Date Published: July 5, 2017
Publisher: Public Library of Science
Author(s): Lisbet Sørensen, Elin Sørhus, Trond Nordtug, John P. Incardona, Tiffany L. Linbo, Laura Giovanetti, Ørjan Karlsen, Sonnich Meier, Ilaria Corsi.
The impact of crude oil pollution on early life stages (ELS) of fish, including larvae and embryos, has received considerable attention in recent years. Of the organic components present in crude oil, polycyclic aromatic hydrocarbons (PAHs) are considered the main class of compounds responsible for toxic effects in marine organisms. Although evidence suggests that they are more toxic, alkylated PAHs remain much less studied than their unsubstituted congeners. Recently, it was established that embryos of Atlantic haddock (Melanogrammus aeglefinus) are particularly sensitive to dispersed crude oil, and it was hypothesized that this was caused by direct interaction with crude oil droplets, which adhered to the chorion of exposed embryos. Such a phenomenon would increase the potential for uptake of less water-soluble compounds, including alkylated PAHs. In the current study, we compared the uptake of parent and alkylated PAHs in Atlantic cod (Gadus morhua) and haddock embryos exposed to dispersed crude oil at a range of environmentally relevant concentrations (10–600 μg oil/liter seawater). Although the species are biologically very similar, the cod chorion does not become fouled with oil droplets, even when the two species are exposed to dispersions of crude oil droplets under similar conditions. A close correlation between the degree of fouling and toxicological response (heart defects, craniofacial malformation) was observed. Oil droplet fouling in haddock led to both quantitative and qualitative differences in PAH uptake. Finally, kinetic data on a large suite of PAHs showed differential elimination, suggesting differential metabolism of unsubstituted versus alkylated compounds.
The impact of crude oil on marine fish and fisheries has received much attention in recent years, particularly in relation to major spill events such as the 1989 Exxon Valdez (EV) spill in the Prince William Sound, Alaska and the 2010 Deepwater Horizon (DWH) event in the northern Gulf of Mexico. Due to their high sensitivity to pollution, early life stages (ELS) of fish, including embryo and larval stages, have been studied extensively. The main sub-lethal, toxic responses in ELS of fish include cardiotoxicity and morphogenetic defects [1–3], but the toxicological mechanisms are still not fully understood. Lasting cardiac defects in juvenile fish could underlie population-level impacts years after a spill event . As offshore oil exploration moves north into the Arctic, it occurs in sensitive spawning areas for several commercially important species of marine fish, such as in the Lofoten-Vesterålen area off the Norwegian coast[5, 6]. Consequently, a large effort towards developing risk assessment tools for evaluating the potential impact of oil exploration in these sensitive areas has been made [5–7]. However, to develop robust models for the effects of spilled crude oil on ELS of cold water marine fish, there is a need for more experimental data on bioaccumulation and critical body burdens of toxic oil compounds . Likewise, there is a lack of data on how dispersed crude oil droplets affect fish ELS . Along with dissolution of the water-soluble fraction (WSF), formation of dispersed oil droplets is considered one of the most important processes influencing the fate of spilled crude oil. Crude oil may be dispersed in the water column by turbulent wave action and/or application of chemical dispersants in the event of a surface spill [9, 10] or through high pressure jets during deep water oil and gas blowouts . Formation of micron-sized oil droplets may increase the bioavailability of toxic oil constituents to marine organisms .
In the current study, the change in PAH body burden in dispersed crude oil exposed Atlantic haddock and cod embryos during a 10 or 11 days long exposure (1-11/12 days post fertilization (dpf)) was investigated. It was determined that haddock eggs, unlike cod, are fouled by crude oil droplets adhering to the chorion when exposed to concentrations > 0.7 μg/L tPAH. This is correlated with an increased body burden of both parent and alkylated PAHs, and a severe increase in toxicological responses (malformations and cardiotoxicity). Due to the fouling of the haddock chorion with crude oil droplets, total measured egg-associated PAHs prior to hatching is higher (particularly for heavier compounds) than what is actually bioavailable to the embryos, and much higher than what is measured in the non-fouled cod eggs. However, the increased cyp1a induction and increased severity of cardiotoxicity and morphological malformations in haddock compared to cod clearly indicate an increased uptake of PAHs in the embryos. This is consistent with a secondary uptake pathway caused by the oil droplets adhering to the surface of the eggs.