The chemical ecology of the soft coral-zooxanthellae association and its signficance to the bleaching process

Biochemical changes in soft corals (Lobophytum compactum and Sinularia flexibilis) affected by bleaching were investigated, with the ultimate aim of understanding how molecular changes are linked to biological responses observed in the wake of bleaching events. Annual variation in photo-protective mycosporine-like amino acids (MAAs) in soft coral populations provides the first evidence that MAA tissue concentrations are positively correlated with seasonal cycles in both solar irradiance and sea-surface temperatures. The timing of peak concentrations of MAAs in summer when exposure to solar irradiance and sea temperatures are greatest, and in female colonies prior to spawning, further corroborate their role as photo-protectants. In manipulative bleaching experiments elevated UVR and temperature were found to act synergistically in the bleaching process. However, chemical degradation of MAAs during exposure to elevated temperature is not, as previously assumed, the key to understanding the synergistic interaction. In fact, MAA levels increased in response to simultaneous exposure to high temperature and UVR, in both experimentally and naturally bleached colonies, suggesting increased resource allocation towards photo-protection in corals already experiencing thermal stress. Soft coral responded to bleaching by increasing the production of terpenoid secondary metabolites, which aid in the prevention of microbial and algal fouling. While changes in secondary metabolites were short-lived, a substantial increase of an anti-microbial agent in S. flexibilis may have contributed to the prevention of fouling by opportunistic bacteria. This suggests that soft corals may alter their secondary metabolite chemistry to prevent fouling by opportunistic bacteria following bleaching. These experimental results were validated through analysis of soft corals affected by the 1998 mass bleaching event, where bleached colonies with high levels of algaecides remained free of fouling, while conspecifics with substantially lower levels were found to be overgrown. This suggests that soft corals are capable of surviving short-term bleaching events and detrimental algal overgrowth that is often associated with bleaching, by regulating their secondary metabolite chemistry to counteract fouling. Understanding the role of symbiotic zooxanthellae in the production of terpenoid secondary metabolites is integral to evaluating the full impact of bleaching disturbances on the soft coral host. Zooxanthella cross-infection experiments with freshly metamorphosed polyps of Lobophytum compactum demonstrated that control over the production of secondary metabolite lies with the animal host. Moreover, the equivalence of secondary metabolite chemistry in apo-and symbiotic polyps clearly shows that the algal partner is not essential for biosynthesis. Despite no direct algal involvement in terpene production, a strong correlation between polyp growth and investment into terpenes suggests that, via their contribution to coral nutrition through primary metabolism, zooxanthellae have the capacity to indirectly influence secondary metabolism. The implications for bleached soft corals are that while the host, with or without energetic contributions from the algal symbiont controls the production of ecologically important terpenes, energy reserves may be insufficient to maintain the production of ecologically significant concentrations. Severe experimental bleaching was found to have long-term sub-lethal impacts on soft corals, reducing overall reproductive output of Lobophytum compactum for at least two spawning seasons. Polyp fecundity and mean egg diameters were inversely correlated with the degree of bleaching, with complete failure of fertilisation in heavily bleached colonies in the first year and significantly reduced fecundity in the second year after the bleaching event. Although bleached corals recovered their zooxanthellae within 4 months, protein, lipid, MAA and carotenoid concentrations were reduced for at least eight months in adult tissues. The reductions were amplified when they were passed on to gametes, with the greatest reductions occurring in lipid and protein concentrations. Although reductions in MAAs were relatively smaller when passed on to gametes, even minor proportional reductions have significant implications for larval survival, given that MAA levels are approximately three times higher in eggs than in maternal tissues. By the second spawning season (20 months after experimental bleaching) the biochemical compositions of both adult tissues and their gametes were indistinguishable from those of control (unbleached) corals.