Reserve design for uncertain responses of coral reefs to climate change

Rising sea temperatures cause mass coral bleaching and threaten reefs worldwide. We show how maps of variations in thermal stress can be used to help manage reefs for climate change. We map proxies of chronic and acute thermal stress and develop evidence-based hypotheses for the future response of corals to each stress regime. We then incorporate spatially realistic predictions of larval connectivity among reefs of the Bahamas and apply novel reserve design algorithms to create reserve networks for a changing climate. We show that scales of larval dispersal are large enough to connect reefs from desirable thermal stress regimes into a reserve network. Critically, we find that reserve designs differ according to the anticipated scope for phenotypic and genetic adaptation in corals, which remains uncertain. Attempts to provide a complete reserve design that hedged against different evolutionary outcomes achieved limited success, which emphasises the importance of considering the scope for adaptation explicitly. Nonetheless, 15% of reserve locations were selected under all evolutionary scenarios, making them a high priority for early designation. Our approach allows new insights into coral holobiont adaptation to be integrated directly into an adaptive approach to management.     

Ecosystem‐based management of coral reefs under climate change

Coral reefs provide food and livelihoods for hundreds of millions of people as well as harbour some of the highest regions of biodiversity in the ocean. However, overexploitation, land‐use change and other local anthropogenic threats to coral reefs have left many degraded. Additionally, coral reefs are faced with the dual emerging threats of ocean warming and acidification due to rising CO₂ emissions, with dire predictions that they will not survive the century. This review evaluates the impacts of climate change on coral reef organisms, communities and ecosystems, focusing on the interactions between climate change factors and local anthropogenic stressors. It then explores the shortcomings of existing management and the move towards ecosystem‐based management and resilience thinking, before highlighting the need for climate change‐ready marine protected areas (MPAs), reduction in local anthropogenic stressors, novel approaches such as human‐assisted evolution and the importance of sustainable socialecological systems. It concludes that designation of climate change‐ready MPAs, integrated with other management strategies involving stakeholders and participation at multiple scales such as marine spatial planning, will be required to maximise coral reef resilience under climate change. However, efforts to reduce carbon emissions are critical if the long‐term efficacy of local management actions is to be maintained and coral reefs are to survive.     

The threat to coral reefs from more intense cyclones under climate change

Ocean warming under climate change threatens coral reefs directly, through fatal heat stress to corals and indirectly, by boosting the energy of cyclones that cause coral destruction and loss of associated organisms. Although cyclone frequency is unlikely to rise, cyclone intensity is predicted to increase globally, causing more frequent occurrences of the most destructive cyclones with potentially severe consequences for coral reef ecosystems. While increasing heat stress is considered a pervasive risk to coral reefs, quantitative estimates of threats from cyclone intensification are lacking due to limited data on cyclone impacts to inform projections. Here, using extensive data from Australia's Great Barrier Reef (GBR), we show that increases in cyclone intensity predicted for this century are sufficient to greatly accelerate coral reef degradation. Coral losses on the outer GBR were small, localized and offset by gains on undisturbed reefs for more than a decade, despite numerous cyclones and periods of record heat stress, until three unusually intense cyclones over 5 years drove coral cover to record lows over >1500 km. Ecological damage was particularly severe in the central‐southern region where 68% of coral cover was destroyed over >1000 km, forcing record declines in the species richness and abundance of associated fish communities, with many local extirpations. Four years later, recovery of average coral cover was relatively slow and there were further declines in fish species richness and abundance. Slow recovery of community diversity appears likely from such a degraded starting point. Highly unusual characteristics of two of the cyclones, aside from high intensity, inflated the extent of severe ecological damage that would more typically have occurred over 100s of km. Modelling published predictions of future cyclone activity, the likelihood of more intense cyclones within time frames of coral recovery by mid‐century poses a global threat to coral reefs and dependent societies.     

Global inequities between polluters and the polluted: climate change impacts on coral reefs

For many ecosystem services, it remains uncertain whether the impacts of climate change will be mostly negative or positive and how these changes will be geographically distributed. These unknowns hamper the identification of regional winners and losers, which can influence debate over climate policy. Here, we use coral reefs to explore the spatial variability of climate stress by modelling the ecological impacts of rising sea temperatures and ocean acidification, two important coral stressors associated with increasing greenhouse gas (GHG) emissions. We then combine these results with national per capita emissions to quantify inequities arising from the distribution of cause (CO₂ emissions) and effect (stress upon reefs) among coral reef countries. We find pollution and coral stress are spatially decoupled, creating substantial inequity of impacts as a function of emissions. We then consider the implications of such inequity for international climate policy. Targets for GHG reductions are likely to be tied to a country's emissions. Yet within a given level of GHG emissions, our analysis reveals that some countries experience relatively high levels of impact and will likely experience greater financial cost in terms of lost ecosystem productivity and more extensive adaptation measures. We suggest countries so disadvantaged be given access to international adaptation funds proportionate with impacts to their ecosystem. We raise the idea that funds could be more equitably allocated by formally including a metric of equity within a vulnerability framework.     

Velocity of climate change algorithms for guiding conservation and management

The velocity of climate change is an elegant analytical concept that can be used to evaluate the exposure of organisms to climate change. In essence, one divides the rate of climate change by the rate of spatial climate variability to obtain a speed at which species must migrate over the surface of the earth to maintain constant climate conditions. However, to apply the algorithm for conservation and management purposes, additional information is needed to improve realism at local scales. For example, destination information is needed to ensure that vectors describing speed and direction of required migration do not point toward a climatic cul‐de‐sac by pointing beyond mountain tops. Here, we present an analytical approach that conforms to standard velocity algorithms if climate equivalents are nearby. Otherwise, the algorithm extends the search for climate refugia, which can be expanded to search for multivariate climate matches. With source and destination information available, forward and backward velocities can be calculated allowing useful inferences about conservation of species (present‐to‐future velocities) and management of species populations (future‐to‐present velocities).     

Coral adaptive capacity insufficient to halt global transition of coral reefs into net erosion under climate change

Projecting the effects of climate change on net reef calcium carbonate production is critical to understanding the future impacts on ecosystem function, but prior estimates have not included corals' natural adaptive capacity to such change. Here we estimate how the ability of symbionts to evolve tolerance to heat stress, or for coral hosts to shuffle to favourable symbionts, and their combination, may influence responses to the combined impacts of ocean warming and acidification under three representative concentration pathway (RCP) emissions scenarios (RCP2.6, RCP4.5 and RCP8.5). We show that symbiont evolution and shuffling, both individually and when combined, favours persistent positive net reef calcium carbonate production. However, our projections of future net calcium carbonate production (NCCP) under climate change vary both spatially and by RCP. For example, 19%–35% of modelled coral reefs are still projected to have net positive NCCP by 2050 if symbionts can evolve increased thermal tolerance, depending on the RCP. Without symbiont adaptive capacity, the number of coral reefs with positive NCCP drops to 9%–13% by 2050. Accounting for both symbiont evolution and shuffling, we project median positive NCPP of coral reefs will still occur under low greenhouse emissions (RCP2.6) in the Indian Ocean, and even under moderate emissions (RCP4.5) in the Pacific Ocean. However, adaptive capacity will be insufficient to halt the transition of coral reefs globally into erosion by 2050 under severe emissions scenarios (RCP8.5).     

Reduced carbon emissions and fishing pressure are both necessary for equatorial coral reefs to keep up with rising seas

A rapid increase in sea-level rise is generating vertical accommodation space on modern coral reefs. Yet increases in sea-surface temperatures (SSTs) are reducing the capacity of coral reefs to keep up with sea-level rise. We use ensemble species distribution models of four coral species (Porites rus, Porites lobata, Acropora hyacinthus and Acropora digitifera) to gauge potential geographic differences in gross carbonate production. Net carbonate production was estimated by considering erosional rates of ocean acidification, increasing cyclone intensity, local pollution, fishing pressure and the projected burdens of increases in SSTs (under Representative Concentration Pathways (RCPs) 4.5, 6.0 and 8.5) through to the year 2100. Our models predict that only 4 ± 0.1% (~60 000 km²) of Indo-Pacific coral reefs are projected to keep up with sea-level rise by the year 2100 under RCP 8.5 – most of which will be located near the Equator. However, with drastic reductions in emissions (under RCPs 4.5 and 6.0 Wm⁻²), we predict that 15 ± 0.3% (~250 000 km²) (under RCP 4.5 Wm⁻²) and 12 ± 0.7% (~200 000 km²) (under RCP 6.0 Wm⁻²) of Indo-Pacific coral reefs, have the potential to keep up with sea-level rise by the year 2100. Yet the burdens of fishing pressure and its cascading effects are projected to be responsible for substantial reef erosion, nearly halving the number of reefs able to keep up with sea-level rise. If action is taken immediately and emissions are drastically reduced to RCPs 4.5 or 6.0 Wm⁻², and reef management reduces the burdens of local pollution and fishing pressure, then our model predicts that 21–27% (~350 000–470 000 km²) of Indo-Pacific coral reefs – most of which will be located near the Equator – would have the potential to keep up with sea-level rise by the year 2100.     

Species‐specific responses to climate change and community composition determine future calcification rates of Florida Keys reefs

Anthropogenic climate change compromises reef growth as a result of increasing temperatures and ocean acidification. Scleractinian corals vary in their sensitivity to these variables, suggesting species composition will influence how reef communities respond to future climate change. Because data are lacking for many species, most studies that model future reef growth rely on uniform scleractinian calcification sensitivities to temperature and ocean acidification. To address this knowledge gap, calcification of twelve common and understudied Caribbean coral species was measured for two months under crossed temperatures (27, 30.3 °C) and CO₂ partial pressures (pCO₂) (400, 900, 1300 μatm). Mixed‐effects models of calcification for each species were then used to project community‐level scleractinian calcification using Florida Keys reef composition data and IPCC AR5 ensemble climate model data. Three of the four most abundant species, Orbicella faveolata, Montastraea cavernosa, and Porites astreoides, had negative calcification responses to both elevated temperature and pCO₂. In the business‐as‐usual CO₂ emissions scenario, reefs with high abundances of these species had projected end‐of‐century declines in scleractinian calcification of >50% relative to present‐day rates. Siderastrea siderea, the other most common species, was insensitive to both temperature and pCO₂ within the levels tested here. Reefs dominated by this species had the most stable end‐of‐century growth. Under more optimistic scenarios of reduced CO₂ emissions, calcification rates throughout the Florida Keys declined <20% by 2100. Under the most extreme emissions scenario, projected declines were highly variable among reefs, ranging 10–100%. Without considering bleaching, reef growth will likely decline on most reefs, especially where resistant species like S. siderea are not already dominant. This study demonstrates how species composition influences reef community responses to climate change and how reduced CO₂ emissions can limit future declines in reef calcification.     

基于全域连通性识别气候变化风险下的生物多样性保护优先区——以京津冀为例

在保护优先区规划中,有必要考虑气候变化的潜在风险并关注物种在气候驱动下的扩散格局。基于未来生物气候数据、地形多样性数据以及土地利用数据,应用Omniscape算法,对21世纪中叶(2040-2061年)气候变化情景下京津冀地区陆生哺乳动物的扩散进行全域连通性建模并与当前情景对比分析,识别出生物多样性保护优先区。结果表明:区域尺度下,气候变化风险使得高连通性的区域逐渐从平原向山区转移,分布趋于集中;斑块尺度下,林缘连通性较高,而位于林地或草地边缘的耕地连通性低。在此基础上,共识别生物多样性保护优先区共51786 km²,其中涵养区(占56.4%)在当前和未来的连通状况均较为良好;优化区(占38.4%)应提升生境质量以满足未来连通性的更高需求;而修复区(占5.22%)面临的气候变化风险较高,亟需进行生态修复以免在未来出现连通性夹点。本研究通过评估京津冀地区两种情景下的全域连通格局,为生物多样性保护的气候适应性规划提供了科学依据。     

Global diversity patterns of larger benthic foraminifera under future climate change

Global warming threatens the viability of tropical coral reefs and associated marine calcifiers, including symbiont-bearing larger benthic foraminifera (LBF). The impacts of current climate change on LBF are debated because they were particularly diverse and abundant during past warm periods. Studies on the responses of selected LBF species to changing environmental conditions reveal varying results. Based on a comprehensive review of the scientific literature on LBF species occurrences, we applied species distribution modeling using Maxent to estimate present-day and future species richness patterns on a global scale for the time periods 2040–2050 and 2090–2100. For our future projections, we focus on Representative Concentration Pathway 6.0 from the Intergovernmental Panel on Climate Change, which projects mean surface temperature changes of +2.2°C by the year 2100. Our results suggest that species richness in the Central Indo-Pacific is two to three times higher than in the Bahamian ecoregion, which we have identified as the present-day center of LBF diversity in the Atlantic. Our future predictions project a dramatic temperature-driven decline in low-latitude species richness and an increasing widening bimodal latitudinal pattern of species diversity. While the central Indo-Pacific, now the stronghold of LBF diversity, is expected to be most pushed outside of the currently realized niches of most species, refugia may be largely preserved in the Atlantic. LBF species will face large-scale non-analogous climatic conditions compared to currently realized climate space in the near future, as reflected in the extensive areas of extrapolation, particularly in the Indo-Pacific. Our study supports hypotheses that species richness and biogeographic patterns of LBF will fundamentally change under future climate conditions, possibly initiating a faunal turnover by the late 21st century.     

Dietary generalism accelerates arrival and persistence of coral‐reef fishes in their novel ranges under climate change

Climate change is redistributing marine and terrestrial species globally. Life‐history traits mediate the ability of species to cope with novel environmental conditions, and can be used to gauge the potential redistribution of taxa facing the challenges of a changing climate. However, it is unclear whether the same traits are important across different stages of range shifts (arrival, population increase, persistence). To test which life‐history traits most mediate the process of range extension, we used a 16‐year dataset of 35 range‐extending coral‐reef fish species and quantified the importance of various traits on the arrival time (earliness) and degree of persistence (prevalence and patchiness) at higher latitudes. We show that traits predisposing species to shift their range more rapidly (large body size, broad latitudinal range, long dispersal duration) did not drive the early stages of redistribution. Instead, we found that as diet breadth increased, the initial arrival and establishment (prevalence and patchiness) of climate migrant species in temperate locations occurred earlier. While the initial incursion of range‐shifting species depends on traits associated with dispersal potential, subsequent establishment hinges more on a species’ ability to exploit novel food resources locally. These results highlight that generalist species that can best adapt to novel food sources might be most successful in a future ocean.     

Assessing the vulnerability of an assemblage of subtropical rainforest vertebrate species to climate change in south‐east Queensland

Global climate change is a threat to ecosystems that are rich in biodiversity and endemism, such as the World Heritage‐listed subtropical rainforests of central eastern Australia. Possible effects of climate change on the biota of tropical rainforests have been studied, but subtropical rainforests have received less attention. We analysed published data for an assemblage of 38 subtropical rainforest vertebrate species in four taxonomic groups to evaluate their relative vulnerability to climate change. Focusing on endemic and/or threatened species, we considered two aspects of vulnerability: (i) resistance, defined by indicators of rarity (geographical range, habitat specificity and local abundance); and (ii) resilience, defined by indicators of a species potential to recover (reproductive output, dispersal potential and climatic niche). Our analysis indicated that frogs are most vulnerable to climate change, followed by reptiles, birds, then mammals. Many species in our assemblage are regionally endemic montane rainforest specialists with high vulnerability. Monitoring of taxa in regenerating rainforest showed that many species with high resilience traits also persisted in disturbed habitat, suggesting that they have capacity to recolonize habitats after disturbance, that is climate change‐induced events. These results will allow us to prioritize adaptation strategies for species most at risk. We conclude that to safeguard the most vulnerable amphibian, reptile and bird species against climate change, climatically stable habitats (cool refugia) that are currently without protection status need to be identified, restored and incorporated in the current reserve system. Our study provides evidence that montane subtropical rainforest deserves highest protection status as habitat for vulnerable taxa.     

Incorporating climate change adaptation into marine protected area planning

Climate change is increasingly impacting marine protected areas (MPAs) and MPA networks, yet adaptation strategies are rarely incorporated into MPA design and management plans according to the primary scientific literature. Here we review the state of knowledge for adapting existing and future MPAs to climate change and synthesize case studies (n = 27) of how marine conservation planning can respond to shifting environmental conditions. First, we derive a generalized conservation planning framework based on five published frameworks that incorporate climate change adaptation to inform MPA design. We then summarize examples from the scientific literature to assess how conservation goals were defined, vulnerability assessments performed and adaptation strategies incorporated into the design and management of existing or new MPAs. Our analysis revealed that 82% of real‐world examples of climate change adaptation in MPA planning derive from tropical reefs, highlighting the need for research in other ecosystems and habitat types. We found contrasting recommendations for adaptation strategies at the planning stage, either focusing only on climate refugia, or aiming for representative protection of areas encompassing the full range of expected climate change impacts. Recommendations for MPA management were more unified and focused on adaptative management approaches. Lastly, we evaluate common barriers to adopting climate change adaptation strategies based on reviewing studies which conducted interviews with MPA managers and other conservation practitioners. This highlights a lack of scientific studies evaluating different adaptation strategies and shortcomings in current governance structures as two major barriers, and we discuss how these could be overcome. Our review provides a comprehensive synthesis of planning frameworks, case studies, adaptation strategies and management actions which can inform a more coordinated global effort to adapt existing and future MPA networks to continued climate change.     

Avoiding a crisis of motivation for ocean management under global environmental change

Climate change and ocean acidification are altering marine ecosystems and, from a human perspective, creating both winners and losers. Human responses to these changes are complex, but may result in reduced government investments in regulation, resource management, monitoring and enforcement. Moreover, a lack of peoples’ experience of climate change may drive some towards attributing the symptoms of climate change to more familiar causes such as management failure. Taken together, we anticipate that management could become weaker and less effective as climate change continues. Using diverse case studies, including the decline of coral reefs, coastal defences from flooding, shifting fish stocks and the emergence of new shipping opportunities in the Arctic, we argue that human interests are better served by increased investments in resource management. But greater government investment in management does not simply mean more of “business‐as‐usual.” Management needs to become more flexible, better at anticipating and responding to surprise, and able to facilitate change where it is desirable. A range of technological, economic, communication and governance solutions exists to help transform management. While not all have been tested, judicious application of the most appropriate solutions should help humanity adapt to novel circumstances and seek opportunity where possible.     

Global assessment of coral bleaching and required rates of adaptation under climate change

Elevated ocean temperatures can cause coral bleaching, the loss of colour from reef‐building corals because of a breakdown of the symbiosis with the dinoflagellate Symbiodinium. Recent studies have warned that global climate change could increase the frequency of coral bleaching and threaten the long‐term viability of coral reefs. These assertions are based on projecting the coarse output from atmosphere–ocean general circulation models (GCMs) to the local conditions around representative coral reefs. Here, we conduct the first comprehensive global assessment of coral bleaching under climate change by adapting the NOAA Coral Reef Watch bleaching prediction method to the output of a low‐ and high‐climate sensitivity GCM. First, we develop and test algorithms for predicting mass coral bleaching with GCM‐resolution sea surface temperatures for thousands of coral reefs, using a global coral reef map and 1985–2002 bleaching prediction data. We then use the algorithms to determine the frequency of coral bleaching and required thermal adaptation by corals and their endosymbionts under two different emissions scenarios. The results indicate that bleaching could become an annual or biannual event for the vast majority of the world's coral reefs in the next 30–50 years without an increase in thermal tolerance of 0.2–1.0°C per decade. The geographic variability in required thermal adaptation found in each model and emissions scenario suggests that coral reefs in some regions, like Micronesia and western Polynesia, may be particularly vulnerable to climate change. Advances in modelling and monitoring will refine the forecast for individual reefs, but this assessment concludes that the global prognosis is unlikely to change without an accelerated effort to stabilize atmospheric greenhouse gas concentrations.     

Biodiversity hotspots, centres of endemicity, and the conservation of coral reefs

On land, biodiversity hotspots typically arise from concentrations of small‐range endemics. For Indo‐Pacific corals and reef fishes, however, centres of high species richness and centres of high endemicity are not concordant. Moreover ranges are not, on average, smaller inside the Central Indo‐Pacific (CI‐P) biodiversity hotspot. The disparity between richness and endemicity arises because corals and reef fishes have strongly skewed range distributions, with many species being very widespread. Consequently, the largest ranges overlap to generate peaks in species richness near the equator and the CI‐P biodiversity hotspot, with only minor contributions from endemics. Furthermore, we find no relationship between the number of coral vs. fish endemics at locations throughout the Indo‐Pacific, even though total richness of the two groups is strongly correlated. The spatial separation of centres of endemicity and biodiversity hotspots in these taxa calls for a two‐pronged management strategy to address conservation needs.