Abstract

BackgroundCoral-associated microbial communities are sensitive to multiple environmental and biotic stressors that can lead to dysbiosis and mortality. Although the processes contributing to these microbial shifts remain inadequately understood, a number of potential mechanisms have been identified. For example, predation by various corallivore species, including ecologically-important taxa such as parrotfishes, may disrupt coral microbiomes via bite-induced transmission and/or enrichment of potentially opportunistic bacteria. Here, we used a combination of mesocosm experiments and field-based observations to investigate whether parrotfish corallivory can alter coral microbial assemblages directly and to identify the potentially relevant pathways (e.g. direct transmission) that may contribute to these changes.ResultsOur mesocosm experiment demonstrated that predation by the parrotfish Chlorurus spilurus on Porites lobata corals resulted in a 2-4x increase in bacterial alpha diversity of the coral microbiome and a shift in bacterial community composition after 48 h. These changes corresponded with greater abundance of both potentially beneficial (i.e. Oceanospirillum) and opportunistic bacteria (i.e. Flammeovirgaceae, Rhodobacteraceae) in predated compared to mechanically wounded corals. Importantly, many of these taxa were detectable in C. spilurus mouths, but not in corals prior to predation. When we sampled bitten and unbitten corals in the field, corals bitten by parrotfishes exhibited 3x greater microbial richness and a shift in community composition towards greater abundance of both potential beneficial symbionts (i.e. Ruegeria) and bacterial opportunists (i.e. Rhodospiralles, Glaciecola). Moreover, we observed 4x greater community variability in naturally bitten vs. unbitten corals, a potential indicator of dysbiosis. Interestingly, some of the microbial taxa detected in naturally bitten corals, but not unbitten colonies, were also detected in parrotfish mouths.ConclusionsOur findings suggest that parrotfish corallivory may represent an unrecognized route of bacterial transmission and/or enrichment of rare and distinct bacterial taxa, both of which could impact coral microbiomes and health. More broadly, we highlight how underappreciated pathways, such as corallivory, may contribute to dysbiosis within reef corals, which will be critical for understanding and predicting coral disease dynamics as reefs further degrade.

Highlights

  • Coral-associated microbial communities are sensitive to multiple environmental and biotic stressors that can lead to dysbiosis and mortality

  • Experimental overview The impacts of parrotfish corallivory on coral microbiomes were assessed using a combination of manipulative experiments and field surveys on the north shore of Mo’orea, French Polynesia

  • To assess the ability of C. spilurus to feed on live Porites lobata corals, we conducted a survey in two back reef areas to quantify the number of C. spilurus bites found on live versus dead corals

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Summary

Introduction

Coral-associated microbial communities are sensitive to multiple environmental and biotic stressors that can lead to dysbiosis and mortality. An array of mutualistic benefits are suggested, encompassing vital functions such as coral nutrition and immunity that may further impact fundamental ecological processes within coral reefs [4, 6, 7]. Despite their beneficial role in host fitness, coralassociated bacteria are sensitive to numerous environmental and biotic stressors that may lead to microbial dysbiosis (i.e., a shift in either the mean composition or variability of the microbiome, including the loss of beneficial symbionts and/or increase of opportunists) [8, 9]. Trophic interactions that are common within reef ecosystems, such predation on corals (i.e. corallivory), may favor the disruption of coral microbiomes and subsequently alter coral health [6, 8, 9, 13]

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