Short-and medium-term exposure to ocean acidification reduces olfactory sensitivity in gilthead seabream

Abstract

The effects of ocean acidification on fish are only partially understood. Studies on olfaction are mostly limited to behavioural
alterations of coral reef fish; studies on temperate species and/or with economic importance are scarce. The current study
evaluated the effects of short- and medium-term exposure to ocean acidification on the olfactory system of gilthead seabream
(Sparus aurata), and attempted to explain observed differences in sensitivity by changes in the protonation state of amino acid
odorants. Short-term exposure to elevated PCO2 decreased olfactory sensitivity to some odorants, such as L-serine, L-leucine,
L-arginine, L-glutamate and conspecific intestinal fluid, but not to others, such as L-glutamine and conspecific bile fluid. Seabream
were unable to compensate for high PCO2 levels in the medium-term; after four weeks’ exposure to high PCO2, the olfactory
sensitivity remained lower in elevated PCO2 water. The decrease in olfactory sensitivity in high PCO2 water could be partly
attributed to changes in the protonation state of the odorants and/or their receptor(s); we illustrate how protonation due to
reduced pH causes changes in the charge distribution of odorant molecules, an essential component for ligand-receptor interaction.
However, there are other mechanisms involved. At a histological level, the olfactory epithelium contained higher densities of
mucus cells in fish kept in high CO2 water, and a shift in pH of the mucus they produced to more neutral. These differences suggest
a physiological response of the olfactory epithelium to lower pH and/or high CO2 levels, but an inability to fully counteract the
effects of acidification on olfactory sensitivity. Therefore, the current study provides evidence for a direct, medium-term, global
effect of ocean acidification on olfactory sensitivity in fish, and possibly other marine organisms, and suggests a partial
explanatory mechanism.