Biodiversity of macroalgae does not differentially suppress coral performance: The other side of a biodiversity issue.

Hundreds of studies now document positive relationships between biodiversity and critical ecosystem processes, but as ecological communities worldwide shift toward new species configurations, less is known regarding how the biodiversity of undesirable species will shape the functioning of ecosystems or foundation species. We manipulated macroalgal species richness in experimental field plots to test whether and how the identity and diversity of competing macroalgae affected the growth, survival, and microbiome of a common coral in Mo'orea, French Polynesia. Compared to controls without algal competitors, coral growth was significantly suppressed across three macroalgal monocultures, a polyculture of the same three macroalgae, and plots containing inert seaweed mimics; coral mortality was limited and did not differ significantly among treatments. One macroalga suppressed coral growth significantly less than the other two, but none differed from the inert mimic in terms of coral suppression. The composition, dispersion, and diversity of coral microbiomes in treatments with live macroalgae or inert plastic mimics did not differ from controls experiencing no competition. Microbiome composition differed between two macroalgal monocultures and a monoculture versus plastic mimics, but no other microbiome differences were observed among macroalgal or mimic treatments. Together, these findings suggest that algal diversity does not alter harmful impacts of macroalgae on coral performance, which could be accounted for by physical structure alone in these field experiments. While enhancing biodiversity is a recognized strategy for promoting desirable species, it would be worrisome if biodiversity also enhanced the negative impacts of undesirable species. We documented no such effects in this investigation.

Removal of detritivore sea cucumbers from reefs increases coral disease.

Coral reefs are in global decline with coral diseases playing a significant role. This is especially true for Acroporid corals that represent ~25% of all Pacific coral species and generate much of the topographic complexity supporting reef biodiversity. Coral diseases are commonly sediment-associated and could be exacerbated by overharvest of sea cucumber detritivores that clean reef sediments and may suppress microbial pathogens as they feed. Here we show, via field manipulations in both French Polynesia and Palmyra Atoll, that historically overharvested sea cucumbers strongly suppress disease among corals in contact with benthic sediments. Sea cucumber removal increased tissue mortality of Acropora pulchra by ~370% and colony mortality by ~1500%. Additionally, farmerfish that kill Acropora pulchra bases to culture their algal gardens further suppress disease by separating corals from contact with the disease-causing sediment-functioning as mutualists rather than parasites despite killing coral bases. Historic overharvesting of sea cucumbers increases coral disease and threatens the persistence of tropical reefs. Enhancing sea cucumbers may enhance reef resilience by suppressing disease.

Biodiversity has a positive but saturating effect on imperiled coral reefs.

Species loss threatens ecosystems worldwide, but the ecological processes and thresholds that underpin positive biodiversity effects among critically important foundation species, such as corals on tropical reefs, remain inadequately understood. In field experiments, we manipulated coral species richness and intraspecific density to test whether, and how, biodiversity affects coral productivity and survival. Corals performed better in mixed species assemblages. Improved performance was unexplained by competition theory alone, suggesting that positive effects exceeded agonistic interactions during our experiments. Peak coral performance occurred at intermediate species richness and declined thereafter. Positive effects of coral diversity suggest that species' losses on degraded reefs make recovery more difficult and further decline more likely. Harnessing these positive interactions may improve ecosystem conservation and restoration in a changing ocean.

Thermal Stress Interacts With Surgeonfish Feces to Increase Coral Susceptibility to Dysbiosis and Reduce Tissue Regeneration.

Dysbiosis of coral microbiomes results from various biotic and environmental stressors, including interactions with important reef fishes which may act as vectors of opportunistic microbes via deposition of fecal material. Additionally, elevated sea surface temperatures have direct effects on coral microbiomes by promoting growth and virulence of opportunists and putative pathogens, thereby altering host immunity and health. However, interactions between these biotic and abiotic factors have yet to be evaluated. Here, we used a factorial experiment to investigate the combined effects of fecal pellet deposition by the widely distributed surgeonfish Ctenochaetus striatus and elevated sea surface temperatures on microbiomes associated with the reef-building coral Porites lobata. Our results showed that regardless of temperature, exposure of P. lobata to C. striatus feces increased alpha diversity, dispersion, and lead to a shift in microbial community composition - all indicative of microbial dysbiosis. Although elevated temperature did not result in significant changes in alpha and beta diversity, we noted an increasing number of differentially abundant taxa in corals exposed to both feces and thermal stress within the first 48h of the experiment. These included opportunistic microbial lineages and taxa closely related to potential coral pathogens (i.e., Vibrio vulnificus, Photobacterium rosenbergii). Some of these taxa were absent in controls but present in surgeonfish feces under both temperature regimes, suggesting mechanisms of microbial transmission and/or enrichment from fish feces to corals. Importantly, the impact to coral microbiomes by fish feces under higher temperatures appeared to inhibit wound healing in corals, as percentages of tissue recovery at the site of feces deposition were lower at 30°C compared to 26°C. Lower percentages of tissue recovery were associated with greater relative abundance of several bacterial lineages, with some of them found in surgeonfish feces (i.e., Rhodobacteraceae, Bdellovibrionaceae, Crocinitomicaceae). Our findings suggest that fish feces interact with elevated sea surface temperatures to favor microbial opportunism and enhance dysbiosis susceptibility in P. lobata. As the frequency and duration of thermal stress related events increase, the ability of coral microbiomes to recover from biotic stressors such as deposition of fish feces may be greatly affected, ultimately compromising coral health and resilience.

Seaweed-coral competition in the field: effects on coral growth, photosynthesis and microbiomes require direct contact.

A number of tropical reefs have transitioned from coral to macroalgal dominance, but the role of macroalgal competition in coral decline is debated. There is a need to understand the relative roles of direct coral-algal effects versus indirect, microbially mediated effects shaping these interactions, as well as the relevant scales at which interactions operate under natural field, as opposed to laboratory, conditions. We conducted a manipulative field experiment investigating how direct contact versus close proximity (approx. 1.5 cm) with macroalgae (Galaxaura rugosa, Sargassum polycystum) impacted the growth, photosynthetic efficiency, and prokaryotic microbiome of the common Indo-Pacific coral Acropora millepora. Both coral growth and photosynthetic efficiency were suppressed when in direct contact with algae or their inert mimics--but not when in close proximity to corals without direct contact. Coral microbiomes were largely unaltered in composition, variability, or diversity regardless of treatment, although a few uncommon taxa differed in abundance among treatments. Negative impacts of macroalgae were contact dependent, accounted for by physical structure alone and had minimal effects on coral microbiomes. The spatial constraints of these interactions have important implications for understanding and predicting benthic community dynamics as reefs degrade.

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

BACKGROUND: Impacts of biotic stressors, such as consumers, on coral microbiomes have gained attention as corals decline worldwide. Corallivore feeding can alter coral microbiomes in ways that contribute to dysbiosis, but feeding strategies are diverse - complicating generalizations about the nature of consumer impacts on coral microbiomes. RESULTS: In field experiments, feeding by Coralliophila violacea, a parasitic snail that suppresses coral growth, altered the microbiome of its host, Porites cylindrica, but these impacts were spatially constrained. Alterations in microbial community composition and variability were largely restricted to snail feeding scars; basal or distal areas ~ 1.5 cm or 6-8 cm away, respectively, were largely unaltered. Feeding scars were enriched in taxa common to stressed corals (e.g. Flavobacteriaceae, Rhodobacteraceae) and depauperate in putative beneficial symbionts (e.g. Endozoicomonadaceae) compared to locations that lacked feeding. CONCLUSIONS: Previous studies that assessed consumer impacts on coral microbiomes suggested that feeding disrupts microbial communities, potentially leading to dysbiosis, but those studies involved mobile corallivores that move across and among numerous individual hosts. Sedentary parasites like C. violacea that spend long intervals with individual hosts and are dependent on hosts for food and shelter may minimize damage to host microbiomes to assure continued host health and thus exploitation. More mobile consumers that forage across numerous hosts should not experience these constraints. Thus, stability or disruption of microbiomes on attacked corals may vary based on the foraging strategy of coral consumers.

Parrotfish predation drives distinct microbial communities in reef-building corals.

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.

Variable effects of local management on coral defenses against a thermally regulated bleaching pathogen.

Bleaching and disease are decimating coral reefs especially when warming promotes bleaching pathogens, such as Vibrio coralliilyticus. We demonstrate that sterilized washes from three common corals suppress V. coralliilyticus but that this defense is compromised when assays are run at higher temperatures. For a coral within the ecologically critical genus Acropora, inhibition was 75 to 154% greater among colonies from coral-dominated marine protected areas versus adjacent fished areas that were macroalgae-dominated. Acropora microbiomes were more variable within fished areas, suggesting that reef degradation may also perturb coral microbial communities. Defenses of a robust poritid coral and a weedy pocilloporid coral were not affected by reef degradation, and microbiomes were unaltered for these species. For some ecologically critical, but bleaching-susceptible, corals such as Acropora, local management to improve reef state may bolster coral resistance to global change, such as bacteria-induced coral bleaching during warming events.

Biodiversity enhances coral growth, tissue survivorship and suppression of macroalgae.

Coral reefs are declining dramatically and losing species richness, but the impact of declining biodiversity on coral well-being remains inadequately understood. Here, we demonstrate that lower coral species richness alone can suppress the growth and survivorship of multiple species of corals (Porites cylindrica, Pocillopora damicornis and Acropora millepora) under field conditions on a degraded, macroalgae-dominated reef. Our findings highlight the positive role of biodiversity in the function of coral reefs, and suggest that the loss of coral species richness may trigger negative feedback that causes further ecosystem decline.

Spatial and temporal limits of coral-macroalgal competition: the negative impacts of macroalgal density, proximity, and history of contact.

Tropical reefs are commonly transitioning from coral- to macroalgal-dominance, producing abrupt, and often lasting, shifts in community composition and ecosystem function. Although negative effects of macroalgae on corals are well documented, whether such effects vary with spatial scale or the density of macroalgae remains inadequately understood, as does the legacy of their impact on coral growth. Using closely adjacent coral- versus macroalgal-dominated areas, we tested effects of macroalgal competition on the Indo-Pacific corals Acropora millepora and Porites cylindrica. When corals were transplanted to areas of: i) macroalgal-dominance, ii) macroalgal-dominance but with nearby macroalgae removed, or iii) coral-dominance lacking macroalgae, coral growth was equivalently high in plots without macroalgae and low (62-90% less) in plots with macroalgae, regardless of location. In a separate experiment, we raised corals above the benthos in each area and exposed them to differing densities of the dominant macroalga Sargassum polycystum. Coral survivorship was high (≥ 93% after 3 months) and did not differ among treatments, whereas the growth of both coral species decreased as a function of Sargassum density. When Sargassum was removed after two months, there was no legacy effect of macroalgal density on coral growth over the next seven months; however, there was no compensation for previously depressed growth. In sum, macroalgal impacts were density dependent, occurred only if macroalgae were in close contact, and coral growth was resilient to prior macroalgal contact. The temporal and spatial constraints of these interactions suggest that corals may be surprisingly resilient to periodic macroalgal competition, which could have important implications for ecosystem trajectories that lead to reef decline or recovery.

Intergenerational effects of macroalgae on a reef coral: major declines in larval survival but subtle changes in microbiomes.

Tropical reefs are shifting from coral to macroalgal dominance, with macroalgae suppressing coral recovery, potentially via effects on coral microbiomes. Understanding how macroalgae affect corals and their microbiomes requires comparing algae- versus coral-dominated reefs without confounding aspects of time and geography. We compared survival, settlement, and post-settlement survival of larvae, as well as the microbiomes of larvae and adults, of the Pacific coral Pocillopora damicornis between an Marine Protected Area (MPA) dominated by corals versus an adjacent fished area dominated by macroalgae. Microbiome composition in adult coral, larval coral, and seawater did not differ between the MPA and fished area. However, microbiomes of adult coral were more variable in the fished area and Vibrionaceae bacteria, including strains most closely related to the pathogen Vibrio shilonii, were significantly enriched, but rare, in adult and larval coral from the fished area. Larvae from the macroalgae-dominated area exhibited higher pre-settlement mortality and reduced settlement compared to those from the coral-dominated area. Juveniles planted into a coral-dominated area survived better than those placed into a fished area dominated by macroalgae. Differential survival depended on whether macroalgae were immediately adjacent to juvenile coral rather than on traits of the areas per se. Contrary to our expectations, coral microbiomes were relatively uniform at the community level despite dramatic differences in macroalgal cover between the MPA (~2% cover) and fished (~90%) area. Reducing macroalgae may elicit declines in rare but potentially harmful microbes in coral and their larvae, as well as positive intergenerational effects on offspring survival.

Overlooked coral predators suppress foundation species as reefs degrade.

Loss of larger consumers from stressed ecosystems can lead to trophic release of mid-level consumers that then impact foundation species, suppressing ecosystem function and resilience. For example, in coral reef ecosystems, outbreaks of coral predators like crown-of-thorns sea stars have been associated with fishing pressure and can dramatically impact the composition and persistence of corals. However, the ecological impacts, and consequences for management, of smaller, less obvious corallivores remain inadequately understood. We investigated whether reef state (coral vs. seaweed domination) influenced densities and size frequencies of the corallivorous gastropod Coralliophila violacea on its common host, the coral Porites cylindrica, within three pairs of small Marine Protected Areas (MPAs) and adjacent fished areas in Fiji. C. violacea densities were 5-35 times greater, and their size frequencies more broadly distributed, within seaweed-dominated fished areas than in adjacent MPAs dominated by corals. Tethering snails (4-9 mm in shell height) in place on their coral hosts indicated that suppression of snails in MPAs was due to predation, apparently by fishes. When tethered on the benthos (where they rarely occur), rather than on their host, mortality of larger snails (15.0-25.0 mm in shell height) was high in all areas, primarily due to hermit crabs killing them and occupying their shells. Because C. violacea is a sessile gastropod that feeds affixed to the base of corals and produces minimal visible damage, it has been considered a "prudent feeder" that minimally impacts its host coral. We assessed this over a 24-d feeding period in the field. Feeding by individual C. violacea reduced P. cylindrica growth by ~18-43% depending on snail size. Our findings highlight the considerable, but underappreciated, negative impacts of this common corallivore on degraded reefs. As reefs degrade and corals are lost, remaining corals (often species of Porites) may gain the full attention of elevated densities of coral consumers. This will further damage the remaining foundation species, suppressing the resilience of corals and enhancing the resilience of degraded, seaweed-dominated reefs.

Size matters: Predator outbreaks threaten foundation species in small Marine Protected Areas.

The unanticipated impacts of consumers in fragmented habitats are frequently a challenge for ecosystem management. On Indo-Pacific coral reefs, crown-of-thorns sea stars (Acanthaster spp.) are coral predators whose outbreaks cause precipitous coral decline. Across large spatial scales, Acanthaster densities are lower in large no-take Marine Protected Areas (MPAs) and reefs subject to limited human exploitation. However, using a combination of observational and manipulative experiments, we found that Acanthaster densities within a network of small, no-take MPAs on reef flats in Fiji were ~2-3.4 times greater inside MPAs than in adjacent fished areas and ~2-2.5 times greater than the upper threshold density indicative of an outbreak. This appeared to result from selective Acanthaster migration to the coral-rich MPAs from fished areas that are coral-poor and dominated by macroalgae. Small MPAs can dramatically increase the cover of foundation species like corals, but may selectively attract coral predators like Acanthaster due to greater food densities within MPAs or because the MPAs are too small to support Acanthaster enemies. As coral cover increases, their chemical and visual cues may concentrate Acanthaster to outbreak densities that cause coral demise, compromising the value of small MPAs. An understanding of predator dynamics as a function of habitat type, size, and fragmentation needs to be incorporated into MPA design and management.

Competitors as accomplices: seaweed competitors hide corals from predatory sea stars.

Indirect biotic effects arising from multispecies interactions can alter the structure and function of ecological communities--often in surprising ways that can vary in direction and magnitude. On Pacific coral reefs, predation by the crown-of-thorns sea star, Acanthaster planci, is associated with broad-scale losses of coral cover and increases of macroalgal cover. Macroalgal blooms increase coral-macroalgal competition and can generate further coral decline. However, using a combination of manipulative field experiments and observations, we demonstrate that macroalgae, such as Sargassum polycystum, produce associational refuges for corals and dramatically reduce their consumption by Acanthaster. Thus, as Acanthaster densities increase, macroalgae can become coral mutualists, despite being competitors that significantly suppress coral growth. Field feeding experiments revealed that the protective effects of macroalgae were strong enough to cause Acanthaster to consume low-preference corals instead of high-preference corals surrounded by macroalgae. This highlights the context-dependent nature of coral-algal interactions when consumers are common. Macroalgal creation of associational refuges from Acanthaster predation may have important implications for the structure,function and resilience of reef communities subject to an increasing number of biotic disturbances.