fish tissue matrices using GC/MS SIM methods . However, relatively large quantities (several grams) of sample material are needed to obtain the necessary sensitivity.…”

The influence of heart developmental anatomy on cardiotoxicity-based adverse outcome pathways in fish

“…In the United States, herring eggs and larvae have been a focus of both field and laboratory studies to assess the ecological impacts of large oil spills, including the 1989 Exxon Valdez spill in Alaska (Carls et al, 1999;Marty et al, 1997) and the 2007 Cosco Busan spill in San Francisco Bay (Incardona et al, 2012a;Incardona et al, 2012b). They have also provided a context for mechanistic studies on crude oil cardiotoxicity (Incardona, et al, 2009;Incardona, et al, 2015). As indicated in Fig.…”

“…2). These effects range from outright embryonic heart failure and mortality at relative high PAH exposures (Adams et al, 2014a;Adams et al, 2014b;Esbaugh et al, 2016;Incardona et al, 2014;Incardona et al, 2013;Jung et al, 2013;Jung et al, 2015;Madison et al, 2015;Martin et al, 2014;McIntyre et al, 2016a;McIntyre et al, 2016b;Sørhus et al, 2015), to more subtle effects on heart shape and delayed impacts on cardiovascular performance at lower concentrations (Hicken et al, 2011;Incardona et al, 2015). These latter, protracted physiological impacts likely contributed to the delayed mortality and poor population recruitment previously observed both in 1) mark-recapture studies with pink salmon (Oncorhynchus gorbuscha) exposed to crude oil during embryogenesis (Heintz, 2007;Heintz et al, 2000) and 2) the losses of wild pink salmon spawned in shoreline habitats that were oiled in the aftermath of the 1989 Exxon Valdez disaster (Rice et al, 2001).…”