Acclimation to Future Climate Exposes Vulnerability to Cold Extremes in Intertidal Sea Hares

Synopsis Highly dynamic environments like estuaries will undergo unpredictable shifts in thermal and salinity regimes with ongoing climate change. These interactive stressors fluctuate predictably and seasonally over historical periods, which has facilitated the evolution of wide environmental tolerance in some estuarine inhabitants. However, physiological and behavioral acclimatization is seasonally based for many estuarine species, meaning that a shift in the unpredictability of climate events and trends will disrupt the effectiveness of evolved tolerance mechanisms. Of particular concern are extreme cold events and high-volume precipitation events, which will acutely and unpredictably alter an estuarine habitat. The eelgrass sea hare, Phyllaplysia taylori, has documented euryhaline and eurythermal tolerance to summer conditions, but the winter environment may pose a greater challenge to seasonally relevant acclimatization scenarios. Here, we characterized lower critical thermal limits, and behavioral responses to stimuli leading up to these limits, in two central California P. taylori populations under four temperature–salinity scenarios in a laboratory acclimation experiment. Acclimation to warmer conditions significantly increased critical thermal minima, while fresher conditions resulted in high mortality. However, the surviving individuals in the fresher conditions were able to respond to stimuli more quickly overall, despite their shortest response time being at a higher temperature than the saltier-acclimated individuals. Within the environmental context of their natural habitats, we find that acclimation to climate change-induced warming will hinder sea hares’ ability to weather existing and future cold extremes and precipitation events.