Coral responses to a catastrophic marine heatwave are decoupled from changes in total coral cover at a continental scale.

The services provided by the world's coral reefs are threatened by increasingly frequent and severe marine heatwaves. Heatwave-induced degradation of reefs has often been inferred from the extent of the decline in total coral cover, which overlooks extreme variation among coral taxa in their susceptibility and responses to thermal stress. Here, we provide a continental-scale assessment of coral cover changes at 262 shallow tropical reef sites around Australia, using ecological survey data on 404 coral taxa before and after the 2016 mass bleaching event. A strong spatial structure in coral community composition along large-scale environmental gradients largely dictated how coral communities responded to heat stress. While heat stress variables were the best predictors of change in total coral cover, the pre-heatwave community composition best predicted the temporal beta-diversity index (an indicator of change in community composition over time). Indicator taxa in each coral community differed before and after the heatwave, highlighting potential winners and losers of climate-driven coral bleaching. Our results demonstrate how assessment of change in total cover alone may conceal very different responses in community structure, some of which showed strong regional consistency, and may provide a telling outlook of how coral reefs may reorganize in a warmer future.

Cumulative risk of future bleaching for the world's coral reefs.

Spatial and temporal patterns of future coral bleaching are uncertain, hampering global conservation efforts to protect coral reefs against climate change. Our analysis of daily projections of ocean warming establishes the severity, annual duration, and onset of severe bleaching risk for global coral reefs this century, pinpointing vital climatic refugia. We show that low-latitude coral regions are most vulnerable to thermal stress and will experience little reprieve from climate mitigation. By 2080, coral bleaching is likely to start on most reefs in spring, rather than late summer, with year-round bleaching risk anticipated to be high for some low-latitude reefs regardless of global efforts to mitigate harmful greenhouse gasses. By identifying Earth's reef regions that are at lowest risk of accelerated bleaching, our results will prioritize efforts to limit future loss of coral reef biodiversity.

Ecological generalism and physiology mediate fish biogeographic ranges under ocean warming.

Climate-driven species redistributions are facilitated by niche modifications that increase a species's chances of establishment in novel communities. It is well understood how range-extending species adjust individual niche traits when entering novel environments, yet whether modification of ecological niche traits collectively alters the pace of range extensions or contractions remains unknown. We quantified habitat niche, abundance, physiological performance and cellular defence/damage of range-extending coral reef fishes and coexisting local temperate fishes along a 2000 km latitudinal gradient. We also assessed their dietary and behavioural niches, and establishment potential, to understand whether ecological generalism facilitates successful range extension of coral reef fishes. The coral reef fish that increased all ecological niches, showed stronger establishment, increased physiological performance and cellular damage, but decreased cellular defence at their cold-range edge, whereas tropical species that showed unmodified ecological niches showed lower establishment. One temperate species showed decreased abundance, habitat niche width and body condition, but increased cellular defence, cellular damage and energy reserves at their warm-trailing range, while other temperate species showed contrasting responses. Therefore, ecological generalists might be more successful than ecological specialists during the initial stages of climate change, with increasing future warming strengthening this pattern by physiologically benefitting tropical generalists but disadvantaging temperate specialists.

Continent-wide declines in shallow reef life over a decade of ocean warming.

Human society is dependent on nature1,2, but whether our ecological foundations are at risk remains unknown in the absence of systematic monitoring of species' populations3. Knowledge of species fluctuations is particularly inadequate in the marine realm4. Here we assess the population trends of 1,057 common shallow reef species from multiple phyla at 1,636 sites around Australia over the past decade. Most populations decreased over this period, including many tropical fishes, temperate invertebrates (particularly echinoderms) and southwestern Australian macroalgae, whereas coral populations remained relatively stable. Population declines typically followed heatwave years, when local water temperatures were more than 0.5 °C above temperatures in 2008. Following heatwaves5,6, species abundances generally tended to decline near warm range edges, and increase near cool range edges. More than 30% of shallow invertebrate species in cool latitudes exhibited high extinction risk, with rapidly declining populations trapped by deep ocean barriers, preventing poleward retreat as temperatures rise. Greater conservation effort is needed to safeguard temperate marine ecosystems, which are disproportionately threatened and include species with deep evolutionary roots. Fundamental among such efforts, and broader societal needs to efficiently adapt to interacting anthropogenic and natural pressures, is greatly expanded monitoring of species' population trends7,8.

Safeguarding nutrients from coral reefs under climate change.

The sustainability of coral reef fisheries is jeopardized by complex and interacting socio-ecological stressors that undermine their contribution to food and nutrition security. Climate change has emerged as one of the key stressors threatening coral reefs and their fish-associated services. How fish nutrient concentrations respond to warming oceans remains unclear but these responses are probably affected by both direct (metabolism and trophodynamics) and indirect (habitat and species range shifts) effects. Climate-driven coral habitat loss can cause changes in fish abundance and biomass, revealing potential winners and losers among major fisheries targets that can be predicted using ecological indicators and biological traits. A critical next step is to extend research focused on the quantity of available food (fish biomass) to also consider its nutritional quality, which is relevant to progress in the fields of food security and malnutrition. Biological traits are robust predictors of fish nutrient content and thus potentially indicate how climate-driven changes are expected to impact nutrient availability within future food webs on coral reefs. Here, we outline future research priorities and an anticipatory framework towards sustainable reef fisheries contributing to nutrition-sensitive food systems in a warming ocean.

Tracking widespread climate-driven change on temperate and tropical reefs.

Warming seas, marine heatwaves, and habitat degradation are increasingly widespread phenomena affecting marine biodiversity, yet our understanding of their broader impacts is largely derived from collective insights from independent localized studies. Insufficient systematic broadscale monitoring limits our understanding of the true extent of these impacts and our capacity to track these at scales relevant to national policies and international agreements. Using an extensive time series of co-located reef fish community structure and habitat data spanning 12 years and the entire Australian continent, we found that reef fish community responses to changing temperatures and habitats are dynamic and widespread but regionally patchy. Shifts in composition and abundance of the fish community often occurred within 2 years of environmental or habitat change, although the relative importance of these two mechanisms of climate impact tended to differ between tropical and temperate zones. The clearest of these changes on temperate and subtropical reefs were temperature related, with responses measured by the reef fish thermal index indicating reshuffling according to the thermal affinities of species present. On low latitude coral reefs, the community generalization index indicated shifting dominance of habitat generalist fishes through time, concurrent with changing coral cover. Our results emphasize the importance of maintaining local ecological detail when scaling up datasets to inform national policies and global biodiversity targets. Scaled-up ecological monitoring is needed to discriminate among increasingly diverse drivers of large-scale biodiversity change and better connect presently disjointed systems of biodiversity observation, indicator research, and governance.

Faster ocean warming threatens richest areas of marine biodiversity.

The vulnerability of marine biodiversity to accelerated rates of climatic change is poorly understood. By developing a new method for identifying extreme oceanic warming events during Earth's most recent deglaciation, and comparing these to 21st century projections, we show that future rates of ocean warming will disproportionately affect the most speciose marine communities, potentially threatening biodiversity in more than 70% of current-day global hotspots of marine species richness. The persistence of these richest areas of marine biodiversity will require many species to move well beyond the biogeographic realm where they are endemic, at rates of redistribution not previously seen. Our approach for quantifying exposure of biodiversity to past and future rates of oceanic warming provides new context and scalable information for deriving and strengthening conservation actions to safeguard marine biodiversity under climate change.

Habitat loss and range shifts contribute to ecological generalization among reef fishes.

Human activities are altering the structure of ecological communities, often favouring generalists over specialists. For reef fishes, increasingly degraded habitats and climate-driven range shifts may independently augment generalization, particularly if fishes with least-specific habitat requirements are more likely to shift geographic ranges to track their thermal niche. Using a unique global dataset on temperate and tropical reef fishes and habitat composition, we calculated a species generalization index that empirically estimates the habitat niche breadth of each fish species. We then applied the species generalization index to evaluate potential impacts of habitat loss and range shifts across large scales, on coral and rocky reefs. Our analyses revealed consistent habitat-induced shifts in community structure that favoured generalist fishes following regional coral mortality events and between adjacent sea urchin barrens and kelp habitats. Analysis of the distribution of tropical fishes also identified the species generalization index as the most important trait in predicting their poleward range extent, more so than body or range size. Generalist tropical reef fishes penetrate further into subtropical and temperate zones than specialists. Dynamic responses of reef fishes to habitat degradation imply loss of specialists at local scales, while generalists will be broadly favoured under intensifying anthropogenic pressures. An increased focus on individual requirements of specialists could provide useful guidance for species threat assessments and conservation actions, while ecosystem and multi-species fisheries models should recognize increasing prevalence of generalists.

Knowledge Gaps in the Biology, Ecology, and Management of the Pacific Crown-of-Thorns Sea Star Acanthaster sp. on Australia's Great Barrier Reef.

AbstractCrown-of-thorns sea stars (Acanthaster sp.) are among the most studied coral reef organisms, owing to their propensity to undergo major population irruptions, which contribute to significant coral loss and reef degradation throughout the Indo-Pacific. However, there are still important knowledge gaps pertaining to the biology, ecology, and management of Acanthaster sp. Renewed efforts to advance understanding and management of Pacific crown-of-thorns sea stars (Acanthaster sp.) on Australia's Great Barrier Reef require explicit consideration of relevant and tractable knowledge gaps. Drawing on established horizon scanning methodologies, this study identified contemporary knowledge gaps by asking active and/or established crown-of-thorns sea star researchers to pose critical research questions that they believe should be addressed to improve the understanding and management of crown-of-thorns sea stars on the Great Barrier Reef. A total of 38 participants proposed 246 independent research questions, organized into 7 themes: feeding ecology, demography, distribution and abundance, predation, settlement, management, and environmental change. Questions were further assigned to 48 specific topics nested within the 7 themes. During this process, redundant questions were removed, which reduced the total number of distinct research questions to 172. Research questions posed were mostly related to themes of demography (46 questions) and management (48 questions). The dominant topics, meanwhile, were the incidence of population irruptions (16 questions), feeding ecology of larval sea stars (15 questions), effects of elevated water temperature on crown-of-thorns sea stars (13 questions), and predation on juveniles (12 questions). While the breadth of questions suggests that there is considerable research needed to improve understanding and management of crown-of-thorns sea stars on the Great Barrier Reef, the predominance of certain themes and topics suggests a major focus for new research while also providing a roadmap to guide future research efforts.

Direct and indirect effects of heatwaves on a coral reef fishery.

Marine heatwaves are increasing in frequency and intensity, and indirectly impacting coral reef fisheries through bleaching-induced degradation of live coral habitats. Marine heatwaves also affect fish metabolism and catchability, but such direct effects of elevated temperatures on reef fisheries are largely unknown. We investigated direct and indirect effects of the devastating 2016 marine heatwave on the largest reef fishery operating along the Great Barrier Reef (GBR). We used a combination of fishery-independent underwater census data on coral trout biomass (Plectropomus and Variola spp.) and catch-per-unit-effort (CPUE) data from the commercial fishery to evaluate changes in the fishery resulting from the 2016 heatwave. The heatwave caused widespread, yet locally patchy, declines in coral cover, but we observed little effect of local coral loss on coral trout biomass. Instead, a pattern of decreasing biomass at northern sites and stable or increasing biomass at southern sites suggested a direct response of populations to the heatwave. Analysis of the fishery-independent data and CPUE found that in-water coral trout biomass estimates were positively related to CPUE, and that coral trout catch rates increased with warmer temperatures. Temperature effects on catch rates were consistent with the thermal affinities of the multiple species contributing to this fishery. Scaling-up the effect of temperature on coral trout catch rates across the region suggests that GBR-wide catches were 18% higher for a given level of effort during the heatwave year relative to catch rates under the mean temperatures in the preceding 6 years. These results highlight a potentially large effect of heatwaves on catch rates of reef fishes, independent of changes in reef habitats, that can add substantial uncertainty to estimates of stock trends inferred from fishery-dependent (CPUE) data. Overestimation of CPUE could initiate declines in reef fisheries that are currently fully exploited, and threaten sustainable management of reef stocks.

Spatial patterns of microbial communities across surface waters of the Great Barrier Reef.

Microorganisms are fundamental drivers of biogeochemical cycling, though their contribution to coral reef ecosystem functioning is poorly understood. Here, we infer predictors of bacterioplankton community dynamics across surface-waters of the Great Barrier Reef (GBR) through a meta-analysis, combining microbial with environmental data from the eReefs platform. Nutrient dynamics and temperature explained 41.4% of inter-seasonal and cross-shelf variation in bacterial assemblages. Bacterial families OCS155, Cryomorphaceae, Flavobacteriaceae, Synechococcaceae and Rhodobacteraceae dominated inshore reefs and their relative abundances positively correlated with nutrient loads. In contrast, Prochlorococcaceae negatively correlated with nutrients and became increasingly dominant towards outershelf reefs. Cyanobacteria in Prochlorococcaceae and Synechococcaceae families occupy complementary cross-shelf biogeochemical niches; their abundance ratios representing a potential indicator of GBR nutrient levels. One Flavobacteriaceae-affiliated taxa was putatively identified as diagnostic for ecosystem degradation. Establishing microbial observatories along GBR environmental gradients will facilitate robust assessments of microbial contributions to reef health and inform tipping-points in reef condition.

Modeling the distribution of a wide-ranging invasive species using the sampling efforts of expert and citizen scientists.

In its invasive range in Australia, the European rabbit threatens the persistence of native flora and fauna and damages agricultural production. Understanding its distribution and ecological niche is critical for developing management plans to reduce populations and avoid further biodiversity and economic losses.We developed an ensemble of species distribution models (SDMs) to determine the geographic range limits and habitat suitability of the rabbit in Australia. We examined the advantage of incorporating data collected by citizens (separately and jointly with expert data) and explored issues of spatial biases in occurrence data by implementing different approaches to generate pseudo-absences. We evaluated the skill of our model using three approaches: cross-validation, out-of-region validation, and evaluation of the covariate response curves according to expert knowledge of rabbit ecology.Combining citizen and expert occurrence data improved model skill based on cross-validation, spatially reproduced important aspects of rabbit ecology, and reduced the need to extrapolate results beyond the studied areas.Our ensemble model projects that rabbits are distributed across approximately two thirds of Australia. Annual maximum temperatures >25°C and annual minimum temperatures >10°C define, respectively, the southern and northern most range limits of its distribution. In the arid and central regions, close access to permanent water (≤~ 0.4 km) and reduced clay soil composition (~20%-50%) were the major factors influencing the probability of occurrence of rabbits. Synthesis and applications. Our results show that citizen science data can play an important role in managing invasive species by providing missing information on occurrences in regions not surveyed by experts because of logistics or financial constraints. The additional sampling effort provided by citizens can improve the capacity of SDMs to capture important elements of a species ecological niche, improving the capacity of statistical models to accurately predict the geographic range of invasive species.

The Australian National Rabbit Database: 50 yr of population monitoring of an invasive species.

With ongoing introductions into Australia since the 1700s, the European rabbit (Oryctolagus cuniculus) has become one of the most widely distributed and abundant vertebrate pests, adversely impacting Australia's biodiversity and agroeconomy. To understand the population and range dynamics of the species and its impacts better, occurrence and abundance data have been collected by researchers and citizens from sites covering a broad spectrum of climatic and environmental conditions in Australia. The lack of a common and accessible repository for these data has, however, limited their use in determining important spatiotemporal drivers of the structure and dynamics of the geographical range of rabbits in Australia. To meet this need, we created the Australian National Rabbit Database, which combines more than 50 yr of historical and contemporary survey data collected from throughout the range of the species in Australia. The survey data, obtained from a suite of complementary monitoring methods, were combined with high-resolution weather, climate, and environmental information, and an assessment of data quality. The database provides records of rabbit occurrence (689,265 records) and abundance (51,241 records, >120 distinct sites) suitable for identifying the spatiotemporal drivers of the rabbit's distribution and for determining spatial patterns of variation in its key life-history traits, including maximum rates of population growth. Because all data are georeferenced and date stamped, they can be coupled with information from other databases and spatial layers to explore the potential effects of rabbit occurrence and abundance on Australia's native wildlife and agricultural production. The Australian National Rabbit Database is an important tool for understanding and managing the European rabbit in its invasive range and its effects on native biodiversity and agricultural production. It also provides a valuable resource for addressing questions related to the biology, success, and impacts of invasive species more generally. No copyright or proprietary restrictions are associated with the use of this data set other than citation of this Data Paper.

Water quality mediates resilience on the Great Barrier Reef.

Threats from climate change and other human pressures have led to widespread concern for the future of Australia's Great Barrier Reef (GBR). Resilience of GBR reefs will be determined by their ability to resist disturbances and to recover from coral loss, generating intense interest in management actions that can moderate these processes. Here we quantify the effect of environmental and human drivers on the resilience of southern and central GBR reefs over the past two decades. Using a composite water quality index, we find that while reefs exposed to poor water quality are more resistant to coral bleaching, they recover from disturbance more slowly and are more susceptible to outbreaks of crown-of-thorns starfish and coral disease-with a net negative impact on recovery and long-term hard coral cover. Given these conditions, we find that 6-17% improvement in water quality will be necessary to bring recovery rates in line with projected increases in coral bleaching among contemporary inshore and mid-shelf reefs. However, such reductions are unlikely to buffer projected bleaching effects among outer-shelf GBR reefs dominated by fast-growing, thermally sensitive corals, demonstrating practical limits to local management of the GBR against the effects of global warming.

Spatial resilience of the Great Barrier Reef under cumulative disturbance impacts.

In the face of increasing cumulative effects from human and natural disturbances, sustaining coral reefs will require a deeper understanding of the drivers of coral resilience in space and time. Here we develop a high-resolution, spatially explicit model of coral dynamics on Australia's Great Barrier Reef (GBR). Our model accounts for biological, ecological and environmental processes, as well as spatial variation in water quality and the cumulative effects of coral diseases, bleaching, outbreaks of crown-of-thorns starfish (Acanthaster cf. solaris), and tropical cyclones. Our projections reconstruct coral cover trajectories between 1996 and 2017 over a total reef area of 14,780 km2 , predicting a mean annual coral loss of -0.67%/year mostly due to the impact of cyclones, followed by starfish outbreaks and coral bleaching. Coral growth rate was the highest for outer shelf coral communities characterized by digitate and tabulate Acropora spp. and exposed to low seasonal variations in salinity and sea surface temperature, and the lowest for inner-shelf communities exposed to reduced water quality. We show that coral resilience (defined as the net effect of resistance and recovery following disturbance) was negatively related to the frequency of river plume conditions, and to reef accessibility to a lesser extent. Surprisingly, reef resilience was substantially lower within no-take marine protected areas, however this difference was mostly driven by the effect of water quality. Our model provides a new validated, spatially explicit platform for identifying the reefs that face the greatest risk of biodiversity loss, and those that have the highest chances to persist under increasing disturbance regimes.

High-resolution characterization of the abiotic environment and disturbance regimes on the Great Barrier Reef, 1985-2017.

This data compilation synthesizes 36 static environmental and spatial variables, and temporally explicit modeled estimates of three major disturbances to coral cover on the Great Barrier Reef (GBR): (1) coral bleaching, (2) tropical cyclones, and (3) outbreaks of the coral-eating crown-of-thorns starfish Acanthaster cf. solaris. Data are provided on a standardized grid (0.01° × 0.01° ~ 1 × 1 km) for reef locations along the GBR, containing 15,928 pixels and excluding the northernmost sections (<12° S) where empirical data were sparse. This compilation provides a consistent and high-resolution characterization of the abiotic environment and disturbance regimes for GBR reef locations at a fine spatial scale to be used in the development of complex ecosystem models. Static estimates of environmental variables (e.g., depth, bed shear stress, average temperature, temperature variation) originally developed by the Commonwealth of Australia's Environment Research Facility (CERF) Marine Biodiversity Hub were provided by Geoscience Australia. Annual (1985-2017) disturbance estimates were either interpolated from empirical data (A. cf. solaris), predicted from proxy indicators (e.g., degree heating weeks [DHW] as a proxy for bleaching severity), or explicitly modeled (e.g., wave height model for each cyclone). This data set synthesizes some of the most recent advances in remote sensing and modeling of environmental conditions on the GBR; yet it is not exhaustive and we highlight areas that should be expanded through future research. The characterization of abiotic and disturbance regimes presented here represent an essential tool for the development of complex regional scale models of the GBR; preventing redundancy between working groups and promoting collaboration, innovation, and consistency. When using the data set, we kindly request that you cite this article and/or the articles cited in the reference section, recognizing the work that went into compiling the data together and the original authors' willingness to make it publicly available.

Outstanding Challenges in the Transferability of Ecological Models.

Predictive models are central to many scientific disciplines and vital for informing management in a rapidly changing world. However, limited understanding of the accuracy and precision of models transferred to novel conditions (their 'transferability') undermines confidence in their predictions. Here, 50 experts identified priority knowledge gaps which, if filled, will most improve model transfers. These are summarized into six technical and six fundamental challenges, which underlie the combined need to intensify research on the determinants of ecological predictability, including species traits and data quality, and develop best practices for transferring models. Of high importance is the identification of a widely applicable set of transferability metrics, with appropriate tools to quantify the sources and impacts of prediction uncertainty under novel conditions.

Challenges of transferring models of fish abundance between coral reefs.

Reliable abundance estimates for species are fundamental in ecology, fisheries, and conservation. Consequently, predictive models able to provide reliable estimates for un- or poorly-surveyed locations would prove a valuable tool for management. Based on commonly used environmental and physical predictors, we developed predictive models of total fish abundance and of abundance by fish family for ten representative taxonomic families for the Great Barrier Reef (GBR) using multiple temporal scenarios. We then tested if models developed for the GBR (reference system) could predict fish abundances at Ningaloo Reef (NR; target system), i.e., if these GBR models could be successfully transferred to NR. Models of abundance by fish family resulted in improved performance (e.g., 44.1%  0.05). High spatio-temporal variability of patterns in fish abundance at the family and population levels in both reef systems likely affected the transferability of these models. Inclusion of additional predictors with potential direct effects on abundance, such as local fishing effort or topographic complexity, may improve transferability of fish abundance models. However, observations of these local-scale predictors are often not available, and might thereby hinder studies on model transferability and its usefulness for conservation planning and management.

Why decadal to century timescale palaeoclimate data are needed to explain present-day patterns of biological diversity and change.

The current distribution of species, environmental conditions and their interactions represent only one snapshot of a planet that is continuously changing, in part due to human influences. To distinguish human impacts from natural factors, the magnitude and pace of climate shifts, since the Last Glacial Maximum, are often used to determine whether patterns of diversity today are artefacts of past climate change. In the absence of high-temporal resolution palaeoclimate reconstructions, this is generally done by assuming that past climate change occurred at a linear pace between widely spaced (usually, ≥1,000 years) climate snapshots. We show here that this is a flawed assumption because regional climates have changed significantly across decades and centuries during glacial-interglacial cycles, likely causing rapid regional replacement of biota. We demonstrate how recent atmosphere-ocean general circulation model (AOGCM) simulations of the climate of the past 21,000 years can provide credible estimates of the details of climate change on decadal to centennial timescales, showing that these details differ radically from what might be inferred from longer timescale information. High-temporal resolution information can provide more meaningful estimates of the magnitude and pace of climate shifts, the location and timing of drivers of physiological stress, and the extent of novel climates. They also produce new opportunities to directly investigate whether short-term climate variability is more important in shaping biodiversity patterns rather than gradual changes in long-term climatic means. Together, these more accurate measures of past climate instability are likely to bring about a better understanding of the role of palaeoclimatic change and variability in shaping current macroecological patterns in many regions of the world.