Fish predation on corals promotes the dispersal of coral symbionts

Abstract

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.

Reef environments shape microbial partners in a highly connected coral population

“…Symbiodiniaceae type profiles were largely made up of C3 variants (Cladocopium genus) along with a few corals hosting A1 and A3 (Symbiodinium genus) (figure 2d-f; electronic supplementary material, figure S7), consistent with compositions found by Putnam et al [57]. Interestingly, Howe-Kerr et al [58] found higher frequencies of Symbiodinium and Durusdinium genera than Cladocopium in their 2019 collections, despite their sampling from adjacent reefs in Mo'orea. This may reflect a shift in A. hyacinthus Symbiodiniaceae communities due to climate change stressors, given that collections from Putnam et al [57] and our study occurred prior to 2014 and a devastating bleaching event occurred in Mo'orea in 2019.…”

Symbiotic Algae of Hydra viridissima Play a Key Role in Maintaining Homeostatic Bacterial Colonization

“…This is of relevance because interhost dispersal of bacteria is not a rare phenomenon. Transmission of microbes from one individual to another one in a shared environment has been documented previously for aquatic systems, as exemplified in corals ( Grupstra et al, 2021 ), zebrafish ( Burns et al, 2017 ), microcosm ( Shen et al, 2018 ), and zooplankton ( Grossart et al, 2010 ). Moreover, co-housing of mice has a profound effect on their gut microbiome ( Caruso et al, 2019 ; Robertson et al, 2019 ).…”

Algae from Aiptasia egesta are robust representations of Symbiodiniaceae in the free-living state

“…The authors noted that egesta released by H. crispa were consumed by symbiotic anemonefish ( Alan Verde, Cleveland & Lee, 2015 ). It is not known if other animals consume Aiptasia egesta in nature, but if so, they may aid in algal dispersal, as algae often survive digestion ( Parker, 1984 ; Grupstra et al, 2021 ; Grupstra et al, 2022 ).…”