Molecular Commerce on Coral Reefs: Using Metabolomics to Reveal Biochemical Exchanges Underlying Holobiont Biology and the Ecology of Coastal Ecosystems

The rapidly advancing field of metabolomics encompasses a diverse suite of powerful analytical and bioinformatic tools that can help to reveal the diversity and activity of chemical compounds in individual organisms, species interactions, and entire ecosystems. In this perspective we use examples from studies of coral reefs to illustrate ways in which metabolomics has been and can be applied to understand coastal ecosystems. Examples of new insights that can be provided by metabolomics include resolving metabolite exchange between microbes and animals in holobiont tissues, identifying the relevant metabolite exchanges associated with the onset and maintenance of diverse bacterial endosymbionts, characterizing unknown molecules associated with coral reproductive cues, or defining the suites of compounds involved in coral-algal competition and microbialization of algal-dominated ecosystems. Here we outline sampling, analytical and informatic methods that marine biologists and ecologists can apply to understand the role of chemical processes in ecosystems, with a focus on open access data analysis workflows and democratized databases. This perspective aims to demonstrate that metabolomics tools and bioinformatics approaches which leverage open access chemical databases can provide scientists the opportunity to map detailed metabolic inventories and dynamics for a holistic view of the relationships among reef organisms, their symbionts and their surrounding marine environment.

Seasonal shifts in the competitive ability of macroalgae influence the outcomes of coral–algal competition

Understanding the effects of natural processes on coral–algal competition is an important step in identifying the role of macroalgae in perturbed coral reef ecosystems. However, studies investigating coral–algal interactions are often conducted in response to a disturbance, and rarely incorporate seasonal variability. Here, naturally occurring coral–algal interactions were assessed in situ four times a year over 2 years across eight sites spanning diverse benthic communities. In over 6500 recorded coral–algal interactions, cyanobacteria and turf algae were found to be the most damaging regardless of season, resulting in visible damage to coral in greater than 95% of interactions. Macroalgae that primarily compete using chemical mechanisms were found to be more damaging than those that compete using physical mechanisms (e.g. abrasion), with both groups demonstrating decreased competitive ability in summer. While crustose coralline algae were the least damaging to competing coral, during summer, it became three times more competitive. Our results demonstrate that the competitive ability of macroalgae and the outcomes of coral–algal competition can fluctuate in seasonal cycles that may be related to biomass, production of chemical defences and/or physical toughness. The results of this study have important implications for understanding the trajectory and resilience of coral reef ecosystems into the future.

Herbivorous damselfishes expand their territories after causing white scars on Porites corals

Turf algae become the most abundant benthic group on coral reefs after mass coral bleaching. By defending feeding territories, damselfishes enhance the growth of turf algae in so-called algal farms and affect coral communities both directly and indirectly. We found several white scars (i.e., bite lesions) on massive Porites colonies around feeding territories. In this study, we examined the occurrence of white scars on corals and their function in coral–algal competition at the boundaries between algal farms of two damselfish species—the intensive farmer Stegastes nigricans, and the intermediate farmer S. lividus—and adjacent Porites corals for 3 years around Okinawa Island, Japan. White scars occurred on Porites colonies only adjacent to the territories of both damselfish species. Of the white scars on corals around S. nigricans territories, 73% of the area was covered by algae within 2 weeks, while the remaining was re-covered by Porites tissues. The coral–algal boundaries encroached further into areas of coral when the area of white scars were larger. These results suggest that both intensive and intermediate farmers bite adjacent Porites colonies causing white scars on corals, and expand their territories onto corals using algae-covered white scars as stepping stones.

Coral-algal interactions at Weizhou Island in the northern South China Sea: variations by taxa and the exacerbating impact of sediments trapped in turf algae

Competitive interactions between corals and benthic algae are increasingly frequent on degrading coral reefs, but the processes and mechanisms surrounding the interactions, as well as the exacerbating effects of sediments trapped in turf algae, are poorly described. We surveyed the frequency, proportion, and outcomes of interactions between benthic algae (turf algae and macroalgae) and 631 corals (genera: Porites, Favites, Favia, Platygyra, and Pavona) on a degenerating reef in the northern South China Sea, with a specific focus on the negative effects of algal contact on corals. Our data indicated that turf algae were the main algal competitors for each surveyed coral genus and the proportion of algal contact along the coral edges varied significantly among the coral genera and the algal types. The proportions of algal wins between corals and turf algae or macroalgae differed significantly among coral genera. Compared to macroalgae, turf algae consistently yielded more algal wins and fewer coral wins on all coral genera. Amongst the coral genera, Porites was the most easily damaged by algal competition. The proportions of turf algal wins on the coral genera increased 1.1–1.9 times in the presence of sediments. Furthermore, the proportions of algal wins on massive and encrusting corals significantly increased with the combination of sediments and turf algae as the algal type. However, the variation in proportions of algal wins between massive and encrusting corals disappeared as sediments became trapped in turf algae. Sediments bound within turf algae further induced damage to corals and reduced the competitive advantage of the different coral growth forms in their competitive interactions with adjacent turf algae.

Positive association between epiphytes and competitiveness of the brown algal genus Lobophora against corals

Observations of coral–algal competition can provide valuable information about the state of coral reef ecosystems. Here, we report contact rates and apparent competition states for six shallow lagoonal reefs in Fiji. A total of 81.4% of examined coral perimeters were found to be in contact with algae, with turf algae (54.7%) and macroalgae of the genus Lobophora (16.8%) representing the most frequently observed contacts. Turf algae competitiveness was low, with 21.8% of coral–turf contacts being won by the algae (i.e. overgrowth or bleaching of coral tissue). In contrast, Lobophora competitiveness against corals was high, with 62.5% of contacts being won by the alga. The presence of epiphytic algae on Lobophora was associated with significantly greater algal competitiveness against corals, with 75.8% and 21.1% of interactions recorded as algal wins in the presence and absence of epiphytes, respectively. Sedimentation rate, herbivorous fish biomass, and coral colony size did not have a significant effect on Lobophora–coral interactions. This research indicates a novel and important role of epiphytes in driving the outcome of coral–algal contacts.