Metabolic adjustments and oxidative constraints: transition from intracapsular confinement to pelagic larval life in the marine gastropod Crepipatella peruviana

Abstract

Many marine gastropods show what is called “mixed development,” in which early stages are retained in the mother or in protective egg capsules and later stages are free-living. In molluscs with such mixed development, encapsulation and physical parental care increase embryo viability by protecting them from environmental stressors. Therefore, hatching from the capsule presents a significant physiological challenge as it involves a rapid transition from a hypoxic environment with limited locomotion to a normoxic environment in which active swimming and planktotrophic feeding impose high metabolic demands. The ability of larvae to cope with the new environmental conditions reflects their energetic capacity, which is a proxy for larval activity. This studyevaluated the oxygen consumption rate (OCR) and the oxidative damage/antioxidant response of encapsulated and free-swimming larvae of the marine gastropod Crepipatella peruviana once they have hatched and become incorporated into the pelagic system. The results indicate that the transition of veliger larvae from an encapsulated environment to the water column generates a strong increase in OCR, reflecting the new metabolic demands of swimming, respiration, and larval feeding processes. Despite the increase in OCR levels during the excapsulated larval phase, the pelagic veliger larvae of C. peruviana significantly reduce levels of lipid peroxidation, which may be associated with a high antioxidant capacity. This capacity is maintained during both the encapsulated and excapsulated phases of development. This supports the possibility that C. peruviana larvae exhibit oxidative stress preparation behaviour (POS), since intracapsular hypoxic conditions may induce antioxidant synthesis as an anticipatory mechanism to cope with the elevated oxygen levels the larvae will encounter when they enter pelagic life after hatching. This strategy may confer an adaptive advantage during the transition to a metabolically demanding environment with elevated oxygen levels, highlighting the critical role of encapsulation in larval physiological programming.