Testing the role of consumers in coral microbiome dispersal and assembly

Carsten G.B. Grupstra, Lauren I Howe-Kerr, Alex J Veglia, Kristen M Rabbitt, Samantha R Coy and Adrienne M.S. Correa, BioSciences, Rice University, Houston, TX, Erika J Eliason and Deron E. Burkepile, Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, Santa Barbara, CA

Background/Question/Methods
Symbioses between microorganisms and foundation species, such as various plants, sponges and stony corals, underpin the biodiversity, productivity, and stability of ecosystems. Consumers such as herbivores and predators shape communities of foundation species through trophic interactions that alter inter- and intraspecific competition. However, the roles of consumers in driving microbiome assembly in foundation species are rarely examined. Here, we investigated the potential for sub-lethal predators of stony corals (corallivores) to mediate coral microbiome assembly. We quantified communities of microorganisms—dinoflagellate symbionts in the family Symbiodiniaceae and bacteria—in feces from 7 fish species (ranging from ‘somewhat corallivorous’ to ‘exclusively corallivorous’), as well as corals, sediments, seawater, and algae from 2 reef zones in Mo’orea (French Polynesia, South Pacific) over 3 years.
Results/Conclusions
Coral predator feces generally contained high abundances of beneficial coral symbionts, including viable Symbiodiniaceae cells in the genus Cladocopium and Endozoicomonas bacteria. We also quantified the diversity of Symbiodiniaceae and bacteria in the feces of three grazer/detritivorous (i.e., ‘no corallivory’) fish species. Feces of these consumers had lower live Symbiodiniaceae cell densities, and were dominated by bacterial taxa associated with coral disease (e.g., Vibrio spp.). Tank-based experiments showed that feces from grazer/detritivores caused distinct shifts in coral microbiomes, compared to feces from corallivores, indicating the feces of consumers have species-specific effects on coral microbiome assembly. Our field collections spanned a mass bleaching event in which the alpha and beta diversity of microbial communities dispersed by reef fish shifted. During the bleaching event, corallivore feces contained a lower diversity of Symbiodiniaceae, as well as increased relative abundances of the genus Durusdinium; some members of Durusdinium are associated with increased thermal tolerance in corals, suggesting that corallivores aid the dispersal of symbionts that may help coral reefs recover from bleaching. Together, these findings demonstrate that corallivorous fish feces are environmental hotspots of beneficial Symbiodiniaceae and bacteria that support coral success and resilience, and open a new line of inquiry into the contexts in which reef fish consumers influence coral microbiome assembly. Most importantly, these findings challenge our understanding of species interactions that have classically been thought of as wholly antagonistic: herbivory and sub-lethal predation may have some positive effects on populations of foundation species through the dispersal of beneficial microorganisms.