Microbial to reef scale interactions between the reef-building coral Montastraea annularis and benthic algae

Abstract

Competition between reef-building corals and benthic algae is of key importance for reef dynamics. These interactions occur on many spatial scales, ranging from chemical to regional. Using microprobes, 16S rDNA pyrosequencing and underwater surveys, we examined the interactions between the reef-building coral Montastraea annularis and four types of benthic algae. The macroalgae Dictyota bartayresiana and Halimeda opuntia, as well as a mixed consortium of turf algae, caused hypoxia on the adjacent coral tissue. Turf algae were also associated with major shifts in the bacterial communities at the interaction zones, including more pathogens and virulence genes. In contrast to turf algae, interactions with crustose coralline algae (CCA) and M. annularis did not appear to be antagonistic at any scale. These zones were not hypoxic, the microbes were not pathogen-like and the abundance of coral-CCA interactions was positively correlated with per cent coral cover. We propose a model in which fleshy algae (i.e. some species of turf and fleshy macroalgae) alter benthic competition dynamics by stimulating bacterial respiration and promoting invasion of virulent bacteria on corals. This gives fleshy algae a competitive advantage over corals when human activities, such as overfishing and eutrophication, remove controls on algal abundance. Together, these results demonstrate the intricate connections and mechanisms that structure coral reefs.

Figure 1.

Typical interaction zones between the coral Montastraea annularis and the four types of algae examined. (a) Intact interactions and (b) interactions after algal removal.

Figure 2.

Dissolved oxygen (DO) concentration changes at the zone of interaction between the coral Montastraea annularis and benthic algae. (a) Unaltered coral–algal interactions. (b) Coral–algal interactions 10 days after removal of the algae. DO concentrations are shown relative to atmospheric saturation of sea water (212 µmol l⁻¹). CCA, crustose coralline algae; Dictyota, Dictyota bartayresiana; Halimeda, Halimeda opuntia. n = 5 for all treatments; ±s.e.m.

Figure 3.

Heat map of relative abundance of Bacteria associated with coral–algal interfaces. (a–d) Relative abundances across all five zones of interaction with one type of algae. Bacterial taxa are listed at the highest classifiable level; taxa listed above genus (e.g. family or order) include only members that could not be classified at a lower level. Operational taxonomic units at the top of each list are those most abundant in coral tissue; those at the bottom are the most abundant in the algal tissue. Scale bar represents relative abundance (%) of each taxon within each library. Asterisks indicate taxa over-represented in coral tissue at or near the coral–algal interface.

Figure 4.

Altered metabolic subsystem abundances in coral-associated Bacteria at coral–algal interfaces. Shown are subsystems that were significantly increased or decreased in the Bacteria over-represented in coral tissue at or near at least one type of algal interface. The fold change is relative to corals distant from the interface. Asterisks indicate significant differences (90% confidence levels with 5000 iterations). Blue, CCA; red, Dictyota; yellow, Halimeda; green, turf.

Figure 5.

Abundance of coral–algal interactions across a range of human impact and coral cover. (a) The average per cent of coral colony edge interacting with the indicated type of algae at the seven surveyed sites east to west across Curacao; the remainder of the perimeter not interacting with algae included interactions with sand, sponges and other corals. Numbers above bars indicate the number of coral colonies observed at each site. (b) Relationship between benthic coral coverage and the average per cent of each colony interacting with crustose coralline algae (CCA) at each site (r² = 0.66; p = 0.026). (a) Brown, Cyanobacteria; green, turf; yellow, Halimeda; red, Dictyota; blue, CCA.