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  1. Abstract

    Climate change-driven ocean warming is increasing the frequency and severity of bleaching events, in which corals appear whitened after losing their dinoflagellate endosymbionts (family Symbiodiniaceae). Viral infections of Symbiodiniaceae may contribute to some bleaching signs, but little empirical evidence exists to support this hypothesis. We present the first temporal analysis of a lineage of Symbiodiniaceae-infecting positive-sense single-stranded RNA viruses (“dinoRNAVs”) in coral colonies, which were exposed to a 5-day heat treatment (+2.1 °C). A total of 124 dinoRNAV major capsid protein gene “aminotypes” (unique amino acid sequences) were detected from five colonies of two closely related Pocillopora-Cladocopium (coral-symbiont) combinations in the experiment; most dinoRNAV aminotypes were shared between the two coral-symbiont combinations (64%) and among multiple colonies (82%). Throughout the experiment, seventeen dinoRNAV aminotypes were found only in heat-treated fragments, and 22 aminotypes were detected at higher relative abundances in heat-treated fragments. DinoRNAVs in fragments of some colonies exhibited higher alpha diversity and dispersion under heat stress. Together, these findings provide the first empirical evidence that exposure to high temperatures triggers some dinoRNAVs to switch from a persistent to a productive infection mode within heat-stressed corals. Over extended time frames, we hypothesize that cumulative dinoRNAV production in the Pocillopora-Cladocopium system could affect colony symbiotic status, for example, by decreasing Symbiodiniaceae densities within corals. This study sets the stage for reef-scale investigations of dinoRNAV dynamics during bleaching events.

     
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  2. Abstract

    Mass thermal bleaching events are a primary threat to coral reefs, yet the sublethal impacts, particularly on energetics and reproduction, are poorly characterized. Given that the persistence of coral populations is contingent upon the reproduction of individuals that survive disturbances, there is an urgent need to understand the sublethal effects of bleaching on reproductive output to accurately predict coral recovery rates. In 2019, the French Polynesian island of Mo’orea experienced a severe mass bleaching event accompanied by widespread coral mortality. At the most heavily impacted sites, we observedAcropora hyacinthusindividuals that were resistant to bleaching, alongside colonies that bleached but showed signs of symbiont recovery shortly after the bleaching event. We collected fragments fromA. hyacinthuscolonies five months post-bleaching and, using energetic assays and histological measurements, examined the physiological and reproductive consequences of these two distinct heat stress responses. Despite healthy appearances in both resistant and recovered corals, we found that recovered colonies had significantly reduced energy reserves compared to resistant colonies. In addition, we detected compound effects of stress on reproduction: recovered colonies displayed both a lower probability of containing gametes and lower fecundity per polyp. Our results indicate that bleaching inflicts an energetic constraint on the concurrent re-accumulation of energy reserves and development of reproductive material, with decreased reproductive potential of survivors possibly hampering overall reef resilience. These findings highlight the presence of intraspecific responses to bleaching and the importance of considering multiple trajectories for individual species when predicting population recovery following disturbance.

     
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  3. Abstract

    The relative importance of evolutionary history and ecology for traits that drive ecosystem processes is poorly understood. Consumers are essential drivers of nutrient cycling on coral reefs, and thus ecosystem productivity. We use nine consumer “chemical traits” associated with nutrient cycling, collected from 1,572 individual coral reef fishes (178 species spanning 41 families) in two biogeographic regions, the Caribbean and Polynesia, to quantify the relative importance of phylogenetic history and ecological context as drivers of chemical trait variation on coral reefs. We find: (1) phylogenetic relatedness is the best predictor of all chemical traits, substantially outweighing the importance of ecological factors thought to be key drivers of these traits, (2) phylogenetic conservatism in chemical traits is greater in the Caribbean than Polynesia, where our data suggests that ecological forces have a greater influence on chemical trait variation, and (3) differences in chemical traits between regions can be explained by differences in nutrient limitation associated with the geologic context of our study locations. Our study provides multiple lines of evidence that phylogeny is a critical determinant of contemporary nutrient dynamics on coral reefs. More broadly our findings highlight the utility of evolutionary history to improve prediction in ecosystem ecology.

     
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  4. Abstract

    For many long‐lived taxa, such as trees and corals, older, and larger individuals often have the lowest mortality and highest fecundity. However, climate change‐driven disturbances such as droughts and heatwaves may fundamentally alter typical size‐dependent patterns of mortality and reproduction in these important foundation taxa. Working in Moorea, French Polynesia, we investigated how a marine heatwave in 2019, one of the most intense marine heatwaves at our sites over the past 30 years, drove patterns of coral bleaching and mortality. The marine heatwave drove island‐wide mass coral bleaching that killed up to 76% and 65% of the largest individuals of the two dominant coral genera,PocilloporaandAcropora, respectively. Colonies ofPocilloporaandAcropora≥30 cm diameter were ~3.5× and ~1.3×, respectively, more likely to die than colonies <30‐cm diameter. Typically, annual mortality in these corals is concentrated on the smallest size classes. Yet, this heatwave dramatically reshaped this pattern, with heat stress disproportionately killing larger coral colonies and equalizing annual mortality rates across the size spectrum. This shift in the size‐mortality relationship reduced the overall fecundity of these genera by >60% because big corals are disproportionately important for reproduction on reefs. Additionally, the survivorship of microscopic coral recruits, critical for the recovery of corals following disturbances, declined to 2%, over an order of magnitude lower compared to a year without elevated thermal stress, where 33% of coral recruits survived. While other research has shown that larger corals can bleach more frequently than smaller corals, we show the severe impact this phenomenon can have at the reef‐wide scale. As marine heatwaves become more frequent and intense, disproportionate mortality of the largest, most fecund corals and near‐complete loss of entire cohorts of newly‐settled coral recruits will likely reduce the recovery capacity of these iconic ecosystems.

     
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  5. Abstract

    The supply of propagules mediates recruitment and population dynamics, thereby driving community resilience following disturbances. These relationships are of interest on tropical reefs, where coral populations have drastically declined in abundance and sexual recruitment is the only means by which they will recover. To better understand the causes and implications of variation in this vital rate (i.e., recruitment), coral recruitment was measured in Mo'orea, French Polynesia, and St. John, U.S. Virgin Islands, using settlement tiles deployed from 2005 to 2019. The results were used to test two hypotheses: (1) annual variation in recruitment is a weak predictor of long‐term variation in recruitment, but (2) it is associated with seawater temperature. Coral recruitment varied over space and time, so that differences in recruitment between consecutive years were uninformative of long‐term trends. Recruitment varied among years in an apparently chaotic manner, but the variation reflected linear and quadratic associations with mean annual temperature and the daily variation in temperature. These associations are consistent with theory addressing the mechanisms by which temperature affects coral larvae and recruitment. Comprehension of these mechanisms is required to accurately interpret evidence of coral recruitment collapse, and to elucidate the conditions favoring recovery of coral communities through recruitment.

     
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  6. Abstract

    Many coral reefs have shifted from coral‐ to macroalgae‐dominated community states, heightening the need to understand resilience of coral communities. Fishing on herbivores often reduces resilience of the coral state, as lower herbivory fosters macroalgal establishment. Despite the acknowledged importance of fishing, relatively little attention has been paid to how fishers change their behavior as macroalgae overgrow reefs, or how the resulting dynamic feedbacks might affect resilience. We address these questions in Moorea, French Polynesia, where local fishers target herbivorous fishes and where shifts to algal dominance have occurred on some lagoon reefs. We quantified fisher preferences for reef habitats where they target various taxa. For the two most ecologically important taxa of herbivores targeted in the fishery, parrotfish (Scaridae) and unicornfish (Naso), fishers preferred to harvest from locations with less macroalgae. We incorporated these habitat preferences into a spatially explicit social–ecological model of reef dynamics to explore consequences of changes in fishing behavior for resilience of the coral state, particularly following disturbance. Fishing that targets low‐macroalgae locations typically generates resilience by facilitating local recovery of herbivores and thus of coral in the less‐targeted macroalgae‐dominated patches. However, the resulting movement of fishers across the seascape can sometimes create fragility; if coral loss is widespread, avoidance of macroalgae concentrates fishing in patches having the highest coral cover, resulting in loss of coral via reduced herbivory. Our results emphasize that resilience and coral‐macroalgae regime shifts cannot be understood without considering humans as a dynamic part of the system.

     
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  7. Abstract

    Synchrony is broadly important to population and community dynamics due to its ubiquity and implications for extinction dynamics, system stability, and species diversity. Investigations of synchrony in community ecology have tended to focus on covariance in the abundances of multiple species in a single location. Yet, the importance of regional environmental variation and spatial processes in community dynamics suggests that community properties, such as species richness, could fluctuate synchronously across patches in a metacommunity, in an analog of population spatial synchrony. Here, we test the prevalence of this phenomenon and the conditions under which it may occur using theoretical simulations and empirical data from 20 marine and terrestrial metacommunities. Additionally, given the importance of biodiversity for stability of ecosystem function, we posit that spatial synchrony in species richness is strongly related to stability. Our findings show that metacommunities often exhibit spatial synchrony in species richness. We also found that richness synchrony can be driven by environmental stochasticity and dispersal, two mechanisms of population spatial synchrony. Richness synchrony also depended on community structure, including species evenness and beta diversity. Strikingly, ecosystem stability was more strongly related to richness synchrony than to species richness itself, likely because richness synchrony integrates information about community processes and environmental forcing. Our study highlights a new approach for studying spatiotemporal community dynamics and emphasizes the spatial dimensions of community dynamics and stability.

     
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  8. Abstract

    Framework‐building corals create the three‐dimensional structure of coral reefs and are subject to predation from fishes, echinoderms, and gastropods. Anthropogenic stressors can magnify the effects of such top‐down pressure on foundation species. The gastropodCoralliophilaviolacea(Kiener, 1836) depletes coral energy reserves via predation, potentially increasing coral susceptibility to land‐based pollution (i.e., sediment accumulation and nutrient pollution). We hypothesized that sedimentation would worsen coral mortality, while nutrient enrichment would mitigate the harmful effects of sediment and predation on coral mortality by increasing the densities of algal symbionts. To test these hypotheses, we conducted in situ surveys of the fringing reefs in Mo'orea, French Polynesia to explore the relationships among massivePoritesspp. cover,C. violaceadensities, and sediment accumulation on coral colonies across low and high nutrient sites. We also conducted a factorial field experiment to test the interactions among these stressors on coral tissue mortality, symbiont densities, and chlorophyll. MassivePoritescolonies at higher nutrient sites hadC. violaceadensities 13 times higher than at low nutrient sites but there was no difference in the amount of live tissue on coral colonies with or without snails among these sites. In our experiment, there were interactions between predation and nutrients as well as nutrients and sediment that impacted coral mortality. Sedimentation and predation byC. violaceaincreased coral tissue mortality independently by ~20%. Nutrient enrichment reduced this effect in corals under sedimentation or predation pressure by lowering coral tissue mortality by 18% and increasing algal symbiont densities by ~28%. Our results indicate that sediment does not magnify top‐down pressure on this coral, and that moderate nutrient enrichment may interact with predation in complex, unexpected ways to alter the responses of corals to top‐down pressure.

     
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  9. Abstract

    Variation among functionally similar species in their response to environmental stress buffers ecosystems from changing states. Functionally similar species may often be cryptic species representing evolutionarily distinct genetic lineages that are morphologically indistinguishable. However, the extent to which cryptic species differ in their response to stress, and could therefore provide a source of response diversity, remains unclear because they are often not identified or are assumed to be ecologically equivalent. Here, we uncover differences in the bleaching response between sympatric cryptic species of the common Indo‐Pacific coral,Pocillopora. In April 2019, prolonged ocean heating occurred at Moorea, French Polynesia. 72% of pocilloporid colonies bleached after 22 d of severe heating (>8oC‐days) at 10 m depth on the north shore fore reef. Colony mortality ranged from 11% to 42% around the island four months after heating subsided. The majority (86%) of pocilloporids that died from bleaching belonged to a single haplotype, despite twelve haplotypes, representing at least five species, being sampled. Mitochondrial (open reading frame) sequence variation was greater between the haplotypes that experienced mortality versus haplotypes that all survived than it was between nominal species that all survived. Colonies > 30 cm in diameter were identified as the haplotype experiencing the most mortality, and in 1125 colonies that were not genetically identified, bleaching and mortality increased with colony size. Mortality did not increase with colony size within the haplotype suffering the highest mortality, suggesting that size‐dependent bleaching and mortality at the genus level was caused instead by differences among cryptic species. The relative abundance of haplotypes shifted between February and August, driven by declines in the same common haplotype for which mortality was estimated directly, at sites where heat accumulation was greatest, and where larger colony sizes occurred. The identification of morphologically indistinguishable species that differ in their response to thermal stress, but share a similar ecological function in terms of maintaining a coral‐dominated state, has important consequences for uncovering response diversity that drives resilience, especially in systems with low or declining functional diversity.

     
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  10. Abstract

    Rainfall mobilizes and transports anthropogenic sources of sediments and nutrients from terrestrial to coastal marine ecosystems, and episodic but extreme rainfall may drive high fluxes to marine communities. Between January 13thand January 22nd, 2017, the South Pacific Island of Moorea, French Polynesia experienced an extreme rainfall event. ~57 cm of rain was delivered over a 10-day storm. We quantified pulsed sediments and nutrients transported to nearshore reefs. We determined the spatial and temporal extent of the sediment pulse with estimates of water transparency. We quantified pulsed nutrients at multiple spatial and temporal scales. To determine if terrestrial nutrients were incorporated into the benthic community, we collected macroalgae over 10 days following the storm and measured tissue nutrient concentrations and δN15. Pulsed sediments impacted water clarity for 6 days following the storm, with greatest impacts closest to the river mouth. Nitrite +nitrate concentrations were >100 times the average while phosphate was >25 times average. Macroalgal tissue nutrients were elevated, and δN15implicates sewage as the source, demonstrating transported nutrients were transferred to producer communities. Future climate change predictions suggest extreme rainfall will become more common in this system, necessitating research on these pulses and their ramifications on marine communities.

     
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