Critical thermal maxima and oxygen uptake in Elysia viridis, a sea slug that steals chloroplasts to photosynthesize

Abstract

Photosynthetic animals produce oxygen, providing an ideal lens for studying how oxygen dynamics influence thermal sensitivity. The algivorous sea slug Elysia viridis can steal and retain chloroplasts from the marine alga Bryopsis sp. for months when starved, but chloroplast retention is mere weeks when they are fed another green alga, Chaetomorpha sp. To examine plasticity in thermal tolerance and changes in net oxygen exchange when fed and starving, slugs fed each alga were acclimated to 17°C (the current maximum temperature to which they are exposed in nature) and 22°C (the increase predicted for 2100) and measured at different points during starvation. We also examined increased illumination to evaluate a potential tradeoff between increased oxygen production but faster chloroplast degradation. Following acclimation, we subjected slugs to acute thermal stress to determine their thermal tolerance. We also measured net oxygen exchange before and after acute thermal stress. Thermal tolerance improved in slugs acclimated to 22°C, indicating they can acclimate to temperatures higher than they naturally experience. All slugs exhibited net oxygen uptake, and rates were highest in recently fed slugs before exposure to acute thermal stress. Oxygen uptake was suppressed following acute thermal stress. Under brighter light, slugs exhibited improved thermal tolerance, possibly because photosynthetic oxygen production alleviated oxygen limitation. Accordingly, this advantage disappeared later in starvation when photosynthesis ceased. Thus, E. viridis can cope with heatwaves by suppressing metabolism and plastically adjusting heat tolerance; however, starvation influences a slug’s thermal tolerance and oxygen uptake such that continuous access to algal food for its potential nutritive and oxygenic benefits is critical when facing thermal stress.