Unexpected Interaction with Dispersed Crude Oil Droplets Drives Severe Toxicity in Atlantic Haddock Embryos

Abstract

The toxicity resulting from exposure to oil droplets in marine fish embryos and larvae is still subject for debate. The most detailed studies have investigated the effects of water-dissolved components of crude oil in water accommodated fractions (WAFs) that lack bulk oil droplets. Although exposure to dissolved petroleum compounds alone is sufficient to cause the characteristic developmental toxicity of crude oil, few studies have addressed whether physical interaction with oil micro-droplets are a relevant exposure pathway for open water marine speices. Here we used controlled delivery of mechanically dispersed crude oil to expose pelagic embryos and larvae of a marine teleost, the Atlantic haddock (Melanogrammus aeglefinus). Haddock embryos were exposed continuously to two different concentrations of dispersed crude oil, high and low, or in pulses. By 24 hours of exposure, micro-droplets of oil were observed adhering and accumulating on the chorion, accompanied by highly elevated levels of cyp1a, a biomarker for exposure to aromatic hydrocarbons. Embryos from all treatment groups showed abnormalities representative of crude oil cardiotoxicity at hatch (5 days of exposure), such as pericardial and yolk sac edema. Compared to other species, the frequency and severity of toxic effects was higher than expected for the waterborne PAH concentrations (e.g., 100% of larvae had edema at the low treatment). These findings suggest an enhanced tissue uptake of PAHs and/or other petroleum compounds from attached oil droplets. These studies highlight a novel property of haddock embryos that leads to greater than expected impact from dispersed crude oil. Given the very limited number of marine species tested in similar exposures, the likelihood of other species with similar properties could be high. This unanticipated result therefore has implications for assessing the ecological impacts of oil spills and the use of methods for dispersing oil in the open sea.

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

“…It should also be noted that the total amount of PAH uptake in the eggs is only 0.27 ± 0.02 μg/g and 3.3 ± 0.8 μg/g wet body weight from 0.1 g samples, which demonstrates that we are able to work at very low concentrations with this method. These concentrations have still been proven environmentally relevant due to the extreme sensitivity of early life stages of some fish species towards crude oil pollution …”

“…Crude oil‐exposed haddock eggs were collected from an ongoing exposure experiment after exposure to mechanically dispersed crude oil over 9 days (total PAH concentration was ~0.7 μg/L water in low dose groups and ~7 μg/L in high dose groups). The exposure conditions are described in Sørhus et al …”

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

“…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).…”

Desert Vegetation Forty Years after an Oil Spill

“…Consequently, its extraction and trade are of high economic importance. Once released to the environment, however, crude oil causes harm by altering soil properties (Ellis and Adams, 1961), and some compounds, especially polycyclic aromatic hydrocarbons (PAHs) are toxic to animals (Sørhus et al, 2015), plants, and microorganisms (Currier and Peoples, 1954; Alkio et al, 2005). Information about the long‐term damage caused by oil spills to ecosystems is required to allow risk assessment of crude oil extraction and transportation as well as appropriate decision making about remediation of spillages.…”