Chemically rich seaweeds poison corals when not controlled by herbivores

Abstract

Coral reefs are in dramatic global decline, with seaweeds commonly replacing corals. It is unclear, however, whether seaweeds harm corals directly or colonize opportunistically following their decline and then suppress coral recruitment. In the Caribbean and tropical Pacific, we show that, when protected from herbivores, ∼40 to 70% of common seaweeds cause bleaching and death of coral tissue when in direct contact. For seaweeds that harmed coral tissues, their lipid-soluble extracts also produced rapid bleaching. Coral bleaching and mortality was limited to areas of direct contact with seaweeds or their extracts. These patterns suggest that allelopathic seaweed-coral interactions can be important on reefs lacking herbivore control of seaweeds, and that these interactions involve lipid-soluble metabolites transferred via direct contact. Seaweeds were rapidly consumed when placed on a Pacific reef protected from fishing but were left intact or consumed at slower rates on an adjacent fished reef, indicating that herbivory will suppress seaweeds and lower frequency of allelopathic damage to corals if reefs retain intact food webs. With continued removal of herbivores from coral reefs, seaweeds are becoming more common. This occurrence will lead to increasing frequency of seaweed-coral contacts, increasing allelopathic suppression of remaining corals, and continuing decline of reef corals.A s foundation species, corals promote marine biodiversity, support a multitude of ecosystem functions, and provide goods and services critical to human societies (1, 2). However, coral reefs are in global decline, with reefs commonly converting from species-rich and topographically complex communities dominated by corals to species-poor and topographically simplified communities dominated by seaweeds (3-7). In the Caribbean, average cover of hard corals has declined by ∼80% in the last 3 decades (5) and more than 30% of the world's coral species face elevated risk of extinction (6). Monitoring (7), field experiments (8-10), and a meta-analysis (11) all indicate that herbivory is critical in preventing seaweed replacement of corals. However, the extent to which seaweeds drive these shifts by outcompeting adult corals in the absence of herbivory, or proliferate only after coral mortality is triggered by other causes (such as disease or bleaching) is debated (12-15). To compound this uncertainty, studies addressing seaweed-coral competition have: (i) produced variable results, (ii) rarely been conducted using numerous species-pairings, (iii) varied in experimental techniques (complicating comparisons), and (iv) sometimes been conducted in laboratory settings lacking ecologically realistic conditions (e.g., flow and turbulence). Thus, the general importance of competition between established seaweeds and corals remains uncertain. An understanding of mechanisms determining the outcomes of seaweed-coral interactions, and of how herbivory mediates these interactions, is needed if reefs are to be better managed, especially with the continu...

Macroalgal terpenes function as allelopathic agents against reef corals

“…A previous study discovered similar patterns for these macroalgae and the coral Porites cylindrica in Fiji (18), but no allelopathic compounds were identified, and it was not possible to assess whether that single coral species was typical or unusual relative to other corals. The present more inclusive study demonstrates that chemical mediation of algal-coral competition is common, and although the magnitude of algal effects varies Fig.…”

“…The hydrophobicity of these allelochemicals likely makes them efficient surface-mediated toxins because their water solubility is very low, allowing these compounds to be retained at algal-coral interfaces. Allelopathic interactions documented among other reef species also occur as the result of transfer of compounds by contact rather than dissolution through the water (18,22,(28)(29)(30), indicating that in general allelopathic compounds may be hydrophobic rather than hydrophilic in benthic marine systems.…”

“…Visual bleaching and photosynthetic efficiency were correlated for all three corals (r = −0.80 to −0.96, P < 0.001 for all comparisons) (Fig. S1); thus, PAM fluorometry measurements are indicative of visual bleaching but are less subjective (17,18,21,22). The most resistant coral was Montipora digitata; for this coral, Dictyota bartayresiana, Galaxaura filamentosa, and Chlorodesmis fastigiata caused significant bleaching and suppression of photosynthetic efficiency, whereas Liagora sp.…”

“…However, the consequences of and mechanisms driving most algal-coral interactions remain poorly understood. Recent field studies suggest that macroalgae may damage corals by (i) shading and abrasion (15), (ii) vectoring of coral disease (16), (iii) release of water-soluble compounds that stimulate harmful, coral-associated microbes (17), or (iv) transfer of hydrophobic allelochemicals by direct contact (18). However, for most of these studies, it is unclear whether the findings are particular to the macroalgal and coral species tested or are common to algal-coral interactions in general and could thus transform the way ecologists and resource managers view processes driving phase-shifts on coral reefs.…”

“…However, for most of these studies, it is unclear whether the findings are particular to the macroalgal and coral species tested or are common to algal-coral interactions in general and could thus transform the way ecologists and resource managers view processes driving phase-shifts on coral reefs. Despite recent studies demonstrating the potential importance of chemically mediated algalcoral competition (17)(18)(19) and its increasing impact as the result of ocean acidification (20), no algal compounds mediating these interactions have been identified.…”