Impacts of marine heatwave stress and harmful algal (Alexandrium spp.) exposure on subadult green-lipped mussels (Perna canaliculus)

Marine heatwaves (MHWs) are increasing globally, including around Aotearoa New Zealand (NZ), where the Tasman Sea is a recognised hotspot. Harmful algal blooms (HABs) represent an additional climate-linked stressor, with species such as the paralytic shellfish toxin (PST) producing dinoflagellate Alexandrium pacificum becoming more frequent with ocean warming, stratification, and nutrient enrichment. In the Marlborough Sounds-NZ's largest green-lipped mussel (GLM, Perna canaliculus) farming area-A. pacificum blooms now coincide with MHWs. This study exposed subadult GLM to two temperatures-17 °C (control) and 22 °C (peak MHW temperature)-and either PST-producing A. pacificum or non-PST-producing Alexandrium minutum combined with a control diet for two weeks. Physiological and molecular endpoints measured included PST accumulation, global DNA methylation in gills, immune responses, lipid profiles, and tissue pathology. Peak MHW-exposed mussels had depleted glycogen reserves, suggesting increased metabolic demand, and accumulated 1.8X less PSTs than mussels at 17 °C, a potentially favourable finding for aquaculture. At 17 °C, A. pacificum exposure induced greater hemocyte mortality and diapedesis compared to mussels at 22 °C, indicating enhanced immune activation but more immune cell death. Mussels at 22 °C displayed a dampened immune response relative to those at 17 °C based on hemocyte responses and histological analyses. DNA methylation in gill tissue was 1.7X higher at 22 °C, suggesting possible epigenetic regulation of responses. These findings highlight the importance of considering both independent and interactive effects of MHWs and HABs. While temperature influenced metabolic and epigenetic responses, Alexandrium exposure shaped outcomes in immune performance and toxin accumulation.