Chemically mediated competition, herbivory, and the structure of coral reefs

Corals, the foundation species of tropical reefs, are in rapid global decline as a result of anthropogenic disturbance. On many reefs, losses of coral have coincided with the over-harvesting of reef herbivores, resulting in ecosystem phase-shifts from coral to macroalgal dominance. It is hypothesized that abundant macroalgae inhibit coral recovery and recruitment, thereby generating ecological feedback processes that reinforce phase-shifts to macroalgae and further diminish reef function. However the extent to which macroalgae directly outcompete coral, the mechanisms involved, and the speciesspecificity of algal-coral competition remains debated. Moreover the capacity for herbivores to prevent vs. reverse ecosystem phase-shifts to macroalgae, and the roles of herbivore diversity in such phenomen remain poorly understood.;Here I demonstrate using field experiments in the tropical Pacific (Fiji) and Caribbean Sea (Panama) that numerous macroalgae directly damage corals, and do so by transferring hydrophobic allelochemicals from algal to coral surfaces upon contact. Algal allelochemicals caused coral damage and/or mortality in ∼75% of the 39 interactions studied, and allelopathic effects of algae on coral were generally localized to areas of direct contact. Coral sensitivity to algal allelopathy was highly species-specific. For two of the most damaging algae, I identified a subset of the molecules responsible for their allelopathic activity -- these terpenoid molecules are the first identified allelochemicals that harm reef-building corals. Together these findings suggest that allelopathic algalcoral competition may commonly limit coral recovery on reefs lacking sufficient herbivory, and therefore reinforce ecosystem phase-shifts to macroalgae.;Here I also demonstrate with field experiments in Fiji that herbivory has the potential to both prevent and reverse coral reef phase-shifts to macroalgae. Herbivory inhibited the establishment of late-succession macroalgae on artificial substrates, both inside and outside of a marine reserve, during a 152 day field study; in contrast, herbivore exclusion resulted in macroalgal proliferation. Nutrient enrichment had little effect on algal growth, indicating top-down control of algal succession on coral reefs. In addition, herbivores consumed all macroalgae used in my algal-coral competition experiments when deployed in marine reserves. Macroalgal consumption could be attributed to feeding by just four fish species, and no macroalgae escaped predation because of complementary feeding among these herbivores; the most allelopathic algae were each consumed by different fish species. Complementary feeding among herbivores was driven largely by their differential tolerances to algal chemical defenses. Also, herbivores preventing the establishment of late-succession macroalgae (by scraping the substratum) differed fundamentally from those fishes removing established macroalgae. Thus, chemically mediated feeding complementarity makes herbivore diversity essential for preventing and reversing phase-shifts on coral reefs, and limiting the negative effects of algae on coral.;Finally, I demonstrate with field experiments in Fiji that competition and herbivory interact via macroalgal secondary chemistry. A chemically rich macroalga simultaneously induced allelochemicals and decreased anti-herbivore chemical defenses in response to competition with coral, resulting in an ecological trade-off for the alga -- increased competitive ability but also increased susceptibility to predation in the field. This pattern for the alga was likely due to a trade-off in the production of different molecules responsible for deterring competitors vs. consumers. If common among allelopathic algae, trade-offs in defensive chemistry may increase herbivore control of allelopathic algae or attenuate algal effects on coral, thus altering the role of allelopathic algae in ecological feedback processes limiting reef recovery.;Coral reefs provide ecosystem services critical to human societies, but are declining at alarming rates. These studies provide evidence that chemically mediated competitive and consumer-prey interactions play important roles in the underlying processes driving coral reef degradation and recovery. Moreover these studies suggest that competition and predation interact in complex ways to affect the ecology and evolution of chemical defense in macroalgae. By providing mechanistic-level insights into the processes controlling coral reef structure and function, such findings should be of broad interest to ecologists, and should also provide resource managers with critical information needed for effective management of these dynamic and diverse, but threatened ecosystems.