Parrotfish Predation Drives Distinct Microbial Communities in Reef-Building Corals Leïla Ezzat1* , Thomas Lamy1, Rebecca L
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Ezzat et al. Animal Microbiome (2020) 2:5 Animal Microbiome https://doi.org/10.1186/s42523-020-0024-0 RESEARCH ARTICLE Open Access Parrotfish predation drives distinct microbial communities in reef-building corals Leïla Ezzat1* , Thomas Lamy1, Rebecca L. Maher2, Katrina S. Munsterman1, Kaitlyn M. Landfield1, Emily R. Schmeltzer2, Cody S. Clements3, Rebecca L. Vega Thurber2 and Deron E. Burkepile1,4 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. Keywords: Parrotfish, Coral reefs, 16S rRNA gene, Corallivory, Bacteria, Corals, Vector, Transmission, Microbiomes * Correspondence: [email protected] 1Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, CA, USA Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Ezzat et al. Animal Microbiome (2020) 2:5 Page 2 of 15 Background nutrient pollution experienced significantly greater mor- Reef-building corals host a wide range of microorgan- tality than when exposed to either stressor alone, which isms including endosymbiotic dinoflagellates (Symbiodi- was attributed to increased bacterial opportunism [13]. naceae), viruses, archaea, and bacteria that collectively Identifying the mechanisms and conditions in which comprise the coral holobiont [1]. The relationship be- parrotfishes can disrupt coral microbiomes will improve tween corals and these microbial associates allows reef our ability to predict the microbial impacts associated corals to thrive in nutrient-poor waters and to support with corallivory and their potential implications for coral high biodiversity [2]. While the coral-dinoflagellate sym- health. biosis is well documented, less is known about the roles Here, we conducted a series of experiments in of coral-associated bacterial communities in coral health Mo’orea, French Polynesia, to assess the effects of and resilience [3–5]. However, an array of mutualistic parrotfish corallivory on coral microbiomes. Specifically, benefits are suggested, encompassing vital functions we tested whether parrotfish can facilitate the enrich- such as coral nutrition and immunity that may further ment and/or transmission of microbes to corals. We fo- impact fundamental ecological processes within coral cused on Chlorurus spilurus, a common parrotfish reefs [4, 6, 7]. species known to prey on large colonies of Porites on Pa- Despite their beneficial role in host fitness, coral- cific reefs [21]. We first performed a controlled meso- associated bacteria are sensitive to numerous environ- cosm experiment comparing the microbiomes of Porites mental and biotic stressors that may lead to microbial lobata colonies that were either mechanically wounded dysbiosis (i.e., a shift in either the mean composition or or predated by C. spilurus parrotfish. Comparisons were variability of the microbiome, including the loss of bene- based on samples collected immediately following preda- ficial symbionts and/or increase of opportunists) [8, 9]. tion or wounding (Ti) and at 48 h (Tf). To examine However, the processes that contribute to dysbiosis re- microbiome patterns in situ, we collected microbial sam- main inadequately understood [8, 10–12]. For example, ples from corals in the field that had either been natur- trophic interactions that are common within reef ecosys- ally bitten by parrotfishes or appeared bite free tems, such predation on corals (i.e. corallivory), may (hereafter “unbitten”). Coral microbiomes from both the favor the disruption of coral microbiomes and subse- mesocosm experiment and field survey were also com- quently alter coral health [6, 8, 9, 13]. pared to microbiomes from parrotfish mouthparts to as- A variety of corallivores, including invertebrates such sess potential predation-mediated pathways (e.g. as fireworms [14], echinoderms [15], and gastropods [16, transmission) that may contribute to coral microbiome 17], may serve as reservoirs and/or vectors of opportun- change. We hypothesized that predation by C. spilurus istic bacteria (i.e. typically non-pathogenic microorgan- facilitates the enrichment and/or transmission of mi- isms that take advantage of their host under certain crobes to corals, resulting in the following impacts on circumstances) or pathogens (i.e. microorganisms that the coral microbiome: (1) increases in alpha diversity, (2) cause infection) to corals. Corallivorous, polyp-feeding differences in community composition (3) increases in butterflyfishes may also spread microbes and parasites community variability, and (4) increased abundance of via their mouthparts [14–18]. However, the fact that microbial taxa typically found in the mouths of parrot- butterflyfishes remove limited coral tissue without ex- fish but absent in healthy corals. posing the underlying skeleton may make them unlikely candidates to transmit microbes among individual corals Results [16]. In contrast, many parrotfishes scrape or excavate Experimental overview both live coral tissue and skeleton, while also ingesting The impacts of parrotfish corallivory on coral micro- detritus and turf algae from rocky surfaces [19]. This in- biomes were assessed using a combination of manipula- vasive feeding method and more varied diet make them tive experiments and field surveys on the north shore of likely candidates for disrupting coral microbiomes. Par- Mo’orea, French Polynesia. First, to assess the ability of rotfishes play a critical role in structuring the benthic C. spilurus to feed on live Porites lobata corals, we con- communities of coral reefs and are generally considered ducted a survey in two back reef areas to quantify the to have a net positive effect on ecosystem functions, pro- number of C. spilurus bites found on live versus dead moting coral dominance by removing competing macro- corals. A manipulative experiment was then performed algae [19] and acting as important agents of reef at the UC Gump Marine station with seven C. spilurus bioerosion [20]. That said, parrotfish predation is a initial phase individuals and ten colonies of Porites chronic stress that may cause significant harm to corals, lobata (about 20 cm) that were previously collected on a especially when coupled with other environmental and/ nearby back reef. When at the station, sterile culture or biotic stressors. For example, recent findings suggest swabs were used to collect microbial samples of the that corals exposed to both parrotfish predation and mouths of each C. spilurus individual. Each C. spilurus Ezzat et al. Animal Microbiome (2020)