Parrotfish predation drives distinct microbial communities in reef-building corals

Abstract

Background: Coral-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.Results: Our 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. Conclusions: Our 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.

Coral Microbiomes Demonstrate Flexibility and Resilience Through a Reduction in Community Diversity Following a Thermal Stress Event

“…Interestingly, Endozoicomonas abundances in Porites did not significantly change over the thermal stress event (Figure 5D). Experiments and surveys on Porites lobata in Mo'orea have shown a similar community response under various stressors, including mechanical wounding, predation, corallivore feces deposition, and combinations of stressors (Ezzat et al, 2019a(Ezzat et al, , 2020. In these experiments, Hahellaceae (family of Endozoicomonas) was a dominant member of the coral microbiome but was generally not differentially abundant with stress.…”

Fish predation on corals promotes the dispersal of coral symbionts

“…Individuals of nine fish species, as well as corals, sediments, and seawater samples ( n = 6–14 per sample type or species, see Table S 1 ) were collected on scuba in July and August 2019 from two reef zones: the back reef (1–2 m depth) and fore reef (5–10 m depth), between LTER sites 1 and 2 of the Mo’orea Coral Reef (MCR) Long Term Ecological Research (LTER) site. We selected fish species that broadly differ in their level of corallivory based on published literature [ 18 , 24 , 57 , 65 ] as obligate corallivores (butterflyfishes Chaetodon lunulatus , Chaetodon ornatissimus, Chaetodon reticulatus, and the filefish Amanses scopas ), facultative corallivores (butterflyfishes Chaetodon citrinellus and Chaetodon pelewensis and the parrotfish Chlorurus spilurus ) and grazer/detritivores (surgeonfishes Ctenochaetus flavicauda and Ctenochaetus striatus ). We sampled three coral species ( Acropora hyacinthus , Pocillopora species complex [ 23 ], and Porites lobata species complex [ 20 , 21 ]) that are dominant reef builders in Mo’orea and that are members of genera frequently targeted by corallivores [ 13 , 50 ].…”

“…Cell densities reported in this study (all obligate corallivore and grazer/detritivore feces data and some data for facultative corallivore feces, sediments and seawater) represent live cell densities only, based on results from hemocytometry with the cell viability dye, trypan blue. Previously published cell densities for sediment and seawater [22,35], macroalgae [22], and facultative corallivore feces [14] may include both dead and live cells and were quantified using hemocytometry [14], a combination of flow-cytometry and hemocytometry [35], or quantitative PCR [22] We characterized Symbiodiniaceae densities and community compositions in the feces of four obligate corallivores (the butterflyfishes Chaetodon lunulatus, CHLU; Chaetodon ornatissimus, CHOR; Chaetodon reticulatus, CHRE; and the filefish Amanses scopas, AMSC) and three facultative corallivores (the butterflyfishes Chaetodon citrinellus, CHCI; and Chaetodon pelewensis, CHPE, and the parrotfish Chlorurus spilurus, CHSP) from a reefscape in Mo'orea, French Polynesia [16,18,57]. To test whether the feces of obligate corallivores constitute 'hotspots' of live Symbiodiniaceae and are proximate environmental sources of Symbiodiniaceae for prospective coral host colonies, we additionally characterized Symbiodiniaceae from reef-associated sediments and water as well as the feces of two grazer/detritivores (surgeonfishes Ctenochaetus flavicauda, CTFL; and Ctenochaetus striatus, CTST).…”

“…We characterized Symbiodiniaceae densities and community compositions in the feces of four obligate corallivores (the butterflyfishes Chaetodon lunulatus , CHLU; Chaetodon ornatissimus , CHOR; Chaetodon reticulatus , CHRE; and the filefish Amanses scopas , AMSC) and three facultative corallivores (the butterflyfishes Chaetodon citrinellus , CHCI; and Chaetodon pelewensis , CHPE, and the parrotfish Chlorurus spilurus , CHSP) from a reefscape in Mo’orea, French Polynesia [ 16 , 18 , 57 ]. To test whether the feces of obligate corallivores constitute ‘hotspots’ of live Symbiodiniaceae and are proximate environmental sources of Symbiodiniaceae for prospective coral host colonies, we additionally characterized Symbiodiniaceae from reef-associated sediments and water as well as the feces of two grazer/detritivores (surgeonfishes Ctenochaetus flavicauda , CTFL; and Ctenochaetus striatus , CTST).…”

Parasite-host ecology: the limited impacts of an intimate enemy on host microbiomes

“…Unlike other well-known, mobile corallivores (e.g. Acanthaster sea stars, parrotfishes, Drupella snails) that cause widespread coral damage and have been implicated in coral microbiome dysbiosis or as potential disease vectors [15][16][17][56][57][58][59][60], C. violacea is a corallivorous parasite known for its sessile mode of feeding that visually results in only minor, and localized, tissue damage. Our findings suggest that this feeding strategy also results in only localized impacts to the coral microbiome, which might be expected for a corallivore that shelters on, and exploits, its host for extended periods of time.…”