Regional and global climate risks for reef corals: Incorporating species-specific vulnerability and exposure to climate hazards.

Climate change is driving rapid and widespread erosion of the environmental conditions that formerly supported species persistence. Existing projections of climate change typically focus on forecasts of acute environmental anomalies and global extinction risks. The current projections also frequently consider all species within a broad taxonomic group together without differentiating species-specific patterns. Consequently, we still know little about the explicit dimensions of climate risk (i.e., species-specific vulnerability, exposure and hazard) that are vital for predicting future biodiversity responses (e.g., adaptation, migration) and developing management and conservation strategies. Here, we use reef corals as model organisms (n = 741 species) to project the extent of regional and global climate risks of marine organisms into the future. We characterise species-specific vulnerability based on the global geographic range and historical environmental conditions (1900-1994) of each coral species within their ranges, and quantify the projected exposure to climate hazard beyond the historical conditions as climate risk. We show that many coral species will experience a complete loss of pre-modern climate analogs at the regional scale and across their entire distributional ranges, and such exposure to hazardous conditions are predicted to pose substantial regional and global climate risks to reef corals. Although high-latitude regions may provide climate refugia for some tropical corals until the mid-21st century, they will not become a universal haven for all corals. Notably, high-latitude specialists and species with small geographic ranges remain particularly vulnerable as they tend to possess limited capacities to avoid climate risks (e.g., via adaptive and migratory responses). Predicted climate risks are amplified substantially under the SSP5-8.5 compared with the SSP1-2.6 scenario, highlighting the need for stringent emission controls. Our projections of both regional and global climate risks offer unique opportunities to facilitate climate action at spatial scales relevant to conservation and management.

Global warming and recurrent mass bleaching of corals.

During 2015-2016, record temperatures triggered a pan-tropical episode of coral bleaching, the third global-scale event since mass bleaching was first documented in the 1980s. Here we examine how and why the severity of recurrent major bleaching events has varied at multiple scales, using aerial and underwater surveys of Australian reefs combined with satellite-derived sea surface temperatures. The distinctive geographic footprints of recurrent bleaching on the Great Barrier Reef in 1998, 2002 and 2016 were determined by the spatial pattern of sea temperatures in each year. Water quality and fishing pressure had minimal effect on the unprecedented bleaching in 2016, suggesting that local protection of reefs affords little or no resistance to extreme heat. Similarly, past exposure to bleaching in 1998 and 2002 did not lessen the severity of bleaching in 2016. Consequently, immediate global action to curb future warming is essential to secure a future for coral reefs.

Research priorities for the sustainability of coral-rich western Pacific seascapes.

Nearly a billion people depend on tropical seascapes. The need to ensure sustainable use of these vital areas is recognised, as one of 17 policy commitments made by world leaders, in Sustainable Development Goal (SDG) 14 ('Life below Water') of the United Nations. SDG 14 seeks to secure marine sustainability by 2030. In a time of increasing social-ecological unpredictability and risk, scientists and policymakers working towards SDG 14 in the Asia-Pacific region need to know: (1) How are seascapes changing? (2) What can global society do about these changes? and (3) How can science and society together achieve sustainable seascape futures? Through a horizon scan, we identified nine emerging research priorities that clarify potential research contributions to marine sustainability in locations with high coral reef abundance. They include research on seascape geological and biological evolution and adaptation; elucidating drivers and mechanisms of change; understanding how seascape functions and services are produced, and how people depend on them; costs, benefits, and trade-offs to people in changing seascapes; improving seascape technologies and practices; learning to govern and manage seascapes for all; sustainable use, justice, and human well-being; bridging communities and epistemologies for innovative, equitable, and scale-crossing solutions; and informing resilient seascape futures through modelling and synthesis. Researchers can contribute to the sustainability of tropical seascapes by co-developing transdisciplinary understandings of people and ecosystems, emphasising the importance of equity and justice, and improving knowledge of key cross-scale and cross-level processes, feedbacks, and thresholds.

Emergence patterns of locally novel plant communities driven by past climate change and modern anthropogenic impacts.

Anthropogenic disturbance and climate change can result in dramatic increases in the emergence of new, ecologically novel, communities of organisms. We used a standardised framework to detect local novel communities in 2135 pollen time series over the last 25,000 years. Eight thousand years of post-glacial warming coincided with a threefold increase in local novel community emergence relative to glacial estimates. Novel communities emerged predominantly at high latitudes and were linked to global and local temperature change across multi-millennial time intervals. In contrast, emergence of locally novel communities in the last 200 years, although already on par with glacial retreat estimates, occurred at midlatitudes and near high human population densities. Anthropogenic warming does not appear to be strongly associated with modern local novel communities, but may drive widespread emergence in the future, with legacy effects for millennia after warming abates.

Projecting coral responses to intensifying marine heatwaves under ocean acidification.

Over this century, coral reefs will run the gauntlet of climate change, as marine heatwaves (MHWs) become more intense and frequent, and ocean acidification (OA) progresses. However, we still lack a quantitative assessment of how, and to what degree, OA will moderate the responses of corals to MHWs as they intensify throughout this century. Here, we first projected future MHW intensities for tropical regions under three future greenhouse gas emissions scenario (representative concentration pathways, RCP2.6, RCP4.5 and RCP8.5) for the near-term (2021-2040), mid-century (2041-2060) and late-century (2081-2100). We then combined these MHW intensity projections with a global data set of 1,788 experiments to assess coral attribute performance and survival under the three emissions scenarios for the near-term, mid-century and late-century in the presence and absence of OA. Although warming and OA had predominately additive impacts on the coral responses, the contribution of OA in affecting most coral attributes was minor relative to the dominant role of intensifying MHWs. However, the addition of OA led to greater decreases in photosynthesis and survival under intermediate and unrestricted emissions scenario for the mid- and late-century than if intensifying MHWs were considered as the only driver. These results show that role of OA in modulating coral responses to intensifying MHWs depended on the focal coral attribute and extremity of the scenario examined. Specifically, intensifying MHWs and OA will cause increasing instances of coral bleaching and substantial declines in coral productivity, calcification and survival within the next two decades under the low and intermediate emissions scenario. These projections suggest that corals must rapidly adapt or acclimatize to projected ocean conditions to persist, which is far more likely under a low emissions scenario and with increasing efforts to manage reefs to enhance resilience.

Integrating environmental variability to broaden the research on coral responses to future ocean conditions.

Our understanding of the response of reef-building corals to changes in their physical environment is largely based on laboratory experiments, analysis of long-term field data, and model projections. Experimental data provide unique insights into how organisms respond to variation of environmental drivers. However, an assessment of how well experimental conditions cover the breadth of environmental conditions and variability where corals live successfully is missing. Here, we compiled and analyzed a globally distributed dataset of in-situ seasonal and diurnal variability of key environmental drivers (temperature, pCO2 , and O2 ) critical for the growth and livelihood of reef-building corals. Using a meta-analysis approach, we compared the variability of environmental conditions assayed in coral experimental studies to current and projected conditions in their natural habitats. We found that annual temperature profiles projected for the end of the 21st century were characterized by distributional shifts in temperatures with warmer winters and longer warm periods in the summer, not just peak temperatures. Furthermore, short-term hourly fluctuations of temperature and pCO2 may regularly expose corals to conditions beyond the projected average increases for the end of the 21st century. Coral reef sites varied in the degree of coupling between temperature, pCO2 , and dissolved O2 , which warrants site-specific, differentiated experimental approaches depending on the local hydrography and influence of biological processes on the carbonate system and O2 availability. Our analysis highlights that a large portion of the natural environmental variability at short and long timescales is underexplored in experimental designs, which may provide a path to extend our understanding on the response of corals to global climate change.

The projected degradation of subtropical coral assemblages by recurrent thermal stress.

Subtropical coral assemblages are threatened by similar extreme thermal stress events to their tropical counterparts. Yet, the mid- and long-term thermal stress responses of corals in subtropical environments remain largely unquantified, limiting our capacity to predict their future viability. The annual survival, growth and recruitment of 311 individual corals within the Solitary Islands Marine Park (Australia) was recorded over a 3-year period (2016-2018), including the 2015/2016 thermal stress event. These data were used to parameterise integral projection models quantifying the effect of thermal stress within a subtropical coral assemblage. Stochastic simulations were also applied to evaluate the implications of recurrent thermal stress scenarios predicted by four different Representative Concentration Pathways. We report differential shifts in population growth rates (λ) among coral populations during both stress and non-stress periods, confirming contrasting bleaching responses among taxa. However, even during non-stress periods, the observed dynamics for all taxa were unable to maintain current community composition, highlighting the need for external recruitment sources to support the community structure. Across all coral taxa, projected stochastic growth rates (λs ) were found to be lowest under higher emissions scenarios. Correspondingly, predicted increases in recurrent thermal stress regimes may accelerate the loss of coral coverage, species diversity and structural complexity within subtropical regions. We suggest that these trends are primarily due to the susceptibility of subtropical specialists and endemic species, such as Pocillopora aliciae, to thermal stress. Similarly, the viability of many tropical coral populations at higher latitudes is highly dependent on the persistence of up-current tropical systems. As such, the inherent dynamics of subtropical coral populations appear unable to support their future persistence under unprecedented thermal disturbance scenarios.

Ecological effects of non-native species in marine ecosystems relate to co-occurring anthropogenic pressures.

Predictors for the ecological effects of non-native species are lacking, even though such knowledge is fundamental to manage non-native species and mitigate their impacts. Current theories suggest that the ecological effects of non-native species may be related to other concomitant anthropogenic stressors, but this has not been tested at a global scale. We combine an exhaustive meta-analysis of the ecological effects of marine non-native species with human footprint proxies to determine whether the ecological changes due to non-native species are modulated by co-occurring anthropogenic impacts. We found that non-native species had greater negative effects on native biodiversity where human population was high and caused reductions in individual performance where cumulative human impacts were large. On this basis we identified several marine ecoregions where non-native species may have the greatest ecological effects, including areas in the Mediterranean Sea and along the northwest coast of the United States. In conclusion, our global assessment suggests coexisting anthropogenic impacts can intensify the ecological effects of non-native species.

Geographical limits to species-range shifts are suggested by climate velocity.

The reorganization of patterns of species diversity driven by anthropogenic climate change, and the consequences for humans, are not yet fully understood or appreciated. Nevertheless, changes in climate conditions are useful for predicting shifts in species distributions at global and local scales. Here we use the velocity of climate change to derive spatial trajectories for climatic niches from 1960 to 2009 (ref. 7) and from 2006 to 2100, and use the properties of these trajectories to infer changes in species distributions. Coastlines act as barriers and locally cooler areas act as attractors for trajectories, creating source and sink areas for local climatic conditions. Climate source areas indicate where locally novel conditions are not connected to areas where similar climates previously occurred, and are thereby inaccessible to climate migrants tracking isotherms: 16% of global surface area for 1960 to 2009, and 34% of ocean for the 'business as usual' climate scenario (representative concentration pathway (RCP) 8.5) representing continued use of fossil fuels without mitigation. Climate sink areas are where climate conditions locally disappear, potentially blocking the movement of climate migrants. Sink areas comprise 1.0% of ocean area and 3.6% of land and are prevalent on coasts and high ground. Using this approach to infer shifts in species distributions gives global and regional maps of the expected direction and rate of shifts of climate migrants, and suggests areas of potential loss of species richness.

U-Th dating reveals regional-scale decline of branching Acropora corals on the Great Barrier Reef over the past century.

Hard coral cover on the Great Barrier Reef (GBR) is on a trajectory of decline. However, little is known about past coral mortality before the advent of long-term monitoring (circa 1980s). Using paleoecological analysis and high-precision uranium-thorium (U-Th) dating, we reveal an extensive loss of branching Acropora corals and changes in coral community structure in the Palm Islands region of the central GBR over the past century. In 2008, dead coral assemblages were dominated by large, branching Acropora and living coral assemblages by genera typically found in turbid inshore environments. The timing of Acropora mortality was found to be occasionally synchronous among reefs and frequently linked to discrete disturbance events, occurring in the 1920s to 1960s and again in the 1980s to 1990s. Surveys conducted in 2014 revealed low Acropora cover (<5%) across all sites, with very little evidence of change for up to 60 y at some sites. Collectively, our results suggest a loss of resilience of this formerly dominant key framework builder at a regional scale, with recovery severely lagging behind predictions. Our study implies that the management of these reefs may be predicated on a shifted baseline.

Broadening the taxonomic scope of coral reef palaeoecological studies using ancient DNA.

Marine environments face acute pressures from human impacts, often resulting in substantial changes in community structure. On the inshore Great Barrier Reef (GBR), palaeoecological studies show the collapse of the previously dominant coral Acropora from the impacts of degraded water quality associated with European colonization. Even more dramatic impacts can result in the replacement of corals by fleshy macroalgae on modern reefs, but their past distribution is unknown because they leave no fossil record. Here, we apply DNA metabarcoding and high-throughput sequencing of the 18S rDNA gene on palaeoenvironmental DNA (aeDNA) derived from sediment cores at two sites on Pandora Reef (GBR), to enhance palaeoecological studies by incorporating key soft-bodied taxa, including macroalgae. We compared temporal trends in this aeDNA record with those of coral genera derived from macrofossils. Multivariate analysis of 12 eukaryotic groups from the aeDNA community showed wide variability over the past 750 years. The occurrence of brown macroalgae was negatively correlated only with the dominant coral at both sites. The occurrence of coralline and green macroalgae was positively correlated with only the dominant coral at one of the sites, where we also observed a significant association between the whole coral community and the occurrence of each of the three macroalgae groups. Our results demonstrate that reef sediments can provide a valuable archive for understanding the past distribution and occurrence of important soft-bodied reef dwellers. Combining information from fossils and aeDNA provides an enhanced understanding of temporal changes of reefs ecosystems at decadal to millennial timescales.

Refugia under threat: Mass bleaching of coral assemblages in high-latitude eastern Australia.

Environmental anomalies that trigger adverse physiological responses and mortality are occurring with increasing frequency due to climate change. At species' range peripheries, environmental anomalies are particularly concerning because species often exist at their environmental tolerance limits and may not be able to migrate to escape unfavourable conditions. Here, we investigated the bleaching response and mortality of 14 coral genera across high-latitude eastern Australia during a global heat stress event in 2016. We evaluated whether the severity of assemblage-scale and genus-level bleaching responses was associated with cumulative heat stress and/or local environmental history, including long-term mean temperatures during the hottest month of each year (SSTLTMAX ), and annual fluctuations in water temperature (SSTVAR ) and solar irradiance (PARZVAR ). The most severely-bleached genera included species that were either endemic to the region (Pocillopora aliciae) or rare in the tropics (e.g. Porites heronensis). Pocillopora spp., in particular, showed high rates of immediate mortality. Bleaching severity of Pocillopora was high where SSTLTMAX was low or PARZVAR was high, whereas bleaching severity of Porites was directly associated with cumulative heat stress. While many tropical Acropora species are extremely vulnerable to bleaching, the Acropora species common at high latitudes, such as A. glauca and A. solitaryensis, showed little incidence of bleaching and immediate mortality. Two other regionally-abundant genera, Goniastrea and Turbinaria, were also largely unaffected by the thermal anomaly. The severity of assemblage-scale bleaching responses was poorly explained by the environmental parameters we examined. Instead, the severity of assemblage-scale bleaching was associated with local differences in species abundance and taxon-specific bleaching responses. The marked taxonomic disparity in bleaching severity, coupled with high mortality of high-latitude endemics, point to climate-driven simplification of assemblage structures and progressive homogenisation of reef functions at these high-latitude locations.

Transcending data gaps: a framework to reduce inferential errors in ecological analyses.

The analysis of functional diversity (FD) has gained increasing importance due to its generality and utility in ecology. In particular, patterns in the spatial distribution and temporal change of FD are being used to predict locations and functional groups that are immediately vulnerable to global changes. A major impediment to the accurate measurement of FD is the pervasiveness of missing data in trait datasets. While such prevalent data gaps can engender misleading inferences in FD analyses, we currently lack any practical guide to handle missing data in trait datasets. Here, we identify significant mismatches between true FD and values derived from datasets that contain missing data. We demonstrate that imputing missing data with a phylogeny-informed approach reduces the risk of misinterpretation of FD patterns, and provides baseline information against which central questions in ecology can be evaluated.

Local and regional controls of phylogenetic structure at the high-latitude range limits of corals.

Understanding how range-edge populations will respond to climate change is an urgent research priority. Here, we used a phylogenetic community ecology approach to examine how ecological and evolutionary processes shape biodiversity patterns of scleractinian corals at their high-latitude range limits in eastern Australia. We estimated phylogenetic signal in seven ecologically important functional traits and conducted tests of phylogenetic structure at local and regional scales using the net relatedness (NRI) and nearest taxon indices (NTI) for the presence/absence and abundance data. Regional tests showed light phylogenetic clustering, indicating that coral species found in this subtropical-to-temperate transition zone are more closely related to each other than are species on the nearby, more northerly Great Barrier Reef. Local tests revealed variable patterns of phylogenetic clustering and overdispersion and higher than expected phylogenetic turnover among sites. In combination, these results are broadly consistent with the hierarchical filtering model, whereby species pass through a regional climatic filter based on their tolerances for marginal conditions and subsequently segregate into local assemblages according to the relative strength of habitat filtering and species interactions. Conservatism of tested traits suggests that corals will likely track their niches with climate change. Nevertheless, high turnover of lineages among sites indicates that range shifts will probably vary among species and highlights the vulnerability and conservation significance of high-latitude reefs.

Historical spatial reconstruction of a spawning-aggregation fishery.

Aggregations of individual animals that form for breeding purposes are a critical ecological process for many species, yet these aggregations are inherently vulnerable to exploitation. Studies of the decline of exploited populations that form breeding aggregations tend to focus on catch rate and thus often overlook reductions in geographic range. We tested the hypothesis that catch rate and site occupancy of exploited fish-spawning aggregations (FSAs) decline in synchrony over time. We used the Spanish mackerel (Scomberomorus commerson) spawning-aggregation fishery in the Great Barrier Reef as a case study. Data were compiled from historical newspaper archives, fisher knowledge, and contemporary fishery logbooks to reconstruct catch rates and exploitation trends from the inception of the fishery. Our fine-scale analysis of catch and effort data spanned 103 years (1911-2013) and revealed a spatial expansion of fishing effort. Effort shifted offshore at a rate of 9.4 nm/decade, and 2.9 newly targeted FSAs were reported/decade. Spatial expansion of effort masked the sequential exploitation, commercial extinction, and loss of 70% of exploited FSAs. After standardizing for improvements in technological innovations, average catch rates declined by 90.5% from 1934 to 2011 (from 119.4 to 11.41 fish/vessel/trip). Mean catch rate of Spanish mackerel and occupancy of exploited mackerel FSAs were not significantly related. Our study revealed a special kind of shifting spatial baseline in which a contraction in exploited FSAs occurred undetected. Knowledge of temporally and spatially explicit information on FSAs can be relevant for the conservation and management of FSA species.

Ecological and methodological drivers of species' distribution and phenology responses to climate change.

Climate change is shifting species' distribution and phenology. Ecological traits, such as mobility or reproductive mode, explain variation in observed rates of shift for some taxa. However, estimates of relationships between traits and climate responses could be influenced by how responses are measured. We compiled a global data set of 651 published marine species' responses to climate change, from 47 papers on distribution shifts and 32 papers on phenology change. We assessed the relative importance of two classes of predictors of the rate of change, ecological traits of the responding taxa and methodological approaches for quantifying biological responses. Methodological differences explained 22% of the variation in range shifts, more than the 7.8% of the variation explained by ecological traits. For phenology change, methodological approaches accounted for 4% of the variation in measurements, whereas 8% of the variation was explained by ecological traits. Our ability to predict responses from traits was hindered by poor representation of species from the tropics, where temperature isotherms are moving most rapidly. Thus, the mean rate of distribution change may be underestimated by this and other global syntheses. Our analyses indicate that methodological approaches should be explicitly considered when designing, analysing and comparing results among studies. To improve climate impact studies, we recommend that (1) reanalyses of existing time series state how the existing data sets may limit the inferences about possible climate responses; (2) qualitative comparisons of species' responses across different studies be limited to studies with similar methodological approaches; (3) meta-analyses of climate responses include methodological attributes as covariates; and (4) that new time series be designed to include the detection of early warnings of change or ecologically relevant change. Greater consideration of methodological attributes will improve the accuracy of analyses that seek to quantify the role of climate change in species' distribution and phenology changes.

Effects of Elevated Temperature on the Shell Density of the Large Benthic Foraminifera Amphistegina lobifera.

This study investigated the effects of elevated temperature on shell density and Mg-ATPase activity of Amphistegina lobifera. This species is abundant in shallow reef habitats, and can be vulnerable to daily physicochemical fluctuations. To assess potential responses and acclimation mechanisms of A. lobifera to changing temperature conditions, we performed a blocked-design experiment exposing specimens collected from different reef sites (inshore and offshore) to three temperature treatments (Control: 24 °C, + 2 °C: 26 °C and + 5 °C: 29 °C) for 30 days. The final size and shell density of inshore reef foraminifera were unaffected by elevated temperature, and the enzyme activity in these individuals showed that they were able to acclimate to new temperature conditions. In contrast, offshore A. lobifera were more sensitive to changes in temperature, and heat stress caused growth impairment and inhibited Mg-ATPase activity. However, newly added chambers were not affected. These results suggested that Mg-ATPase plays an important role in regulating intracellular Mg2+ ions, but has little influence in the onset of calcification in A. lobifera. Moreover, it suggests that even though A. lobifera can regulate intracellular functions, local habitat seems to play a crucial role in determining how foraminifera respond to environmental changes.

Symbiodinium identity alters the temperature-dependent settlement behaviour of Acropora millepora coral larvae before the onset of symbiosis.

The global distribution of marine species, many of which disperse during the larval stages, is influenced by ocean temperature regimes. Here, we test how temperature and the coral symbionts (Symbiodinium) affect survival, symbiont uptake, settlement success and habitat choice of Acropora millepora larvae. Experiments were conducted at Heron Island (Australia), where larvae were exposed to 22.5, 24.5, 26.5 and 28.5°C. Within each temperature treatment, larvae were offered symbionts with distinct characteristics: (i) homologous Symbiodinium type C3, (ii) regionally homologous thermo-tolerant type D1, and (iii) heterologous thermo-tolerant type C15, as well as controls of (iv) un-filtered and (v) filtered seawater. Results show that lower instead of higher temperatures adversely affected recruitment by reducing larval survival and settlement. Low temperatures also reduced recruit habitat choice and initial symbiont densities, both of which impact on post-settlement survival. At lower temperatures, larvae increasingly settle away from preferred vertical surfaces and not on crustose coralline algae (CCA). Surprisingly, substrate preference to CCA was modified by the presence of specific symbiont genotypes that were present ex-hospite (outside the coral larvae). When different symbionts were mixed, the outcomes were non-additive, indicating that symbiont interactions modify the response. We propose that the observed influence of ex-hospite symbionts on settlement behaviour may have evolved through ecological facilitation and the study highlights the importance of biological processes during coral settlement.

Ocean acidification induces biochemical and morphological changes in the calcification process of large benthic foraminifera.

Large benthic foraminifera are significant contributors to sediment formation on coral reefs, yet they are vulnerable to ocean acidification. Here, we assessed the biochemical and morphological impacts of acidification on the calcification of Amphistegina lessonii and Marginopora vertebralis exposed to different pH conditions. We measured growth rates (surface area and buoyant weight) and Ca-ATPase and Mg-ATPase activities and calculated shell density using micro-computer tomography images. In A. lessonii, we detected a significant decrease in buoyant weight, a reduction in the density of inner skeletal chambers, and an increase of Ca-ATPase and Mg-ATPase activities at pH 7.6 when compared with ambient conditions of pH 8.1. By contrast, M. vertebralis showed an inhibition in Mg-ATPase activity under lowered pH, with growth rate and skeletal density remaining constant. While M. vertebralis is considered to be more sensitive than A. lessonii owing to its high-Mg-calcite skeleton, it appears to be less affected by changes in pH, based on the parameters assessed in this study. We suggest difference in biochemical pathways of calcification as the main factor influencing response to changes in pH levels, and that A. lessonii and M. vertebralis have the ability to regulate biochemical functions to cope with short-term increases in acidity.