Predator-induced shifts in energy metabolism: Anaerobic activation in juvenile sea cucumbers

Abstract

The sea cucumber Stichopus monotuberculatus serves as a primary species for benthic ecological restoration in southern China, and has significant economic value. However, pressure from their predators remains a critical factor constraining their survival rates during stocking in marine ranching. To study the effect of fear from predator, the physiological responses of S. monotuberculatus to different risk cues were evaluated: cues from crab Portunus pelagicus group (PPG), same-species injury group (SSIG), and different-species injury group (DSIG). Results showed under PPG treatment, oxygen consumption initially decreased but surged upon repeated exposure, indicating an adjustment to acute stress. Injury cues from sea cucumbers (conspecific, SSIG and heterospecific, DSIG) resulted in metabolic peaks at 6 h and 12 h respectively. At the 6 h time point, DSIG elicited higher ammonia excretion and a markedly elevated O:N ratio, reflecting a major shift in metabolic pathways toward non-protein energy substrates. Under exposure to PPG, ATP levels surged 20-fold at 1 h, reaching 14,353.81 ± 1308.36 μmol·gprot⁻¹. Meanwhile, the activities of lactate dehydrogenase (LDH) and hexokinase (HK) significantly increased, while pyruvate dehydrogenase (PDH) activity decreased, which indicated that anaerobic metabolism dominates during acute stress from predator crab. Under DSIG treatment, PDH and HK activities first increased and then decreased, accompanied by slower ATP recovery than PPG treatment, which reflects the adjustment of aerobic metabolism in response to heterospecific injury cues. This study reveals that S. monotuberculatus dynamically modulates its metabolic physiology in response to varying predation risks, employing acute anaerobic responses under crab threats and shifting toward aerobic metabolic reorganization under heterospecific injury cues. These findings enhance our understanding of how juvenile sea cucumbers adjusted physiologically to predation pressure, providing a theoretical basis for development of predator stress modification strategies for its bottom sowing and stock enhancement practices.