Abstract
BackgroundThe microbiomes of foundation (habitat-forming) species such as corals and sponges underpin the biodiversity, productivity, and stability of ecosystems. Consumers shape communities of foundation species through trophic interactions, but the role of consumers in dispersing the microbiomes of such species is rarely examined. For example, stony corals rely on a nutritional symbiosis with single-celled endosymbiotic dinoflagellates (family Symbiodiniaceae) to construct reefs. Most corals acquire Symbiodiniaceae from the environment, but the processes that make Symbiodiniaceae available for uptake are not resolved. Here, we provide the first comprehensive, reef-scale demonstration that predation by diverse coral-eating (corallivorous) fish species promotes the dispersal of Symbiodiniaceae, based on symbiont cell densities and community compositions from the feces of four obligate corallivores, three facultative corallivores, two grazer/detritivores as well as samples of reef sediment and water.ResultsObligate corallivore feces are environmental hotspots of Symbiodiniaceae cells: live symbiont cell concentrations in such feces are 5–7 orders of magnitude higher than sediment and water environmental reservoirs. Symbiodiniaceae community compositions in the feces of obligate corallivores are similar to those in two locally abundant coral genera (Pocillopora and Porites), but differ from Symbiodiniaceae communities in the feces of facultative corallivores and grazer/detritivores as well as sediment and water. Combining our data on live Symbiodiniaceae cell densities in feces with in situ observations of fish, we estimate that some obligate corallivorous fish species release over 100 million Symbiodiniaceae cells per 100 m2 of reef per day. Released corallivore feces came in direct contact with coral colonies in the fore reef zone following 91% of observed egestion events, providing a potential mechanism for the transfer of live Symbiodiniaceae cells among coral colonies.ConclusionsTaken together, our findings show that fish predation on corals may support the maintenance of coral cover on reefs in an unexpected way: through the dispersal of beneficial coral symbionts in corallivore feces. Few studies examine the processes that make symbionts available to foundation species, or how environmental reservoirs of such symbionts are replenished. This work sets the stage for parallel studies of consumer-mediated microbiome dispersal and assembly in other sessile, habitat-forming species.
Highlights
Most animals and plants studied to date host resident communities of microorganisms— microbiomes—that influence their health and survival [7, 38]
Corallivores that feed on corals without killing them may mediate the dispersal of coral microbiomes by egesting Symbiodiniaceae—and other members of the coral microbiome—in their feces as they move across reefs [43, 59]
These results provide a first indication that facultative corallivores contribute to the dispersal of some coral-associated Symbiodiniaceae genera, at cell concentrations at least comparable to sediments
Summary
Most animals and plants studied to date host resident communities of microorganisms— microbiomes—that influence their health and survival [7, 38]. Cladocopium and Durusdinium, the two other genera commonly detected in Caribbean corals, were not observed in S. viride feces [14] These results provide a first indication that facultative corallivores contribute to the dispersal of some coral-associated Symbiodiniaceae genera, at cell concentrations at least comparable to sediments. We conducted the first comprehensive, reef-scale quantification of fishmediated coral microbiome dispersal on a Pacific reef and found, surprisingly, that the feces of both obligate and facultative corallivorous fishes contain high densities of live Symbiodiniaceae cells. We provide the first comprehensive, reefscale demonstration that predation by diverse coral-eating (corallivorous) fish species promotes the dispersal of Symbiodiniaceae, based on symbiont cell densities and community compositions from the feces of four obligate corallivores, three facultative corallivores, two grazer/detritivores as well as samples of reef sediment and water
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