Abstract
Because seaweeds uncontrolled by herbivores can overgrow and kill corals, competition can exclude corals from temperate latitudes where herbivores generally fail to control seaweed biomass. In this study, we show that the coral Oculina arbuscula persists on reefs in temperate North Carolina where seaweeds are common by harboring the omnivorous crab Mithrax forceps, which removes seaweeds and invertebrates growing on or near the coral. In the field, corals from which crabs are experimentally removed develop a dense cover of epibionts, exhibiting reduced growth and increased mortality relative to corals with crabs, which remain epibiont-free. This crab is unusual in that it readily consumes all local seaweeds in laboratory choice assays and is not deterred by chemical defenses that suppress feeding by local fishes, sea urchins, and other crabs. This allows Mithrax to defend corals from overgrowth by chemically noxious seaweeds like Dictyota and Sargassum that are avoided by most local herbivores. However, further field manipulations under reduced light conditions demonstrate that the outcome of the crab–coral interaction is context-dependent: crabs only benefit corals in well-lit areas where seaweeds are abundant. Field observations and tethering experiments show that, by living in association with Oculina, Mithrax gains a refuge from predation. Additionally, crabs grow faster when associated with live corals than with structurally equivalent dead corals, apparently because they are able to consume lipid-rich coral mucus. This mucus provides a dietary supplement that may help corals attract and retain low-mobility symbionts such as Mithrax, securing for the coral long-term and predictable protection against competitors. Structurally complex but competitively inferior organisms, like some corals and coralline algae, provide the biogenic habitat complexity upon which many other species depend. Because these sessile organisms may be dependent on symbionts to remove superior competitors, mutualisms can play an important, but currently underappreciated, role in structuring marine communities where biotic interactions are intense. In this study, the mutualism between Oculina and Mithrax promotes the persistence of both species in habitats from which they might otherwise be excluded by competition and predation.
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