Unraveling the Phidiana paradox: Phidiana lynceus can retain algal symbionts but its nocturnal tendencies prevent benefits from photosynthesis

Abstract

Numerous marine invertebrates form symbiotic relationships with single-celled algae, termed “photosymbioses”, and the diversity of these interactions is likely underestimated. We examined Phidiana lynceus, a cladobranch sea slug that feeds on photosymbiotic hydrozoans. We assessed its ability to acquire/retain algal symbionts by examining specimens in starvation, finding that P. lynceus is able to incorporate and retain symbionts for up to 20 days. Examining body size during starvation revealed that P. lynceus does not receive enough energy from hosting symbionts to maintain its body mass let alone grow. Intact symbionts were still present in deceased specimens, indicating that P. lynceus does not digest all of its symbionts, even when starving to death. We also examined slug behavior in the field and lab to determine if it seeks light to facilitate photosynthesis, which could provide energetic and oxygenic benefits. In the field, slugs were always observed hiding under stones during the day and they displayed light avoidance in the lab, suggesting this species actively prevents photosynthesis and the benefits it could receive. Lastly, we measured their metabolic rates during the day and night and when treated with and without a photosynthetic inhibitor. Higher metabolic rates at night indicate that this species displays nocturnal tendencies, expending more energy when it emerges at night to forage. Paradoxically, P. lynceus has evolved all of the requisite adaptations to profit from photosymbiosis but it chooses to live in the dark instead, calling into question the nature of this symbiosis and what each partner might receive from their interaction.