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1. Different nitrogen sources speed recovery from corallivory and uniquely alter the microbiome of a reef-building coral

   https://doi.org/10.7717/peerj.8056  

   Rice, Mallory M. ; Maher, Rebecca L. ; Vega Thurber, Rebecca ; Burkepile, Deron E. ( January 2019 , PeerJ)

   Corals are in decline worldwide due to local anthropogenic stressors, such as nutrient loading, and global stressors, such as ocean warming. Anthropogenic nutrient loading, which is often rich in nitrate, inhibits coral growth and worsens corals’ response to warming while natural sources of nitrogen, such as ammonium from fish excretion, promotes coral growth. Although the effects of nutrient loading and ocean warming have been well-studied, it remains unclear how these factors may interact with biotic processes, such as corallivory, to alter coral health and the coral microbiome. This study examined how nitrate vs. ammonium enrichment altered the effects of increased seawater temperature and simulated parrotfish corallivory on the health of Pocillopora meandrina and its microbial community. We tested the effects of nitrogen source on the response to corallivory under contrasting temperatures (control: 26 °C, warming: 29 °C) in a factorial mesocosm experiment in Moorea, French Polynesia. Corals were able to maintain growth rates despite simultaneous stressors. Seawater warming suppressed wound healing rates by nearly 66%. However, both ammonium and nitrate enrichment counteracted the effect of higher temperatures on would healing rates. Elevated seawater temperature and ammonium enrichment independently increased Symbiodiniaceae densities relative to controls, yet there was no effect of nitrate enrichment on algal symbiont densities. Microbiome variability increased with the addition of nitrate or ammonium. Moreover, microbial indicator analysis showed that Desulfovibrionaceae Operational taxonomic units (OTUs) are indicators of exclusively temperature stress while Rhodobacteraceae and Saprospiraceae OTUs were indicators of high temperature, wounding, and nitrogen enrichment. Overall, our results suggest that nitrogen source may not alter the response of the coral host to simultaneous stressors, but that the associated microbial community may be distinct depending on the source of enrichment. 

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2. Fish predation on corals promotes the dispersal of coral symbionts

   https://doi.org/10.1186/s42523-021-00086-4  

   Grupstra, Carsten G. ; Rabbitt, Kristen M. ; Howe-Kerr, Lauren I. ; Correa, Adrienne M. ( December 2021 , Animal Microbiome)

   null (Ed.)

   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 m 2 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. 

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3. The role of predators in coral disease dynamics

   https://doi.org/10.1007/s00338-022-02219-w  

   Renzi, Julianna J. ; Shaver, Elizabeth C. ; Burkepile, Deron E. ; Silliman, Brian R. ( April 2022 , Coral Reefs)

   Abstract Coral disease is becoming increasingly problematic on reefs worldwide. However, most coral disease research has focused on the abiotic drivers of disease, potentially overlooking the role of species interactions in disease dynamics. Coral predators in particular can influence disease by breaking through protective tissues and exposing corals to infections, vectoring diseases among corals, or serving as reservoirs for pathogens. Numerous studies have demonstrated the relationship between corallivores and disease in certain contexts, but to date there has been no comprehensive synthesis of the relationships between corallivores and disease, which hinders our understanding of coral disease dynamics. To address this void, we identified 65 studies from 26 different ecoregions that examine this predator–prey-disease relationship. Observational studies found over 20 positive correlations between disease prevalence and corallivore abundance, with just four instances documenting a negative correlation between corallivores and disease. Studies found putative pathogens in corallivore guts and experiments demonstrated the ability of corallivores to vector pathogens. Corallivores were also frequently found infesting disease margins or targeting diseased tissues, but the ecological ramifications of this behavior remains unknown. We found that the impact of corallivores was taxon-dependent, with most invertebrates increasing disease incidence, prevalence, or progression; fish showing highly context-dependent effects; and xanthid crabs decreasing disease progression. Simulated wounding caused disease in many cases, but experimental wound debridement slowed disease progression in others, which could explain contrasting findings from different taxa. The negative effects of corallivores are likely to worsen as storms intensify, macroalgal cover increases, more nutrients are added to marine systems, and water temperatures increase. As diseases continue to impact coral reefs globally, a more complete understanding of the ecological dynamics of disease—including those involving coral predators—is of paramount importance to coral reef conservation and management. 

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4. Extended phenotypes on coral reefs: cryptic phenotypes modulate coral‐vermetid interactions

   https://doi.org/10.1002/ecy.3215  

   Brown, A. L. ; Hamman, E. A. ; Shima, J. S. ; Wares, J. P. ; Osenberg, C. W. ( January 2021 , Ecology)

   Phenotypic variation can lead to variation in the strength and outcome of species interactions. Variation in phenotypic traits can arise due to plastic responses to environmental stimuli, underlying genetic variation, or both, and may reflect differences in the focal organism or aspects of the extended phenotype (e.g., associated microbes). We used a reciprocal transplant experiment ofPoritescorals to evaluate the role of plasticity vs. heritable diversity on phenotypic traits and performance of corals that varied in their prior exposure to vermetid gastropods, an organism known to reduce coral growth and survival. We measured a suite of phenotypic traits associated with coral performance, many of which showed a plastic response to vermetid exposure. Vermetids decreased calcification of corals, increased microbial diversity, and shifted microbial composition. Most traits also showed a signature of previous exposure environment that persisted even when exposure was reversed: i.e., under the same conditions, corals naïve to vermetids had slower calcification rates, thicker tissues, higher Symbiodiniaceae densities, and different microbiomes than corals previously exposed to vermetids. We suggest the phenotypic differences are heritable, as reefs with and without vermetids were comprised of two different mitotypes, that revealed high, consistent genetic variation. Vermetids were only found on the fast‐growing coral mitotype that was characterized by thin tissue, and that likely had a history of disturbance. As extended phenotypes can have community impacts, we suggest vermetid, in addition to microbes, are part of the extended community phenotype of these corals. Coral genotypes can establish different reef trajectories, with thin‐tissue types more prone to disturbance and subsequent colonization by other species, like vermetids, which can further facilitate the degradation of coral reefs. The effects of the extended phenotype of species likely influence heterogeneity across landscapes as well as temporal differences in community composition.

    

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5. Corallivory on small Porites colonies increases with coral colony size but is reduced by macroalgal associational refuge

   https://doi.org/10.1007/s00338-023-02424-1  

   Srednick, G. ; Edmunds, P. J. ( September 2023 , Coral Reefs)

   Numerous tropical macroalgae provide associational refuge to other benthic organisms, presumably due to their physical structure and/or production of chemical metabolites. One feature determining their effectiveness as an associational refuge is likely to be the size of the organism benefitting from the refuge. Using a manipulative experiment in the back reef of Moorea, French Polynesia, we tested if the macroalgaTurbinaria ornataprovided an associational refuge from fish corallivores for small colonies of massivePoritesspp., and how this differed with colony size (20–100 mm diameter). Tissue loss through corallivory increased with colony size but was ~ 72% less forPoritescolonies associated withT. ornataversus colonies separated from this macroalga, while dense macroalgae beds on contemporary reefs negatively impact the recruitment, growth and survival of corals, small colonies ofPoritesappear to benefit, through reduced corallivory, by associating with the macroalgaTurbinaria. This association may come at a cost (e.g., reduced growth) and should be the focus of future research.

    

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