Starvation and dormancy in marine gastropods: taxonomic and ecological patterns, and energetic implications

ABSTRACT Dormancy, defined as an extended rest period of an animal, is widespread across the tree of life. Although characteristic of all terrestrial gastropods, the nature and distribution of dormancy in marine gastropods are complex and poorly understood. Dormancy carries serious implications for organismal energetics, motivating assessment of how it relates to taxonomic, ecological (habitat type), trophic and climatic (latitudinal) attributes of marine gastropods. We first undertook a meta-analytical assessment of the effects of these attributes on starvation tolerance, as an estimate of dormancy capacity. We then experimentally assessed survival and physiological integrity of prolonged dormancy in mangrove snails and compared physiological thermal performance between starved and unstarved high and low rocky-shore snails. Our meta-analysis revealed dormancy capacity was significantly influenced by taxonomic group and habitat, but not by trophic niche or latitude. This capacity was enhanced in the evolutionarily advanced lineages (Caenogastropoda, Heterobranchia and Neritimorpha) compared to the primitive lineages (Vetigastropoda and Patellogastropoda), and in supratidal compared to intertidal and subtidal gastropods. The laboratory experiments showed that mangrove species (including Littorinoidea, Cerithidiodea, Muricoidea and Ellobioidea) survive and maintain robust cardiac activity following starvation and that starvation differentially influenced thermal physiological performance between high and low rocky-shore snails. Starvation increased cardiac thermal independence, suppressed HRmax (indicative of metabolic depression) and lowered thermal tolerance in the high-shore Planaxis sulcatus (90 days), whereas in the low-shore Trochus radiatus (6 days), this caused gross cardiac irregularities, indicative of physiological stress. Our findings suggest starvation tolerance is lineage dependent but has emerged independently within a lineage in response to a lifestyle (trophic behaviour, habit, and habitat) that limits regular food intake. Because dormancy is widespread across marine gastropods and is rapidly elicited in direct response to environmental change, its inclusion into theoretical contexts and empirical protocols is crucial for realistic interpretation and understanding of gastropod organismal energetics.