Prior exposure to weathered oil influences foraging of an ecologically important saltmarsh resident fish

Abstract

Estuarine ecosystem balance typically relies on strong food web interconnectedness dependent on a relatively low number of resident taxa, presenting a potential ecological vulnerability to extreme ecosystem disturbances. Following the Deepwater Horizon (DwH) oil spill disaster of the northern Gulf of Mexico (USA), numerous ecotoxicological studies showed severe species-level impacts of oil exposure on estuarine fish and invertebrates, yet post-spill surveys found little evidence for severe impacts to coastal populations, communities, or food webs. The acknowledgement that several confounding factors may have limited researchers' abilities to detect negative ecosystem-level impacts following the DwH spill drives the need for direct testing of weathered oil exposure effects on estuarine residents with high trophic connectivity. Here, we describe an experiment that examined the influence of previous exposure to four weathered oil concentrations (control: 0.0 L oil m^-2; low: 0.1 L oil m^-2; moderate: 0.5-1 L oil m^-2; high: 3.0 L oil m^-2) on foraging rates of the ecologically important Gulf killifish (Fundulus grandis). Following exposure in oiled saltmarsh mesocosms, killifish were allowed to forage on grass shrimp (Palaeomonetes pugio) for up to 21 h. We found that previous exposure to the high oil treatment reduced killifish foraging rate by ~37% on average, compared with no oil control treatment. Previous exposure to the moderate oil treatment showed highly variable foraging rate responses, while low exposure treatment was similar to unexposed responses. Declining foraging rate responses to previous high weathered oil exposure suggests potential oil spill influence on energy transfer between saltmarsh and off-marsh systems. Additionally, foraging rate variability at the moderate level highlights the large degree of intraspecific variability for this sublethal response and indicates this concentration represents a potential threshold of oil exposure influence on killifish foraging. We also found that consumption of gravid vs non-gravid shrimp was not independent of prior oil exposure concentration, as high oil exposure treatment killifish consumed ~3× more gravid shrimp than expected. Our study findings highlight the sublethal effects of prior oil exposure on foraging abilities of ecologically valuable Gulf killifish at realistic oil exposure levels, suggesting that important trophic transfers of energy to off-marsh systems may have been impacted, at least in the short-term, by shoreline oiling at highly localized scales. This study provides support for further experimental testing of oil exposure effects on sublethal behavioral impacts of ecologically important estuarine species, due to the likelihood that some ecological ramifications of DwH on saltmarshes likely went undetected.

Keywords: Feeding effort; Fish behavior; Macondo; Mesocosm; Nekton.

Figure 1. Gulf killifish foraging rates per replicate for each prior oil exposure treatment.

Gulf killifish foraging rates (number of shrimp consumed fish⁻¹ min⁻¹) per bucket replicate for each prior oil exposure treatment. Solid lines in boxes represent treatment medians and dots are outliers. Different letters indicate treatment differences based on results from Games-Howell post-hoc contrast.

Figure 2. Proportions of gravid shrimp consumption by Gulf killifish.

Proportions of observed values of gravid shrimp consumed (out of total shrimp consumed) by Gulf killifish for the entire experiment (grey bar) and at different treatment levels of prior oil exposure, with the calculated expected proportion values represented by dotted lines.