Marine and terrestrial herbivores display convergent chemical ecology despite 400 million years of independent evolution

Abstract

Chemical cues regulate key ecological interactions in marine and terrestrial ecosystems. They are particularly important in terrestrial plant-herbivore interactions, where they mediate both herbivore foraging and plant defense. Although well described for terrestrial interactions, the identity and ecological importance of herbivore foraging cues in marine ecosystems remain unknown. Here we show that the specialist gastropod Elysia tuca hunts its seaweed prey, Halimeda incrassata, by tracking 4-hydroxybenzoic acid to find vegetative prey and the defensive metabolite halimedatetraacetate to find reproductive prey. Foraging cues were predicted to be polar compounds but instead were nonpolar secondary metabolites similar to those used by specialist terrestrial insects. Tracking halimedatetraacetate enables Elysia to increase in abundance by 12-to 18-fold on reproductive Halimeda, despite reproduction in Halimeda being rare and lasting for only ∼36 h. Elysia swarm to reproductive Halimeda where they consume the alga's gametes, which are resource rich but are chemically defended from most consumers. Elysia sequester functional chloroplasts and halimedatetraacetate from Halimeda to become photosynthetic and chemically defended. Feeding by Elysia suppresses the growth of vegetative Halimeda by ∼50%. Halimeda responds by dropping branches occupied by Elysia, apparently to prevent fungal infection associated with Elysia feeding. Elysia is remarkably similar to some terrestrial insects, not only in its hunting strategy, but also its feeding method, defense tactics, and effects on prey behavior and performance. Such striking parallels indicate that specialist herbivores in marine and terrestrial systems can evolve convergent ecological strategies despite 400 million years of independent evolution in vastly different habitats.C hemical cues and signals govern the processes that shape species demography, community structure, and ecosystem function in both terrestrial and marine ecosystems. However, the chemicals regulating these processes are better known for terrestrial systems, especially with regard to plant-herbivore interactions (1, 2). Terrestrial insect herbivores, most of which are trophic specialists (3), commonly locate prey by tracking plant volatiles (4). In response, plants induce chemical defenses both to reduce herbivory and to limit the spread of pathogens introduced by herbivore feeding (5); some also release volatile compounds that attract predators of their herbivores (6, 7). These volatile compounds involved in insect foraging and plant defense are well described; generally, they are nonpolar secondary compounds (or blends of compounds) that are plantspecific. In contrast, few herbivores in marine ecosystems are trophic specialists (8), and whether they use chemical cues to locate their prey remains poorly understood (9, 10). The identities of such foraging cues are unknown but are predicted to be polar compounds that diffuse readily through water (9, 10).Halimeda incrassata is the dominant seaweed within ...

The emergent role of small-bodied herbivores in pre-empting phase shifts on degraded coral reefs

“…The one alga species not affected, Halimeda spp., has strong structural and chemical defenses against most herbivores24 explaining why it alone persisted. Slight decreases in the abundance of Halimeda in the caged treatment may have been due to secondary effects of transplantation, or to the presence of a small Halimeda- specialist herbivore, such as the sea slug Elysia luca 25, which would itself have benefited from the protection of cages. Second, there was a positive response of algal recruitment and growth when herbivory was limited by caging or territorial damselfish in our herbivory x nutrient experiment.…”

Detection of a chemical cue from the host seaweed Laurencia dendroidea by the associated mollusc Aplysia brasiliana

“…Liposoluble terpenoids can mediate different alga-herbivore interactions. Halimedatetraacetate is a sesquiterpenoid produced by the green alga Halimeda incrassata identified as a foraging cue for the specialist gastropod Elysia tuca [ 38 ]. As one of the few herbivores that preferentially consume Halimeda species, Elysia may locate its prey by tracking Halimeda -derived chemical cues.…”

Bacterial diversity in theclarkiecotype of the photosynthetic sacoglossan,Elysia crispata

“…Sacoglossan sea slugs are a group of herbivorous marine gastropods that feed suctorially on siphonaceous green algae. The close relationship that these slugs have with their algal food has caused them to receive some attention for a variety of reasons including their ability to sequester chemical secondary metabolites from host algae (Marin & Ros, 2004), convergent ecological roles similar to terrestrial insects (Rasher et al, 2015) and due to the unusual ability found in some species to sequester algal chloroplasts known as kleptoplasty (reviewed by Pierce & Curtis, 2012; Pierce, Curtis, & Middlebrooks, 2015). Despite interest in some areas of their biology, much about the sacoglossans generally remains poorly studied.…”