Salinity shapes the stress responses and energy reserves of marine polychaetes exposed to warming: From molecular to functional phenotypes

Estuarine systems are critical transition zones influenced by sea, land and freshwater. An array of human activities impacts these areas leading to multiple-stressor interactions. Temperature and salinity are among the most relevant drivers in estuaries, shaping species growth, reproduction and distribution. However, few studies provide an overview of cellular rewiring processes under multiple-stressor environments. Here, we tested how salinity could shape the response of ragworms Hediste diversicolor, an important bioindicator and commercial species, to elevated temperature. We exposed polychaetes to three temperatures for a month, simulating control, ocean warming and heatwave conditions (24, 27 and 30 °C, respectively) combined with two salinities (20 and 30). We quantified whole-organism performance (wet weight gain and survival), along with cellular stress response (CSR) and energy reserves of worms after 14 and 28 days of exposure. Significant three-way interactions between temperature, salinity and exposure time show the non-linearity of molecular responses. Worms at a salinity of 20 were more sensitive to warming than worms exposed to a salinity of 30. The combination of high temperature and low salinity can act synergistically to induce oxidative stress and macromolecular damage in worm tissues. This finding was supported by an induction of the CSR, with a concomitant decrease of energy reserves, pointing towards a metabolic compensation strategy. However, under a higher salinity (30), the need for a CSR upon thermal challenge was reduced and energy content increased with temperature, which suggests that environmental conditions were within the optimum range. Heatwaves striking low-salinity areas of estuaries can therefore negatively impact the cellular physiology of H. diversicolor, with greater metabolic costs. However, extreme stress levels were not reached as worms incremented wet weight and survival was high under all conditions tested. Our findings are important for the optimization of ragworm aquaculture and adaptive conservation strategies of estuarine systems.