High response diversity and conspecific density-dependence, not species interactions, drive dynamics of coral reef fish communities.

Species-to-species and species-to-environment interactions are key drivers of community dynamics. Disentangling these drivers in species-rich assemblages is challenging due to the high number of potentially interacting species (the 'curse of dimensionality'). We develop a process-based model that quantifies how intraspecific and interspecific interactions, and species' covarying responses to environmental fluctuations, jointly drive community dynamics. We fit the model to reef fish abundance time series from 41 reefs of Australia's Great Barrier Reef. We found that fluctuating relative abundances are driven by species' heterogenous responses to environmental fluctuations, whereas interspecific interactions are negligible. Species differences in long-term average abundances are driven by interspecific variation in the magnitudes of both conspecific density-dependence and density-independent growth rates. This study introduces a novel approach to overcoming the curse of dimensionality, which reveals highly individualistic dynamics in coral reef fish communities that imply a high level of niche structure.

Disturbance-Induced Changes in Population Size Structure Promote Coral Biodiversity.

AbstractReef-building coral assemblages are typically species rich, yet the processes maintaining high biodiversity remain poorly understood. Disturbance has long been thought to promote coral species coexistence by reducing the strength of competition (i.e., the intermediate disturbance hypothesis [IDH]). However, such disturbance-induced effects are insufficient to inhibit competitive exclusion. Nevertheless, there are other mechanisms by which disturbance and, more generally, environmental variation can favor coexistence. Here, we develop a size-structured, stochastic coral competition model calibrated with field data from two common colony morphologies to investigate the effects of hydrodynamic disturbance on community dynamics. We show that fluctuations in wave action can promote coral species coexistence but that this occurs via interspecific differences in size-dependent mortality rather than solely via stochastic fluctuations in competition (i.e., free space availability). While this mechanism differs from that originally envisioned in the IDH, it is nonetheless a mechanism by which intermediate levels of disturbance do promote coexistence. Given the sensitivity of coexistence to disturbance frequency and intensity, anthropogenic changes in disturbance regimes are likely to affect coral assemblages in ways that are not predictable from single-population models.

Sustainable reference points for multispecies coral reef fisheries.

Sustainably managing fisheries requires regular and reliable evaluation of stock status. However, most multispecies reef fisheries around the globe tend to lack research and monitoring capacity, preventing the estimation of sustainable reference points against which stocks can be assessed. Here, combining fish biomass data for >2000 coral reefs, we estimate site-specific sustainable reference points for coral reef fisheries and use these and available catch estimates to assess the status of global coral reef fish stocks. We reveal that >50% of sites and jurisdictions with available information have stocks of conservation concern, having failed at least one fisheries sustainability benchmark. We quantify the trade-offs between biodiversity, fish length, and ecosystem functions relative to key benchmarks and highlight the ecological benefits of increasing sustainability. Our approach yields multispecies sustainable reference points for coral reef fisheries using environmental conditions, a promising means for enhancing the sustainability of the world's coral reef fisheries.

Six years of demography data for 11 reef coral species.

Scleractinian corals are colonial animals with a range of life-history strategies, making up diverse species assemblages that define coral reefs. We tagged and tracked ~30 colonies from each of 11 species during seven trips spanning 6 years (2009-2015) to measure their vital rates and competitive interactions on the reef crest at Trimodal Reef, Lizard Island, Australia. Pairs of species were chosen from five growth forms in which one species of the pair was locally rare (R) and the other common (C). The sampled growth forms were massive (Goniastrea pectinata [R] and G. retiformis [C]), digitate (Acropora humilis [R] and A. cf. digitifera [C]), corymbose (A. millepora [R] and A. nasuta [C]), tabular (A. cytherea [R] and A. hyacinthus [C]) and arborescent (A. robusta [R] and A. intermedia [C]). An extra corymbose species with intermediate abundance, A. spathulata was included when it became apparent that A. millepora was too rare on the reef crest, making the 11 species in total. The tagged colonies were visited each year in the weeks prior to spawning. During visits, two or more observers each took two or three photographs of each tagged colony from directly above and on the horizontal plane with a scale plate to track planar area. Dead or missing colonies were recorded and new colonies tagged to maintain ~30 colonies per species throughout the 6 years of the study. In addition to tracking tagged corals, 30 fragments were collected from neighboring untagged colonies of each species for counting numbers of eggs per polyp (fecundity); and fragments of untagged colonies were brought into the laboratory where spawned eggs were collected for biomass and energy measurements. We also conducted surveys at the study site to generate size structure data for each species in several of the years. Each tagged colony photograph was digitized by at least two people. Therefore, we could examine sources of error in planar area for both photographers and outliners. Competitive interactions were recorded for a subset of species by measuring the margins of tagged colony outlines interacting with neighboring corals. The study was abruptly ended by Tropical Cyclone Nathan (Category 4) that killed all but nine of the more than 300 tagged colonies in early 2015. Nonetheless, these data will be of use to other researchers interested in coral demography and coexistence, functional ecology, and parametrizing population, community, and ecosystem models. The data set is not copyright restricted, and users should cite this paper when using the data.

Benthic composition changes on coral reefs at global scales.

Globally, ecosystems are being reconfigured by a range of intensifying human-induced stressors. Coral reefs are at the forefront of this environmental transformation, and if we are to secure their key ecosystem functions and services, it is important to understand the likely configuration of future reefs. However, the composition and trajectory of global coral reef benthic communities is currently unclear. Here our global dataset of 24,468 observations spanning 22 years (1997-2018) revealed that particularly marked declines in coral cover occurred in the Western Atlantic and Central Pacific. The data also suggest that high macroalgal cover, widely regarded as the major degraded state on coral reefs, is a phenomenon largely restricted to the Western Atlantic. At a global scale, the raw data suggest decreased average (± standard error of the mean) hard coral cover from 36 ± 1.4% to 19 ± 0.4% (during a period delineated by the first global coral bleaching event (1998) until the end of the most recent event (2017)) was largely associated with increased low-lying algal cover such as algal turfs and crustose coralline algae. Enhanced understanding of reef change, typified by decreased hard coral cover and increased cover of low-lying algal communities, will be key to managing Anthropocene coral reefs.

Net effects of life-history traits explain persistent differences in abundance among similar species.

Life-history traits are promising tools to predict species commonness and rarity because they influence a population's fitness in a given environment. Yet, species with similar traits can have vastly different abundances, challenging the prospect of robust trait-based predictions. Using long-term demographic monitoring, we show that coral populations with similar morphological and life-history traits show persistent (decade-long) differences in abundance. Morphological groups predicted species positions along two, well known life-history axes (the fast-slow continuum and size-specific fecundity). However, integral projection models revealed that density-independent population growth (λ) was more variable within morphological groups, and was consistently higher in dominant species relative to rare species. Within-group λ differences projected large abundance differences among similar species in short timeframes, and were generated by small but compounding variation in growth, survival, and reproduction. Our study shows that easily measured morphological traits predict demographic strategies, yet small life-history differences can accumulate into large differences in λ and abundance among similar species. Quantifying the net effects of multiple traits on population dynamics is therefore essential to anticipate species commonness and rarity.

Volatility in coral cover erodes niche structure, but not diversity, in reef fish assemblages.

The world's coral reefs are experiencing increasing volatility in coral cover, largely because of anthropogenic environmental change, highlighting the need to understand how such volatility will influence the structure and dynamics of reef assemblages. These changes may influence not only richness or evenness but also the temporal stability of species' relative abundances (temporal beta-diversity). Here, we analyzed reef fish assemblage time series from the Great Barrier Reef to show that, overall, 75% of the variance in abundance among species was attributable to persistent differences in species' long-term mean abundances. However, the relative importance of stochastic fluctuations in abundance was higher on reefs that experienced greater volatility in coral cover, whereas it did not vary with drivers of alpha-diversity. These findings imply that increased coral cover volatility decreases temporal stability in relative abundances of fishes, a transformation that is not detectable from static measures of biodiversity.

Interactive effects of multiple stressors vary with consumer interactions, stressor dynamics and magnitude.

Predicting the impacts of multiple stressors is important for informing ecosystem management but is impeded by a lack of a general framework for predicting whether stressors interact synergistically, additively or antagonistically. Here, we use process-based models to study how interactions generalise across three levels of biological organisation (physiological, population and consumer-resource) for a two-stressor experiment on a seagrass model system. We found that the same underlying processes could result in synergistic, additive or antagonistic interactions, with interaction type depending on initial conditions, experiment duration, stressor dynamics and consumer presence. Our results help explain why meta-analyses of multiple stressor experimental results have struggled to identify predictors of consistently non-additive interactions in the natural environment. Experiments run over extended temporal scales, with treatments across gradients of stressor magnitude, are needed to identify the processes that underpin how stressors interact and provide useful predictions to management.

Emergent properties in the responses of tropical corals to recurrent climate extremes.

The frequency, intensity, and spatial scale of climate extremes are changing rapidly due to anthropogenic global warming.1,2 A growing research challenge is to understand how multiple climate-driven disturbances interact with each other over multi-decadal time frames, generating combined effects that cannot be predicted from single events alone.3-5 Here we examine the emergent dynamics of five coral bleaching events along the 2,300 km length of the Great Barrier Reef that affected >98% of the Reef between 1998 and 2020. We show that the bleaching responses of corals to a given level of heat exposure differed in each event and were strongly influenced by contingency and the spatial overlap and strength of interactions between events. Naive regions that escaped bleaching for a decade or longer were the most susceptible to bouts of heat exposure. Conversely, when pairs of successive bleaching episodes were close together (1-3 years apart), the thermal threshold for severe bleaching increased because the earlier event hardened regions of the Great Barrier Reef to further impacts. In the near future, the biological responses to recurrent bleaching events may become stronger as the cumulative geographic footprint expands further, potentially impairing the stock-recruitment relationships among lightly and severely bleached reefs with diverse recent histories. Understanding the emergent properties and collective dynamics of recurrent disturbances will be critical for predicting spatial refuges and cumulative ecological responses, and for managing the longer-term impacts of anthropogenic climate change on ecosystems.

Coral adaptation to climate change: Meta-analysis reveals high heritability across multiple traits.

Anthropogenic climate change is a rapidly intensifying selection pressure on biodiversity across the globe and, particularly, on the world's coral reefs. The rate of adaptation to climate change is proportional to the amount of phenotypic variation that can be inherited by subsequent generations (i.e., narrow-sense heritability, h2 ). Thus, traits that have higher heritability (e.g., h2  > 0.5) are likely to adapt to future conditions faster than traits with lower heritability (e.g., h2  < 0.1). Here, we synthesize 95 heritability estimates across 19 species of reef-building corals. Our meta-analysis reveals low heritability (h2 < 0.25) of gene expression metrics, intermediate heritability (h2  = 0.25-0.50) of photochemistry, growth, and bleaching, and high heritability (h2  > 0.50) for metrics related to survival and immune responses. Some of these values are higher than typically observed in other taxa, such as survival and growth, while others were more comparable, such as gene expression and photochemistry. There was no detectable effect of temperature on heritability, but narrow-sense heritability estimates were generally lower than broad-sense estimates, indicative of significant non-additive genetic variation across traits. Trait heritability also varied depending on coral life stage, with bleaching and growth in juveniles generally having lower heritability compared to bleaching and growth in larvae and adults. These differences may be the result of previous stabilizing selection on juveniles or may be due to constrained evolution resulting from genetic trade-offs or genetic correlations between growth and thermotolerance. While we find no evidence that heritability decreases under temperature stress, explicit tests of the heritability of thermal tolerance itself-such as coral thermal reaction norm shape-are lacking. Nevertheless, our findings overall reveal high trait heritability for the majority of coral traits, suggesting corals may have a greater potential to adapt to climate change than has been assumed in recent evolutionary models.

Natural experiments and long-term monitoring are critical to understand and predict marine host-microbe ecology and evolution.

Marine multicellular organisms host a diverse collection of bacteria, archaea, microbial eukaryotes, and viruses that form their microbiome. Such host-associated microbes can significantly influence the host's physiological capacities; however, the identity and functional role(s) of key members of the microbiome ("core microbiome") in most marine hosts coexisting in natural settings remain obscure. Also unclear is how dynamic interactions between hosts and the immense standing pool of microbial genetic variation will affect marine ecosystems' capacity to adjust to environmental changes. Here, we argue that significantly advancing our understanding of how host-associated microbes shape marine hosts' plastic and adaptive responses to environmental change requires (i) recognizing that individual host-microbe systems do not exist in an ecological or evolutionary vacuum and (ii) expanding the field toward long-term, multidisciplinary research on entire communities of hosts and microbes. Natural experiments, such as time-calibrated geological events associated with well-characterized environmental gradients, provide unique ecological and evolutionary contexts to address this challenge. We focus here particularly on mutualistic interactions between hosts and microbes, but note that many of the same lessons and approaches would apply to other types of interactions.

The spatial footprint and patchiness of large-scale disturbances on coral reefs.

Ecosystems have always been shaped by disturbances, but many of these events are becoming larger, more severe and more frequent. The recovery capacity of depleted populations depends on the frequency of disturbances, the spatial distribution of mortality and the scale of dispersal. Here, we show that four mass coral bleaching events on the Great Barrier Reef (in 1998, 2002, 2016 and 2017) each had markedly larger disturbance footprints and were less patchy than a severe category 5 tropical cyclone (Cyclone Yasi, 2011). Severely bleached reefs in 2016 and 2017 were isolated from the nearest lightly affected reefs by up to 146 and 200 km, respectively. In contrast, reefs damaged by Cyclone Yasi were on average 20 km away from relatively undisturbed reefs, well within the estimated range of larval dispersal for most corals. Based on these results, we present a model of coral reef disturbance and recovery to examine (1) how the spatial clustering of disturbances modifies large-scale recovery rates; and (2) how recovery rates are shaped by species' dispersal abilities. Our findings illustrate that the spatial footprint of the recent mass bleaching events poses an unprecedented threat to the resilience of coral species in human history, a threat that is even larger than the amount of mortality suggests.

The population sizes and global extinction risk of reef-building coral species at biogeographic scales.

Knowledge of a species' abundance is critically important for assessing its risk of extinction, but for the vast majority of wild animal and plant species such data are scarce at biogeographic scales. Here, we estimate the total number of reef-building corals and the population sizes of more than 300 individual species on reefs spanning the Pacific Ocean biodiversity gradient, from Indonesia to French Polynesia. Our analysis suggests that approximately half a trillion corals (0.3 × 1012-0.8 × 1012) inhabit these coral reefs, similar to the number of trees in the Amazon. Two-thirds of the examined species have population sizes exceeding 100 million colonies, and one-fifth of the species even have population sizes greater than 1 billion colonies. Our findings suggest that, while local depletions pose imminent threats that can have ecologically devastating impacts to coral reefs, the global extinction risk of most coral species is lower than previously estimated.

An Indo-Pacific coral spawning database.

The discovery of multi-species synchronous spawning of scleractinian corals on the Great Barrier Reef in the 1980s stimulated an extraordinary effort to document spawning times in other parts of the globe. Unfortunately, most of these data remain unpublished which limits our understanding of regional and global reproductive patterns. The Coral Spawning Database (CSD) collates much of these disparate data into a single place. The CSD includes 6178 observations (3085 of which were unpublished) of the time or day of spawning for over 300 scleractinian species in 61 genera from 101 sites in the Indo-Pacific. The goal of the CSD is to provide open access to coral spawning data to accelerate our understanding of coral reproductive biology and to provide a baseline against which to evaluate any future changes in reproductive phenology.

Long-term shifts in the colony size structure of coral populations along the Great Barrier Reef.

The age or size structure of a population has a marked influence on its demography and reproductive capacity. While declines in coral cover are well documented, concomitant shifts in the size-frequency distribution of coral colonies are rarely measured at large spatial scales. Here, we document major shifts in the colony size structure of coral populations along the 2300 km length of the Great Barrier Reef relative to historical baselines (1995/1996). Coral colony abundances on reef crests and slopes have declined sharply across all colony size classes and in all coral taxa compared to historical baselines. Declines were particularly pronounced in the northern and central regions of the Great Barrier Reef, following mass coral bleaching in 2016 and 2017. The relative abundances of large colonies remained relatively stable, but this apparent stability masks steep declines in absolute abundance. The potential for recovery of older fecund corals is uncertain given the increasing frequency and intensity of disturbance events. The systematic decline in smaller colonies across regions, habitats and taxa, suggests that a decline in recruitment has further eroded the recovery potential and resilience of coral populations.

Partitioning colony size variation into growth and partial mortality.

Body size is a trait that broadly influences the demography and ecology of organisms. In unitary organisms, body size tends to increase with age. In modular organisms, body size can either increase or decrease with age, with size changes being the net difference between modules added through growth and modules lost through partial mortality. Rates of colony extension are independent of body size, but net growth is allometric, suggesting a significant role of size-dependent mortality. In this study, we develop a generalizable model of partitioned growth and partial mortality and apply it to data from 11 species of reef-building coral. We show that corals generally grow at constant radial increments that are size independent, and that partial mortality acts more strongly on small colonies. We also show a clear life-history trade-off between growth and partial mortality that is governed by growth form. This decomposition of net growth can provide mechanistic insights into the relative demographic effects of the intrinsic factors (e.g. acquisition of food and life-history strategy), which tend to affect growth, and extrinsic factors (e.g. physical damage, and predation), which tend to affect mortality.

Hierarchical modeling strengthens evidence for density dependence in observational time series of population dynamics.

The extent to which populations in nature are regulated by density-dependent processes is unresolved. While experiments increasingly find evidence of strong density dependence, unmanipulated population time series yield much more ambiguous evidence of regulation, especially when accounting for effects of observation error. Here, we reexamine the evidence for density dependence in time series of population sizes in nature, by conducting an aggregate analysis of the populations in the Global Population Dynamics Database (GPDD). First, following the conventional approach, we fit a density-dependent and a density-independent variant of the Gompertz state-space model to each time series. Then, we conduct an aggregate analysis of the entire database by considering two random-effects density-dependent models that leverage information across data sets. When individual time series are tested independently, we find very little evidence for density dependence. However, in the aggregate, we find very strong evidence for density dependence, even though, paradoxically, estimated strengths of density dependence for individual time series tend to be weaker than when each individual time series is analyzed independently. Furthermore, a hierarchical model that accounts for taxonomic variation in the strength of density dependence reveals that density dependence is consistently stronger in insects and fish than in birds and mammals. Our findings resolve apparent inconsistencies between observational and experimental studies of density dependence by revealing that the observational record does indeed contain strong support for the hypothesis that density dependence is widespread in nature.

Human exploitation shapes productivity-biomass relationships on coral reefs.

Coral reef fisheries support the livelihoods of millions of people in tropical countries, despite large-scale depletion of fish biomass. While human adaptability can help to explain the resistance of fisheries to biomass depletion, compensatory ecological mechanisms may also be involved. If this is the case, high productivity should coexist with low biomass under relatively high exploitation. Here we integrate large spatial scale empirical data analysis and a theory-driven modelling approach to unveil the effects of human exploitation on reef fish productivity-biomass relationships. We show that differences in how productivity and biomass respond to overexploitation can decouple their relationship. As size-selective exploitation depletes fish biomass, it triggers increased production per unit biomass, averting immediate productivity collapse in both the modelling and the empirical systems. This 'buffering productivity' exposes the danger of assuming resource production-biomass equivalence, but may help to explain why some biomass-depleted fish assemblages still provide ecosystem goods under continued global fishing exploitation.