Diffuse Coevolutionary Arms Race Among Herbivorous Sea Urchins and Chemically-Rich Seaweeds

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Craft, Jonathan Douglas
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A diffuse coevolutionary arms-race between seaweeds and their herbivores is hypothesized to have operated on tropical reefs. Herbivorous sea urchins strongly structure seaweed communities on temperate and tropical reefs, and the diversity and concentrations of lipophilic secondary metabolites found in seaweeds from tropical floras are higher than those from temperate floras. However, the coevolutionary prediction that tropical herbivores have evolved stronger feeding resistance toward these seaweed metabolites has received little attention. I assessed the feeding responses of seven lineages of tropical and temperate sea urchin species toward lipophilic extracts from tropical seaweeds using a series of laboratory-based feeding preference assays. Consistent with a coevolutionary expectation, tropical urchins in the genera Diadema, Echinometra, and Arbacia were more willing to consume lipophilic chemical defenses from tropical seaweeds than were temperate urchins in the genera Strongylocentrotus and Arbacia. Although little is known about the mechanisms that underlie differences among herbivore species in their feeding resistance to seaweed secondary metabolites, one candidate protein family is glutathione S-transferase (GST). These detoxification enzymes are known to facilitate metabolic resistance to plant chemical defenses in terrestrial herbivores. I surveyed constitutive GST levels in the digestive tract of six urchin species and found that the most omnivorous of these urchins (Arbacia punctulata) had significantly higher constitutive levels of GST. I tested the inducibility of GST in A. punctulata after offering urchins foods with or without seaweed secondary metabolites and at multiple water temperatures. These induction experiments suggested that GST is not induced by lipophilic secondary metabolites from tropical seaweeds; however, when Arbacia punctulata were exposed to colder temperatures than typically experienced in nature, the individuals exhibited higher GST levels, suggesting oxidative stress. When cold-stressed these urchins reduced their feeding rate on and preference toward a lipophilic extract from Dictyota pulchella. Thus, cold-stress can compromise feeding resistance to seaweed chemical defenses. This finding has broad implications for seaweed-herbivore dynamics during cold exposure caused by upwellings, seasonality, and climate change.
Sea urchins -- Ecology; Sea urchins -- Effect of cold on; Marine algae as food