Effect of Deepwater Horizon Crude Oil Water Accommodated Fraction on Olfactory Function in the Atlantic Stingray, Hypanus sabinus

Abstract

The Deepwater Horizon oil spill was the largest accidental marine oil spill in history, releasing nearly 5 million barrels of crude oil. Crude oil causes both lethal and sublethal effects on marine organisms, and sensory systems have the potential to be strongly affected. Marine fishes rely upon the effective functioning of their sensory systems for detection of prey, mates, and predators. However, despite the obvious importance of sensory systems, the impact of crude oil exposure upon sensory function remains largely unexplored. Here we show that olfactory organ responses to amino acids are significantly depressed in oil exposed stingrays. We found that the response magnitude of the electro-olfactogram (EOG) to 1 mM amino acids decreased by an average of 45.8% after 48 h of exposure to an oil concentration replicating that measured in coastal areas. Additionally, in oil exposed individuals, the EOG response onset was significantly slower, and the clearing time was protracted. This study is the first to employ an electrophysiological assay to demonstrate crude oil impairment of the olfactory system in a marine fish. We show that stingrays inhabiting an area impacted by an oil spill experience reduced olfactory function, which would detrimentally impact fitness, could lead to premature death, and could cause additional cascading effects through lower trophic levels.

Previous oil exposure alters oil avoidance behavior in a common marsh fish, the Gulf KillifishFundulus grandis

“…Moreover, damage to the higher order central nervous system processing was implicated in this decreased oil avoidance behavior. Olfactory damage is also known to occur with oil exposure in some fishes (such as Atlantic stingrays, Cave et al 2018) and reduced recognition of threats via these cues is also possible (Schlenker et al 2019b). Whether highly weathered crude oil elicits similar effects and the specific chemical constituents in oil involved in these detrimental physiological changes remain unclear.…”

“…Previous research indicates that oil exposure can inhibit or damage sensory mechanisms used by fishes to detect oil. For example, exposure to the water-accommodated fraction of oil in Atlantic stingrays Hypanus sabinus damaged olfactory function (Cave et al 2018). After oil exposure, bicolor damselfish Stegastes partitus showed a reduction in the response to conspecific alarm cues (Schlenker et al 2019b).…”

A review of the toxicology of oil in vertebrates: what we have learned following the Deepwater Horizon oil spill

“…Olfaction. There were clear effects of oil exposure on olfaction in fish (Cave and Kajiura 2018), an area largely unexplored prior to the DWH oil spill. Studies in Atlantic stingrays (Hypanus sabinus) reported an average decrease in magnitude of the olfactory response by 45.8% after 48 hr exposure to oil mimicking the concentrations found in the coastal regions.…”

Bridging disciplines to advance elasmobranch conservation: applications of physiological ecology

“…Exposure to anthropogenic contaminants also poses threats to the performance and health of elasmobranch fishes in unexpected ways. For example, the olfactory sensitivity of Atlantic stingray to amino acids is reduced after acute exposure to mixtures of crude oil, which may impair their ability to forage successfully (Cave and Kajiura, 2018).…”