Metabolic trade-offs shape acute thermal responses in the marine predator Rapana venosa

Ocean warming poses disproportionate threats to active marine predators due to their high metabolic demands. However, the coordinated survival strategy centered on energy adjustment they adopted remains unclear. Here we investigated thermal responses of the predatory gastropod Rapana venosa by integrating metabolic rate measurements with tissue-specific transcriptomics across ecologically relevant temperatures (20-35 °C). Standard metabolic rate exhibited a unimodal curve, peaking at the current summer extreme of 29 °C, and declining sharply at higher temperatures, indicating a narrow thermal performance window. Transcriptomic analyses revealed severity-dependent, hierarchical activation of cellular stress responses: moderate heat (29 °C) primarily induced heat shock proteins (e.g., hsp70, hsp90), whereas severe stress (35 °C) engaged anti-apoptotic pathways. Concurrently, key genes governing gluconeogenesis, lipogenesis, and ATP hydrolysis were progressively downregulated, reflecting strategic reallocation of energy from growth/maintenance to survival. Tissue-specific responses diverged as gills mounted aggressive oxidative defense and apoptosis regulation, while foot muscle conserved energy through metabolic suppression and prioritized protein-folding machinery. This functional division optimizes resilience but creates a critical decoupling: aerobic scope contraction at 29-32 °C combined with locomotor tissue metabolic suppression mechanistically suggest impairment of foraging and escape, consistent with published data showing feeding performance declines above 30 °C, before physiological failure above 35 °C. Our findings underscore the vulnerability of metabolically demanding predators to future ocean warming and emphasize the need to consider both physiological and molecular signatures of performance decline when predicting climate change impacts on marine food webs.