Interactions between Zooplankton and Crude Oil: Toxic Effects and Bioaccumulation of Polycyclic Aromatic Hydrocarbons

We conducted ship-, shore- and laboratory-based crude oil exposure experiments to investigate (1) the effects of crude oil (Louisiana light sweet oil) on survival and bioaccumulation of polycyclic aromatic hydrocarbons (PAHs) in mesozooplankton communities, (2) the lethal effects of dispersant (Corexit 9500A) and dispersant-treated oil on mesozooplankton, (3) the influence of UVB radiation/sunlight exposure on the toxicity of dispersed crude oil to mesozooplankton, and (4) the role of marine protozoans on the sublethal effects of crude oil and in the bioaccumulation of PAHs in the copepod Acartia tonsa. Mortality of mesozooplankton increased with increasing oil concentration following a sigmoid model with a median lethal concentration of 32.4 ml L21 in 16 h. At the ratio of dispersant to oil commonly used in the treatment of oil spills (i.e. 1:20), dispersant (0.25 ml L21 ) and dispersant- treated oil were 2.3 and 3.4 times more toxic, respectively, than crude oil alone (5 ml L21 ) to mesozooplankton. UVB radiation increased the lethal effects of dispersed crude oil in mesozooplankton communities by 35%. We observed selective bioaccumulation of five PAHs, fluoranthene, phenanthrene, pyrene, chrysene and benzo[b]fluoranthene in both mesozooplankton communities and in the copepod A. tonsa. The presence of the protozoan Oxyrrhis marina reduced sublethal effects of oil on A. tonsa and was related to lower accumulations of PAHs in tissues and fecal pellets, suggesting that protozoa may be important in mitigating the harmful effects of crude oil exposure in copepods and the transfer of PAHs to higher trophic levels. Overall, our results indicate that the negative impact of oil spills on mesozooplankton may be increased by the use of chemical dispersant and UV radiation, but attenuated by crude oil-microbial food webs interactions, and that both mesozooplankton and protozoans may play an important role in fate of PAHs in marine environments.Zoe Wambaugh was supported by the National Science Foundation (NSF) Research Experiences for Undergraduates (REU) program (grant OCE- 1062745). This research was made possible by a grant from BP/The Gulf of Mexico Research Initiative through the University of Texas Marine Science Institute (DROPPS consortium: ‘Dispersion Research on Oil: Physics and Plankton Studies’). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Marine Scienc

Concentration of polycyclic aromatic hydrocarbons, PAHs (µg L⁻¹), in the water at the different crude oil exposure levels (5–100 µl L⁻¹) used in the experiments.

<p>Concentration of PAHs was estimated from the oil added to the containers using the concentration of PAHs determined in the crude oil (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0067212#pone-0067212-g002" target="_blank">Fig. 2</a>) Crude oil exposure levels are also expressed in mg L⁻¹ using a crude oil density of 0.845g/ml. Naphthalene (Nap), acenaphthene (Ace), acenaphthylene (Acy), fluorene (Flu), phenanthrene (Phe), anthracene (An), fluoranthene (Flua), pyrene (Pyr), benzo[a]anthracene (BaA), chrysene (Chr), benzo[b]fluoranthene (BbF).</p

Relationship between mesozooplankton mortality and crude oil concentration after 16 h of exposure in onboard incubations (25°C, sunlight exposure) conducted in the northern Gulf of Mexico.

<p>Regression line based on <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0067212#pone.0067212.e001" target="_blank">Equation (1</a>) (solid line) and 95% confidence intervals (dashed lines).</p

Map indicating the zooplankton sampling stations during the cruise in the northern Gulf of Mexico: station A (A), station B (B) and Mississippi River Mouth station (MRM).

<p>Stations are located in the area affected by the deepwater horizon (DWH) oil spill on April 2010.</p

Bioaccumulation factors of PAHs in natural mesozooplankton communities from the northern Gulf of Mexico (Stations A, B and MRM) exposed to different concentrations of crude oil.

<p>Naphthalene (Nap), phenanthrene (Phe), fluoranthene (Flua), pyrene (Pyr), chrysene (Chr), benzo[b]fluoranthene (BbF). The hash symbol indicates that BAF were similar or lower than respective control treatments (non-exposed copepods). <i>n.d.</i> = no detected.</p

Concentration of PAHs in body tissues (A, B), fecal pellets (C, D) and eggs (E, F) of <i>Acartia tonsa</i> feeding on <i>Rhodomonas</i> sp.(left column) or <i>Rhodomonas</i> sp. plus <i>Oxyrrhis</i> marina (right column).

<p>Experimental: copepods exposed to oil (5 µl L⁻¹). Control: non-exposed copepods. The asterisks indicate the PAH was not detected.</p

Concentration of the polycyclic aromatic hydrocarbons detected in natural copepod assemblages after 16 h of exposure to different crude oil concentrations (10–100 µl L⁻¹) in the experiments conducted in the North of Gulf Mexico stations (A, B, MRM).

<p>A: naphthalene, B: phenanthrene, C: fluoranthene, D: pyrene, E: chrysene, F: benzo[b]fluorantheneThe asterisks indicate the PAH was not detected.</p

Concentration of polycyclic aromatic hydrocarbons (PAHs, ng µL⁻¹) in the crude oil used in the experiments (Louisiana light sweet crude oil).

<p>Concentration of polycyclic aromatic hydrocarbons (PAHs, ng µL⁻¹) in the crude oil used in the experiments (Louisiana light sweet crude oil).</p