Pelagic-feeding seabirds deliver nutrient subsidies that enhance the productivity, biodiversity, and resilience of terrestrial and marine ecosystems, particularly in nutrient-poor tropical environments. However, the biogeophysical variables governing the fluxes of these nutrients within and among interconnected ecosystems remain poorly understood. To address this, we examined the spatial distribution of seabird-vectored nutrients in the seascape of Tetiaroa, a semi-enclosed coral atoll in French Polynesia, where seabird populations and associated nutrient cycles are recovering after recent rat eradication. We focus on the nitrogen isotope (delta 15N) signatures of a dominant marine alga as evidence of seabird-vectored nutrient uptake. Integrating stable isotope analysis within a seascape ecology framework, we show that breeding seabird biomass, depth, distance to land, geographic location within the atoll, and seafloor curvature drive spatial patterns of nutrient enrichment. Specifically, our models account for up to 88% of the variation in algal delta 15N signatures and reveal peak enrichment in shallow, nearshore areas where water flow slows and converges due to localised seafloor curvature. These results extend previous research by highlighting seafloor geomorphology, notably curvature, as a modulator of fine-scale nutrient delivery patterns. Although a complex model incorporating 11 high-resolution biogeophysical variables enhanced spatial predictions by revealing fine-scale variations, a simpler model using only five of these variables was comparably effective in capturing overall spatial trends. This study identifies the key seascape configuration and complexity characteristics likely to affect the spatial patterns of recovery potential following the restoration of seabird-driven nutrient cycles, offering valuable guidance for ongoing restoration efforts in this coupled island-reef system. Future investigations could assess how the effects of biogeophysical variables on nutrient delivery vary in magnitude and direction across different geographic, geological, and anthropogenic contexts.

Ecosystems are intrinsically linked, such that management actions in one ecosystem can influence adjacent ecosystems. However, adequate data, and even protocols, for monitoring cross-ecosystem responses to conservation initiatives are lacking. Here, we evaluate potential indicators, operating on different spatial, temporal, and biological scales, for measuring the effects of island-based restoration on coral reef ecosystems. We show that island restoration status had consistent effects on populations of tropical seabirds across spatial scales from 100 m to entire islands. Seabirds, in turn, provided nutrient subsidies that were incorporated by marine algae and coral-reef fishes, with the most pronounced effects closer to shore, at leeward sites, and at low trophic levels. Microbes and macroalgae exhibited assemblage-level responses to seabird-derived nutrients entering the marine environment, but there were few differences in coral reef benthic and fish assemblages. By identifying and focusing on specific indicators such as macroalgal nutrients, managers can better monitor cross-ecosystem responses to conservation interventions with limited resources.

BackgroundEvolutionary tradeoffs between life-history strategies are important in animal evolution. Because microbes can influence multiple aspects of host physiology, including growth rate and susceptibility to disease or stress, changes in animal-microbial symbioses have the potential to mediate life-history tradeoffs. Scleractinian corals provide a biodiverse, data-rich, and ecologically-relevant host system to explore this idea.ResultsUsing a comparative approach, we tested if coral microbiomes correlate with disease susceptibility across 425 million years of coral evolution by conducting a cross-species coral microbiome survey (the "Global Coral Microbiome Project") and combining the results with long-term global disease prevalence and coral trait data. Interpreting these data in their phylogenetic context, we show that microbial dominance predicts disease susceptibility, and traced this dominance-disease association to a single putatively beneficial symbiont genus, Endozoicomonas. Endozoicomonas relative abundance in coral tissue explained 30% of variation in disease susceptibility and 60% of variation in microbiome dominance across 40 coral genera, while also correlating strongly with high growth rates.ConclusionsThese results demonstrate that the evolution of Endozoicomonas symbiosis in corals correlates with both disease prevalence and growth rate, and suggest a mediating role. Exploration of the mechanistic basis for these findings will be important for our understanding of how microbial symbioses influence animal life-history tradeoffs.

Nearly a third of seabird species are at risk of extinction, rendering them among the most threatened bird taxa globally. The decline in seabird populations has major ramifications for their associated ecosystems. An expansive literature covers seabird impacts on their breeding islands, and growing research expands understanding of the circular seabird economy — cross-ecosystem connections of seabirds from oceans to islands, and back to nearshore marine ecosystems, mainly driven by nutrient transfer. Amid the twin biodiversity and climate crises, maintaining and restoring the circular seabird economy is one way to achieve large-scale, cross-ecosystem impacts with simple and time-tested conservation methods. This Review summarizes researchers’ understanding of the circular seabird economy and outlines goals for future research. Historically, research has focused on terrestrial impacts, with emerging research explicitly studying the cross-ecosystem impacts of seabirds. We identify substantial knowledge gaps, with research needed to understand how the circular seabird economy changes with space, time, across biomes and with island size. Emerging analytic and monitoring tools will help to propel this research forward. Many coastal communities, especially Indigenous people, rely on seabirds for their livelihoods and cultural connections, and so taking a people-centred approach incorporating Indigenous knowledge and perspectives is critical moving forward. Seabirds are top predators and nutrient cyclers in marine island ecosystems, but are threatened by risk of extinction. This Review explores the circular seabird economy around islands and discusses how healthy seabird populations can support more resilient island ecosystems.

Nutrient availability drives community structure and ecosystem processes, especially in tropical lagoons that are typically oligotrophic but often receive allochthonous inputs from land. Terrestrially derived nutrients are introduced to tropical lagoons by surface runoff and submarine groundwater discharge, which are influenced by seasonal precipitation. However, terrigenous inputs presumably diminish along the onshore-offshore gradients within lagoons. We characterized nutrient availability in the lagoons of a tropical high island, Moorea, French Polynesia, using spatially distributed measurements of nitrogen content in the tissues of a widespread macroalga during the rainy season over 4 yr. We used synoptic water column sampling to identify associations among macroalgal nutrient content and the composition of inorganic macronutrients, dissolved organic matter, and microbial communities. We paired these data with quantifications of land use in nearby watersheds to uncover links between terrestrial factors, aquatic chemistry, and microbial communities. Algal N content was highest near shore and near large, human-impacted watersheds, and lower at offshore sites. Sites with high algal N had water columns with high nitrite + nitrate, silicate, and increased humic organic matter (based on a fluorescence Humification Index), especially following rain. Microbial communities were differentiated among nearshore habitats and covaried with algal N and water chemistry, supporting the hypothesis that terrigenous nutrient enrichment shapes microbial dynamics in otherwise oligotrophic tropical lagoons. This study reveals that land-sea connections create nutrient subsidies that are important for lagoon biogeochemistry and microbiology, indicating that future changes in land use or precipitation will modify ecosystem processes in tropical lagoons.

Coral reefs are global biodiversity hotspots, important for ocean health and providing ecosystem services for thousands of species (including humans). Coral benthic communities form the structural basis of these ecosystems, influencing ecological processes and ecosystem functions. For thousands of years, coral benthic communities have been driven by naturally occurring properties of the environment, which we refer to as biophysical drivers. However, as humans increasingly encroach on and alter coastal marine ecosystems, anthropogenic conditions may override biophysical drivers, making it challenging to identify the sources of changes in community composition and consequent ecosystem functioning. Here, we use multivariate analyses to demonstrate that bathymetric slope (surface steepness) and intercardinal bearing, a proxy for wind and wave exposure, are significant drivers of benthic composition across Tetiaroa, French Polynesia, a remote coral atoll where the influences of biophysical conditions have not been previously investigated. Distance-based redundancy analysis concluded that together, these biophysical variables explained 66.02% of the variance in benthic community composition. Determining the most important drivers of benthic community composition in this area of minimal human influence provides baseline data for natural coral reef ecosystems. This information will help us understand and predict coral reef community responses to changing environmental conditions and guide conservation and restoration efforts of this ecologically important atoll.

Microbiomes are essential features of holobionts, providing their hosts with key metabolic and functional traits like resistance to environmental disturbances and diseases. In scleractinian corals, questions remain about the microbiome's role in resistance and resilience to factors contributing to the ongoing global coral decline and whether microbes serve as a form of holobiont ecological memory. To test if and how coral microbiomes affect host health outcomes during repeated disturbances, we conducted a large-scale (32 exclosures, 200 colonies, and 3 coral species sampled) and long-term (28 months, 2018-2020) manipulative experiment on the forereef of Mo'orea, French Polynesia. In 2019 and 2020, this reef experienced the two most severe marine heatwaves on record for the site. Our experiment and these events afforded us the opportunity to test microbiome dynamics and roles in the context of coral bleaching and mortality resulting from these successive and severe heatwaves. We report unique microbiome responses to repeated heatwaves in Acropora retusa, Porites lobata, and Pocillopora spp., which included: microbiome acclimatization in A. retusa, and both microbiome resilience to the first marine heatwave and microbiome resistance to the second marine heatwave in Pocillopora spp. Moreover, observed microbiome dynamics significantly correlated with coral species-specific phenotypes. For example, bleaching and mortality in A. retusa both significantly increased with greater microbiome beta dispersion and greater Shannon Diversity, while P. lobata colonies had different microbiomes across mortality prevalence. Compositional microbiome changes, such as changes to proportions of differentially abundant putatively beneficial to putatively detrimental taxa to coral health outcomes during repeated heat stress, also correlated with host mortality, with higher proportions of detrimental taxa yielding higher mortality in A. retusa. This study reveals evidence for coral species-specific microbial responses to repeated heatwaves and, importantly, suggests that host-dependent microbiome dynamics may provide a form of holobiont ecological memory to repeated heat stress.

Coral microhabitats are colonized by a myriad of microorganisms, including diverse bacteria which are essential for host functioning and survival. However, the location, transmission, and functions of individual bacterial species living inside the coral tissues remain poorly studied. Here, we show that a previously undescribed bacterial symbiont of the coral Pocillopora acuta forms cell-associated microbial aggregates (CAMAs) within the mesenterial filaments. CAMAs were found in both adults and larval offspring, suggesting vertical transmission. In situ laser capture microdissection of CAMAs followed by 16S rRNA gene amplicon sequencing and shotgun metagenomics produced a near complete metagenome-assembled genome. We subsequently cultured the CAMA bacteria from Pocillopora acuta colonies, and sequenced and assembled their genomes. Phylogenetic analyses showed that the CAMA bacteria belong to an undescribed Endozoicomonadaceae genus and species, which we propose to name Candidatus Sororendozoicomonas aggregata gen. nov sp. nov. Metabolic pathway reconstruction from its genome sequence suggests this species can synthesize most amino acids, several B vitamins, and antioxidants, and participate in carbon cycling and prey digestion, which may be beneficial to its coral hosts. This study provides detailed insights into a new member of the widespread Endozoicomonadaceae family, thereby improving our understanding of coral holobiont functioning. Vertically transmitted, tissue-associated bacteria, such as Sororendozoicomonas aggregata may be key candidates for the development of microbiome manipulation approaches with long-term positive effects on the coral host.

Over the past two decades, researchers have searched for methods to better understand the relationship between coral hosts and their microbiomes. Data on how coral-associated bacteria are involved in their host’s responses to stressors that cause bleaching, disease, and other deleterious effects can elucidate how they may mediate, ameliorate, and exacerbate interactions between the coral and the surrounding environment. At the same time tracking coral bacteria dynamics can reveal previously undiscovered mechanisms of coral resilience, acclimatization, and evolutionary adaptation. Although modern techniques have reduced the cost of conducting high-throughput sequencing of coral microbes, to explore the composition, function, and dynamics of coral-associated bacteria, it is necessary that the entire procedure, from collection to sequencing, and subsequent analysis be carried out in an objective and effective way. Corals represent a difficult host with which to work, and unique steps in the process of microbiome assessment are necessary to avoid inaccuracies or unusable data in microbiome libraries, such as off-target amplification of host sequences. Here, we review, compare and contrast, and recommend methods for sample collection, preservation, and processing (e.g., DNA extraction) pipelines to best generate 16S amplicon libraries with the aim of tracking coral microbiome dynamics. We also discuss some basic quality assurance and general bioinformatic methods to analyze the diversity, composition, and taxonomic profiles of the microbiomes. This review aims to be a generalizable guide for researchers interested in starting and modifying the molecular biology aspects of coral microbiome research, highlighting best practices and tricks of the trade.

AbstractCoral microhabitats are colonized by a myriad of microorganisms, including diverse bacteria which are essential for host functioning and survival. However, the location, transmission, and functions of individual bacterial species living inside the coral tissues remain poorly studied. Here, we show that a previously undescribed bacterial symbiont of the coralPocillopora acutaforms cell-associated microbial aggregates (CAMAs) within the mesenterial filaments. CAMAs were found in both adults and larval offspring, providing evidence of vertical transmission.In situlaser capture microdissection of CAMAs followed by 16S rRNA gene metabarcoding and shotgun metagenomics produced a near complete metagenome-assembled genome. We subsequently cultured the CAMA bacteria fromP. acutacolonies, and sequenced and assembled their genomes. Phylogenetic analyses showed that the CAMA bacteria belong to an undescribed Endozoicomonadaceae genus and species, which we propose to nameSororendozoicomonas aggregatagen. nov sp. nov. Metabolic pathway reconstruction from its genome sequence suggests this species can synthesize most amino acids, several B vitamins, and antioxidants, which may be beneficial to its coral hosts. This study provides detailed insights into a new member of the widespread Endozoicomonadaceae family, thereby improving our understanding of coral holobiont functioning. Vertically transmitted, tissue-associated bacteria, such asS. aggregatamay be key candidates for the development of microbiome manipulation approaches with long-term positive effects on the coral host.

A growing body of research has established that the microbiome can mediate the dynamics and functional capacities of diverse biological systems. Yet, we understand little about what governs the response of these microbial communities to host or environmental changes.

16S rRNA gene profiling (amplicon sequencing) is a popular technique for understanding host-associated and environmental microbial communities. Most protocols for sequencing amplicon libraries follow a standardized pipeline that can differ slightly depending on laboratory facility and user. Given that the same variable region of the 16S gene is targeted, it is generally accepted that sequencing output from differing protocols are comparable and this assumption underlies our ability to identify universal patterns in microbial dynamics through meta-analyses. However, discrepant results from a combined 16S rRNA gene dataset prepared by two labs whose protocols differed only in DNA polymerase and sequencing platform led us to scrutinize the outputs and challenge the idea of confidently combining them for standard microbiome analysis. Using technical replicates of reef-building coral samples from two species, Montipora aequituberculata and Porites lobata, we evaluated the consistency of alpha and beta diversity metrics between data resulting from these highly similar protocols. While we found minimal variation in alpha diversity between platform, significant differences were revealed with most beta diversity metrics, dependent on host species. These inconsistencies persisted following removal of low abundance taxa and when comparing across higher taxonomic levels, suggesting that bacterial community differences associated with sequencing protocol are likely to be context dependent and difficult to correct without extensive validation work. The results of this study encourage caution in the statistical comparison and interpretation of studies that combine rRNA gene sequence data from distinct protocols and point to a need for further work identifying mechanistic causes of these observed differences.

Coral cover worldwide has been declining due to heat stress caused by climate change. Here we report the impacts of the 2015–2016 El Niño mass coral bleaching event on the coral cover of reefs located on central and northern atolls of the Maldives. We surveyed six reef sites in the Alifu Alifu (Ari) and Baa (South Maalhosmadulu) Atolls using replicate 20 m benthic photo transects at two depths per reef site. Live and recently dead coral cover identified from images differed between reef sites and depth. Recently dead corals on average made up 33% of the coral assemblage at shallow sites and 24% at deep sites. This mortality was significantly lower in massive corals than in branching corals, reaching an average of only 6% compared to 41%, respectively. The best predictors of live coral cover were depth and morphology, with a greater percentage of live coral at deep sites and in massive corals. The same predictors best described the prevalence of recently dead coral, but showed inverse trends to live coral. However, there was high variability among reef sites, which could be attributed to additional local stressors. Coral bleaching and resulting coral mortalities, such as the ones reported here, are of particular concern for small island nations like the Maldives, which are reliant on coral reefs.

Prospects for coral persistence through increasingly frequent and extended heatwaves seem bleak. Coral recovery from bleaching is only known to occur after temperatures return to normal, and mitigation of local stressors does not appear to augment coral survival. Capitalizing on a natural experiment in the equatorial Pacific, we track individual coral colonies at sites spanning a gradient of local anthropogenic disturbance through a tropical heatwave of unprecedented duration. Unexpectedly, some corals survived the event by recovering from bleaching while still at elevated temperatures. These corals initially had heat-sensitive algal symbiont communities, endured bleaching, and then recovered through proliferation of heat-tolerant symbionts. This pathway to survival only occurred in the absence of strong local stressors. In contrast, corals in highly disturbed areas were already dominated by heat-tolerant symbionts, and despite initially resisting bleaching, these corals had no survival advantage in one species and 3.3 times lower survival in the other. These unanticipated connections between disturbance, coral symbioses and heat stress resilience reveal multiple pathways to coral survival through future prolonged heatwaves.

The structural complexity of coral reef environments has a strong influence on the assemblage of reef-associated fishes and invertebrates. These unique ecosystems provide these reef-associated species with a broad range of potential habitats, which offer important resources such as food and shelter. The most studied habitat association on reefs is that of hard coral and fish, where hard coral cover has been found to have a large and positive influence on the assemblage of reef fishes. In contrast, soft coral has been considered poor habitat due to their chemical defences and weak body architecture. However, the empirical basis for this assumption is minimal and the ecological importance of soft corals remains controversial and unresolved. The present study closely examined fish assemblages utilising a mixed mosaic of coral reef habitats at sites ranging from hard to soft coral dominated assemblages. Fishes associated with soft coral in a variety of ways including as shelter, a source of food or a surface on which epiphytic food was sourced. Fish assemblages remained similar between soft and hard coral dominated habitats, and there was no evidence that a high percentage cover of soft coral had deleterious effects. Further, a significant increase in species richness of fishes was found with increasing soft coral cover, suggesting that the importance of soft coral habitat has been underestimated on reefs with a mosaic of different habitats. Here, we discuss the implications of these associations and suggest that soft coral provides distinct habitat for reef fishes, and future research should address their ecological importance.

The world's coral reefs are under unparalleled pressure due to climate change, stimulating research focused on preventing further damage and loss in these ecosystems. The coral microbiome has been widely acknowledged as crucial to coral health and function, playing multiple roles in key biological processes. Recent empirical studies suggest that microbes may contribute to coral host tolerance of thermal stress, and harnessing these benefits through microbiome engineering (ME) may provide a mechanism for enhancing climate resilience in corals. Although coral ME is in its infancy, similar and successful ME approaches that are already underway in other fields - including agriculture, medicine, and wastewater treatment - may serve to guide and improve ME techniques in corals. We discuss current applications of ME, identify three key research priorities that will help elucidate the viability of ME for corals, and consider the implications of using these approaches for reef restoration.

The coral microbiome is known to fluctuate in response to environmental variation and has been suggested to vary seasonally. However, most studies to date, particularly studies on bacterial communities, have examined temporal variation over a time frame of less than 1 year, which is insufficient to establish if microbiome variations are indeed seasonal in nature. The present study focused on expanding our understanding of long-term variability in microbial community composition using two common coral species, Acropora hyacinthus, and Acropora spathulata, at two mid-shelf reefs on the Great Barrier Reef. By sampling over a 2-year time period, this study aimed to determine whether temporal variations reflect seasonal cycles. Community composition of both bacteria and Symbiodiniaceae was characterized through 16S rRNA gene and ITS2 rDNA metabarcoding. We observed significant variations in community composition of both bacteria and Symbiodiniaceae among time points for A. hyacinthus and A. spathulata. However, there was no evidence to suggest that temporal variations were cyclical in nature and represented seasonal variation. Clear evidence for differences in the microbial communities found between reefs suggests that reef location and coral species play a larger role than season in driving microbial community composition in corals. In order to identify the basis of temporal patterns in coral microbial community composition, future studies should employ longer time series of sampling at sufficient temporal resolution to identify the environmental correlates of microbiome variation.