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Abstract Microbiomes are essential features of holobionts, providing their hosts with key metabolic and functional traits like resistance to environmental disturbances and diseases. In scleractinian corals, questions remain about the microbiome's role in resistance and resilience to factors contributing to the ongoing global coral decline and whether microbes serve as a form of holobiont ecological memory. To test if and how coral microbiomes affect host health outcomes during repeated disturbances, we conducted a large‐scale (32 exclosures, 200 colonies, and 3 coral species sampled) and long‐term (28 months, 2018–2020) manipulative experiment on the forereef of Mo'orea, French Polynesia. In 2019 and 2020, this reef experienced the two most severe marine heatwaves on record for the site. Our experiment and these events afforded us the opportunity to test microbiome dynamics and roles in the context of coral bleaching and mortality resulting from these successive and severe heatwaves. We report unique microbiome responses to repeated heatwaves inAcropora retusa,Porites lobata, andPocilloporaspp., which included: microbiome acclimatization inA. retusa, and both microbiome resilience to the first marine heatwave and microbiome resistance to the second marine heatwave inPocilloporaspp. Moreover, observed microbiome dynamics significantly correlated with coral species‐specific phenotypes. For example, bleaching and mortality inA. retusaboth significantly increased with greater microbiome beta dispersion and greater Shannon Diversity, whileP. lobatacolonies had different microbiomes across mortality prevalence. Compositional microbiome changes, such as changes to proportions of differentially abundant putatively beneficial to putatively detrimental taxa to coral health outcomes during repeated heat stress, also correlated with host mortality, with higher proportions of detrimental taxa yielding higher mortality inA. retusa. This study reveals evidence for coral species‐specific microbial responses to repeated heatwaves and, importantly, suggests that host‐dependent microbiome dynamics may provide a form of holobiont ecological memory to repeated heat stress. 

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.