Symbiodiniaceae cell densities in feces of coral reef fish, sediments and seawater in Mo'orea, French Polynesia, July-August 2019

Background: The 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. Results: Obligate 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. Conclusions: Taken 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.