Abstract

Early life stages of fish are highly sensitive to crude oil exposure and thus, short term exposures during critical developmental periods could have detrimental consequences for juvenile survival. Here we administered crude oil to Atlantic haddock (Melanogrammus aeglefinus) in short term (3-day) exposures at two developmental time periods: before first heartbeat, from gastrulation to cardiac cone stage (early), and from first heartbeat to one day before hatching (late). A frequent sampling regime enabled us to determine immediate PAH uptake, metabolite formation and gene expression changes. In general, the embryotoxic consequences of an oil exposure were more severe in the early exposure animals. Oil droplets on the eggshell resulted in severe cardiac and craniofacial abnormalities in the highest treatments. Gene expression changes of Cytochrome 1 a, b, c and d (cyp1a, b, c, d), Bone morphogenetic protein 10 (bmp10), ABC transporter b1 (abcb1) and Rh-associated G-protein (rhag) were linked to PAH uptake, occurrence of metabolites of phenanthrene and developmental and functional abnormalities. We detected circulation-independent, oil-induced gene expression changes and separated phenotypes linked to proliferation, growth and disruption of formation events at early and late developmental stages. Changes in bmp10 expression suggest a direct oil-induced effect on calcium homeostasis. Localized expression of rhag propose an impact on osmoregulation. Severe eye abnormalities were linked to possible inappropriate overexpression of cyp1b in the eyes. This study gives an increased knowledge about developmentally dependent effects of crude oil toxicity. Thus, our findings provide more knowledge and detail to new and several existing adverse outcome pathways of crude oil toxicity.

Highlights

  • Fish habitats are frequently impacted by accidental oil spills

  • We focused on genes found interesting in a previous study (Sørhus et al, 2017) that are involved in various parts of development and function: cardiac development and calcium homeostasis (Bone morphogenetic protein 10), transport of xenobiotic products (ABC transporter b1), osmoregulation and ammonium waste excretion (Rh-associated G-protein), and enzymes possibly involved in phase I xenobiotic metabolism (Cytochrome P450 1s)

  • Oil droplet fouling was observed on embryos in both submerged (L, M, held submerged under the water surface (H sub)) and surface (H surf) exposures regardless of timing, and was evident after only 1 h of exposure (Fig. 2A and B, top panels)

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Summary

Introduction

Fish habitats are frequently impacted by accidental oil spills. For fish, consequences of crude oil toxicity are stage dependent, and early life stages (eggs and larvae) are thought to be highly vulnerable for several reasons. Life stages drift and have no opportunity to avoid contaminated areas compared to juvenile and mature fish (Carroll et al, 2018; Olsen et al, 2010). Relative content of lipids and surfacearea-to-volume ratio are higher in early life stages compared to juveniles/adults, making them more susceptible to accumulation of lipophilic environmental toxicants (Petersen and Kristensen, 1998). The Atlantic haddock (Melanogrammus aeglefinus) has a sticky eggshell which adhere oil droplets. Due to this oil droplet fouling, the haddock embryo is approximately 10 times more sensitive to crude oil than its close relative Atlantic cod (Gadus morhua) (Sørensen et al, 2017)

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