Parasitism enhances gastropod feeding on invasive and native algae while altering essential energy reserves for organismal homeostasis upon warming

Abstract

Marine bioinvasions are of increasing attention due to their potential of causing ecological and economic loss. The seaweed Gracilaria vermiculophylla has recently invaded the Baltic Sea, where, under certain conditions, it was found to outcompete the native alga Fucus vesiculosus. Parasites of grazers and temperature are among the potential factors which might indirectly modulate the interactions between these co-occurring algae through their single and combined effects on grazing rates. We tested the temperature and parasitism effects on the feeding of the gastropod Littorina littorea on F. vesiculosus vs. G. vermiculophylla. Uninfected and trematode-infected gastropods were exposed to 10, 16, 22, and 28 °C for 4 days while fed with either algae. Faeces production was determined as a proxy for grazing rate, and HSP70 expression, glycogen and lipid concentrations were used to assess the gastropod's biochemical condition. Gracilaria vermiculophylla was grazed more than F. vesiculosus. Trematode infection significantly enhanced faeces production, decreased glycogen concentrations, and increased lipid concentrations in the gastropod. Warming significantly affected glycogen and lipid concentrations, with glycogen peaking at 16 °C and lipids at 22 °C. Although not significant, warming and trematode infection increased HSP70 levels. Increased faeces production in infected snails and higher faeces production by L. littorea fed with G. vermiculophylla compared to those which fed on F. vesiculosus, suggest parasitism as an important indirect modulator of the interaction between these algae. The changes in the gastropod's biochemical condition indicate that thermal stress induced the mobilization of energy reserves, suggesting a possible onset of compensatory metabolism. Finally, glycogen decrease in infected snails compared to uninfected ones might make them more susceptible to thermal stress.

Keywords: Climate change; Global warming; Himasthla elongata; Invasion biology; Parasites; Species interactions.