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.     

Extinction vulnerability of coral reef fishes

With rapidly increasing rates of contemporary extinction, predicting extinction vulnerability and identifying how multiple stressors drive non-random species loss have become key challenges in ecology. These assessments are crucial for avoiding the loss of key functional groups that sustain ecosystem processes and services. We developed a novel predictive framework of species extinction vulnerability and applied it to coral reef fishes. Although relatively few coral reef fishes are at risk of global extinction from climate disturbances, a negative convex relationship between fish species locally vulnerable to climate change vs. fisheries exploitation indicates that the entire community is vulnerable on the many reefs where both stressors co-occur. Fishes involved in maintaining key ecosystem functions are more at risk from fishing than climate disturbances. This finding is encouraging as local and regional commitment to fisheries management action can maintain reef ecosystem functions pending progress towards the more complex global problem of stabilizing the climate.     

Ocean acidification and warming will lower coral reef resilience

Ocean warming and acidification from increasing levels of atmospheric CO₂ represent major global threats to coral reefs, and are in many regions exacerbated by local‐scale disturbances such as overfishing and nutrient enrichment. Our understanding of global threats and local‐scale disturbances on reefs is growing, but their relative contribution to reef resilience and vulnerability in the future is unclear. Here, we analyse quantitatively how different combinations of CO₂ and fishing pressure on herbivores will affect the ecological resilience of a simplified benthic reef community, as defined by its capacity to maintain and recover to coral‐dominated states. We use a dynamic community model integrated with the growth and mortality responses for branching corals (Acropora) and fleshy macroalgae (Lobophora). We operationalize the resilience framework by parameterizing the response function for coral growth (calcification) by ocean acidification and warming, coral bleaching and mortality by warming, macroalgal mortality by herbivore grazing and macroalgal growth via nutrient loading. The model was run for changes in sea surface temperature and water chemistry predicted by the rise in atmospheric CO₂ projected from the IPCC's fossil‐fuel intensive A1FI scenario during this century. Results demonstrated that severe acidification and warming alone can lower reef resilience (via impairment of coral growth and increased coral mortality) even under high grazing intensity and low nutrients. Further, the threshold at which herbivore overfishing (reduced grazing) leads to a coral–algal phase shift was lowered by acidification and warming. These analyses support two important conclusions: Firstly, reefs already subjected to herbivore overfishing and nutrification are likely to be more vulnerable to increasing CO₂. Secondly, under CO₂ regimes above 450–500 ppm, management of local‐scale disturbances will become critical to keeping reefs within an Acropora‐rich domain.     

Climate warming, marine protected areas and the ocean-scale integrity of coral reef ecosystems

Coral reefs have emerged as one of the ecosystems most vulnerable to climate variation and change. While the contribution of a warming climate to the loss of live coral cover has been well documented across large spatial and temporal scales, the associated effects on fish have not. Here, we respond to recent and repeated calls to assess the importance of local management in conserving coral reefs in the context of global climate change. Such information is important, as coral reef fish assemblages are the most species dense vertebrate communities on earth, contributing critical ecosystem functions and providing crucial ecosystem services to human societies in tropical countries. Our assessment of the impacts of the 1998 mass bleaching event on coral cover, reef structural complexity, and reef associated fishes spans 7 countries, 66 sites and 26 degrees of latitude in the Indian Ocean. Using Bayesian meta-analysis we show that changes in the size structure, diversity and trophic composition of the reef fish community have followed coral declines. Although the ocean scale integrity of these coral reef ecosystems has been lost, it is positive to see the effects are spatially variable at multiple scales, with impacts and vulnerability affected by geography but not management regime. Existing no-take marine protected areas still support high biomass of fish, however they had no positive affect on the ecosystem response to large-scale disturbance. This suggests a need for future conservation and management efforts to identify and protect regional refugia, which should be integrated into existing management frameworks and combined with policies to improve system-wide resilience to climate variation and change.     

New directions in coral reef microbial ecology

Microbial processes largely control the health and resilience of coral reef ecosystems, and new technologies have led to an exciting wave of discovery regarding the mechanisms by which microbial communities support the functioning of these incredibly diverse and valuable systems. There are three questions at the forefront of discovery: What mechanisms underlie coral reef health and resilience? How do environmental and anthropogenic pressures affect ecosystem function? What is the ecology of microbial diseases of corals? The goal is to understand the functioning of coral reefs as integrated systems from microbes and molecules to regional and ocean‐basin scale ecosystems to enable accurate predictions of resilience and responses to perturbations such as climate change and eutrophication. This review outlines recent discoveries regarding the microbial ecology of different microenvironments within coral ecosystems, and highlights research directions that take advantage of new technologies to build a quantitative and mechanistic understanding of how coral health is connected through microbial processes to its surrounding environment. The time is ripe for natural resource managers and microbial ecologists to work together to create an integrated understanding of coral reef functioning. In the context of long‐term survival and conservation of reefs, the need for this work is immediate.     

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.     

海洋酸化对珊瑚礁生态系统的影响研究进展

目前,大气CO2浓度的升高已导致海水pH值比工业革命前下降了约0.1,海水碳酸盐平衡体系随之变化,进而影响珊瑚礁生态系统的健康。近年来的研究表明海洋酸化导致造礁石珊瑚幼体补充和群落恢复更加困难,造礁石珊瑚和其它造礁生物(Reef-building organisms)钙化率降低甚至溶解,乃至影响珊瑚礁鱼类的生命活动。虽然海洋酸化对造礁石珊瑚光合作用的影响不显著,但珊瑚-虫黄藻共生体系会受到一定影响。建议选择典型海区进行长期系统监测,结合室内与原位模拟试验,从个体、种群、群落到系统不同层面,运用生理学和分子生物学技术,结合生态学研究手段,综合研究珊瑚的相应响应,以期深入认识海洋酸化对珊瑚礁生态系统健康(例如珊瑚白化)的影响及其效应。     

Could some coral reefs become sponge reefs as our climate changes?

Coral reefs across the world have been seriously degraded and have a bleak future in response to predicted global warming and ocean acidification (OA). However, this is not the first time that biocalcifying organisms, including corals, have faced the threat of extinction. The end‐Triassic mass extinction (200 million years ago) was the most severe biotic crisis experienced by modern marine invertebrates, which selected against biocalcifiers; this was followed by the proliferation of another invertebrate group, sponges. The duration of this sponge‐dominated period far surpasses that of alternative stable‐ecosystem or phase‐shift states reported on modern day coral reefs and, as such, a shift to sponge‐dominated reefs warrants serious consideration as one future trajectory of coral reefs. We hypothesise that some coral reefs of today may become sponge reefs in the future, as sponges and corals respond differently to changing ocean chemistry and environmental conditions. To support this hypothesis, we discuss: (i) the presence of sponge reefs in the geological record; (ii) reported shifts from coral‐ to sponge‐dominated systems; and (iii) direct and indirect responses of the sponge holobiont and its constituent parts (host and symbionts) to changes in temperature and pH. Based on this evidence, we propose that sponges may be one group to benefit from projected climate change and ocean acidification scenarios, and that increased sponge abundance represents a possible future trajectory for some coral reefs, which would have important implications for overall reef functioning.     

Resilience in reef‐building corals: The ecological and evolutionary importance of the host response to thermal stress

Coral reefs are under extreme threat due to a number of stressors, but temperature increases due to changing climate are the most severe. Rising ocean temperatures coupled with local extremes lead to extensive bleaching, where the coral‐algal symbiosis breaks down and corals may die, compromising the structure and function of reefs. Although the symbiotic nature of the coral colony has historically been a focus of research on coral resilience, the host itself is a foundational component in the response to thermal stress. Fixed effects in the coral host set trait baselines through evolutionary processes, acting on many loci of small effect to create mosaics of thermal tolerance across latitudes and individual coral reefs. These genomic differences can be strongly heritable, producing wide variation among clones of different genotypes or families of a specific larval cross. Phenotypic plasticity is overlaid on these baselines and a growing body of knowledge demonstrates the potential for acclimatization of reef‐building corals through a variety of mechanisms that promote resilience and stress tolerance. The long‐term persistence of coral reefs will require many of these mechanisms to adjust to warmer temperatures within a generation, bridging the gap to reproductive events that allow recombination of standing diversity and adaptive change. Business‐as‐usual climate scenarios will probably lead to the loss of some coral populations or species in the future, so the interaction between intragenerational effects and evolutionary pressure is critical for the survival of reefs.     

Building resilience into practical conservation: identifying local management responses to global climate change in the southern Great Barrier Reef

Climate change is now considered the greatest long-term threat to coral reefs, with some future change inevitable despite mitigation efforts. Managers must therefore focus on supporting the natural resilience of reefs, requiring that resilient reefs and reef regions be identified. We develop a framework for assessing resilience and trial it by applying the framework to target management responses to climate change on the southern Great Barrier Reef. The framework generates a resilience score for a site based on the evaluation of 19 differentially weighted indicators known or thought to confer resilience to coral reefs. Scores are summed, and sites within a region are ranked in terms of (1) their resilience relative to the other sites being assessed, and (2) the extent to which managers can influence their resilience. The framework was applied to 31 sites in Keppel Bay of the southern Great Barrier Reef, which has a long history of disturbance and recovery. Resilience and ‘management influence potential’ were both found to vary widely in Keppel Bay, informing site selection for the staged implementation of resilience-based management strategies. The assessment framework represents a step towards making the concept of resilience operational to reef managers and conservationists. Also, it is customisable, easy to teach and implement and effective in building support among local communities and stakeholders for management responses to climate change.     

Modelling Coral Reef Futures to Inform Management: Can Reducing Local-Scale Stressors Conserve Reefs under Climate Change?

Climate change has emerged as a principal threat to coral reefs, and is expected to exacerbate coral reef degradation caused by more localised stressors. Management of local stressors is widely advocated to bolster coral reef resilience, but the extent to which management of local stressors might affect future trajectories of reef state remains unclear. This is in part because of limited understanding of the cumulative impact of multiple stressors. Models are ideal tools to aid understanding of future reef state under alternative management and climatic scenarios, but to date few have been sufficiently developed to be useful as decision support tools for local management of coral reefs subject to multiple stressors. We used a simulation model of coral reefs to investigate the extent to which the management of local stressors (namely poor water quality and fishing) might influence future reef state under varying climatic scenarios relating to coral bleaching. We parameterised the model for Bolinao, the Philippines, and explored how simulation modelling can be used to provide decision support for local management. We found that management of water quality, and to a lesser extent fishing, can have a significant impact on future reef state, including coral recovery following bleaching-induced mortality. The stressors we examined interacted antagonistically to affect reef state, highlighting the importance of considering the combined impact of multiple stressors rather than considering them individually. Further, by providing explicit guidance for management of Bolinao''s reef system, such as which course of management action will most likely to be effective over what time scales and at which sites, we demonstrated the utility of simulation models for supporting management. Aside from providing explicit guidance for management of Bolinao''s reef system, our study offers insights which could inform reef management more broadly, as well as general understanding of reef systems.     

Opposite latitudinal gradients in projected ocean acidification and bleaching impacts on coral reefs

Coral reefs and the services they provide are seriously threatened by ocean acidification and climate change impacts like coral bleaching. Here, we present updated global projections for these key threats to coral reefs based on ensembles of IPCC AR5 climate models using the new Representative Concentration Pathway (RCP) experiments. For all tropical reef locations, we project absolute and percentage changes in aragonite saturation state (Ωarag) for the period between 2006 and the onset of annual severe bleaching (thermal stress >8 degree heating weeks); a point at which it is difficult to believe reefs can persist as we know them. Severe annual bleaching is projected to start 10–15 years later at high‐latitude reefs than for reefs in low latitudes under RCP8.5. In these 10–15 years, Ωarag keeps declining and thus any benefits for high‐latitude reefs of later onset of annual bleaching may be negated by the effects of acidification. There are no long‐term refugia from the effects of both acidification and bleaching. Of all reef locations, 90% are projected to experience severe bleaching annually by 2055. Furthermore, 5% declines in calcification are projected for all reef locations by 2034 under RCP8.5, assuming a 15% decline in calcification per unit of Ωarag. Drastic emissions cuts, such as those represented by RCP6.0, result in an average year for the onset of annual severe bleaching that is ~20 years later (2062 vs. 2044). However, global emissions are tracking above the current worst‐case scenario devised by the scientific community, as has happened in previous generations of emission scenarios. The projections here for conditions on coral reefs are dire, but provide the most up‐to‐date assessment of what the changing climate and ocean acidification mean for the persistence of coral reefs.     

Positive genetic associations among fitness traits support evolvability of a reef‐building coral under multiple stressors

Climate change threatens organisms in a variety of interactive ways that requires simultaneous adaptation of multiple traits. Predicting evolutionary responses requires an understanding of the potential for interactions among stressors and the genetic variance and covariance among fitness‐related traits that may reinforce or constrain an adaptive response. Here we investigate the capacity of Acropora millepora, a reef‐building coral, to adapt to multiple environmental stressors: rising sea surface temperature, ocean acidification, and increased prevalence of infectious diseases. We measured growth rates (weight gain), coral color (a proxy for Symbiodiniaceae density), and survival, in addition to nine physiological indicators of coral and algal health in 40 coral genets exposed to each of these three stressors singly and combined. Individual stressors resulted in predicted responses (e.g., corals developed lesions after bacterial challenge and bleached under thermal stress). However, corals did not suffer substantially more when all three stressors were combined. Nor were trade‐offs observed between tolerances to different stressors; instead, individuals performing well under one stressor also tended to perform well under every other stressor. An analysis of genetic correlations between traits revealed positive covariances, suggesting that selection to multiple stressors will reinforce rather than constrain the simultaneous evolution of traits related to holobiont health (e.g., weight gain and algal density). These findings support the potential for rapid coral adaptation under climate change and emphasize the importance of accounting for corals’ adaptive capacity when predicting the future of coral reefs.     

Spatial Resilience of Coral Reefs

There have been several earlier studies that addressed the influence of natural disturbance regimes on coral reefs. Humans alter natural disturbance regimes, introduce new stressors, and modify background conditions of reefs. We focus on how coral reef ecosystems relate to disturbance in an increasingly human-dominated environment. The concept of ecosystem resilience—that is, the capacity of complex systems with multiple stable states to absorb disturbance, reorganize, and adapt to change—is central in this context. Instead of focusing on the recovery of certain species and populations within disturbed sites of individual reefs, we address spatial resilience—that is, the dynamic capacity of a reef matrix to reorganize and maintain ecosystem function following disturbance. The interplay between disturbance and ecosystem resilience is highlighted. We begin the identification of spatial sources of resilience in dynamic seascapes and exemplify and discuss the relation between “ecological memory” (biological legacies, mobile link species, and support areas) and functional diversity for seascape resilience. Managing for resilience in dynamic seascapes not only enhances the likelihood of conserving coral reefs, it also provides insurance to society by sustaining essential ecosystem services. Received 25 February 2000; accepted 31 January 2001.     

Vulnerability of the Great Barrier Reef to climate change and local pressures

Australia's Great Barrier Reef (GBR) is under pressure from a suite of stressors including cyclones, crown‐of‐thorns starfish (COTS), nutrients from river run‐off and warming events that drive mass coral bleaching. Two key questions are: how vulnerable will the GBR be to future environmental scenarios, and to what extent can local management actions lower vulnerability in the face of climate change? To address these questions, we use a simple empirical and mechanistic coral model to explore six scenarios that represent plausible combinations of climate change projections (from four Representative Concentration Pathways, RCPs), cyclones and local stressors. Projections (2017–2050) indicate significant potential for coral recovery in the near‐term, relative to current state, followed by climate‐driven decline. Under a scenario of unmitigated emissions (RCP8.5) and business‐as‐usual management of local stressors, mean coral cover on the GBR is predicted to recover over the next decade and then rapidly decline to only 3% by year 2050. In contrast, a scenario of strong carbon mitigation (RCP2.6) and improved water quality, predicts significant coral recovery over the next two decades, followed by a relatively modest climate‐driven decline that sustained coral cover above 26% by 2050. In an analysis of the impacts of cumulative stressors on coral cover relative to potential coral cover in the absence of such impacts, we found that GBR‐wide reef performance will decline 27%–74% depending on the scenario. Up to 66% of performance loss is attributable to local stressors. The potential for management to reduce vulnerability, measured here as the mean number of years coral cover can be kept above 30%, is spatially variable. Management strategies that alleviate cumulative impacts have the potential to reduce the vulnerability of some midshelf reefs in the central GBR by 83%, but only if combined with strong mitigation of carbon emissions.     

Beyond corals and fish: the effects of climate change on noncoral benthic invertebrates of tropical reefs

Climate change is threatening tropical reefs across the world, with most scientists agreeing that the current changes in climate conditions are occurring at a much faster rate than in the past and are potentially beyond the capacity of reefs to adapt and recover. Current research in tropical ecosystems focuses largely on corals and fishes, although other benthic marine invertebrates provide crucial services to reef systems, with roles in nutrient cycling, water quality regulation, and herbivory. We review available information on the effects of environmental conditions associated with climate change on noncoral tropical benthic invertebrates, including inferences from modern and fossil records. Increasing sea surface temperatures may decrease survivorship and increase the developmental rate, as well as alter the timing of gonad development, spawning, and food availability. The broad latitudinal distribution and associated temperature ranges of several pantropical taxa suggest that some reef communities may have an in‐built adaptive capacity. Tropical benthic invertebrates will also show species‐specific sublethal and lethal responses to sea‐level rise, ocean acidification, physical disturbance, runoff, turbidity, sedimentation, and changes in ocean circulation. In order to accurately predict a species' response to these stressors, we must consider the magnitude and duration of exposure to each stressor, as well as the physiology, mobility, and habitat requirements of the species. Stressors will not act independently, and many organisms will be exposed to multiple stressors concurrently, including anthropogenic stressors. Environmental changes associated with climate change are linked to larger ecological processes, including changes in larval dispersal and recruitment success, shifts in community structure and range extensions, and the establishment and spread of invasive species. Loss of some species will trigger economic losses and negative effects on ecosystem function. Our review is intended to create a framework with which to predict the vulnerability of benthic invertebrates to the stressors associated with climate change, as well as their adaptive capacity. We anticipate that this review will assist scientists, managers, and policy‐makers to better develop and implement regional research and management strategies, based on observed and predicted changes in environmental conditions.     

珊瑚礁生态脆弱性评价--以泰国思仓岛为例

珊瑚礁生态系统受到环境变化、人类活动等各种因素的严重威胁,保护珊瑚礁生态系统是目前全球海洋生态保护的热点,对珊瑚礁开展定量的生态脆弱性评估能够为保护管理对策的制定提供重要科学依据。本研究选取泰国思仓岛作为研究区域,结合空间分析技术建立了具有通用性的珊瑚礁生态脆弱性评估方法。基于ESA模型构建了珊瑚礁生态脆弱性综合指数和评价指标体系,系统分析了思仓岛珊瑚礁脆弱性的来源、构成,并直观展现了脆弱性的区域空间分布。结果表明:思仓岛研究区东北侧的珊瑚礁生态脆弱性大于西南侧,当地珊瑚礁的关键影响因子分别为驳船排污、港口码头、水体透明度等。根据脆弱性评价的结果,提出了当地珊瑚礁保护与修复的空间分区管理对策。本研究为印度-太平洋区系珊瑚礁生态脆弱性评价提供了可行的示例,也为中国的珊瑚礁可持续管理研究提供了借鉴和参照。     

Ocean warming and acidification have complex interactive effects on the dynamics of a marine fungal disease

Diseases threaten the structure and function of marine ecosystems and are contributing to the global decline of coral reefs. We currently lack an understanding of how climate change stressors, such as ocean acidification (OA) and warming, may simultaneously affect coral reef disease dynamics, particularly diseases threatening key reef-building organisms, for example crustose coralline algae (CCA). Here, we use coralline fungal disease (CFD), a previously described CCA disease from the Pacific, to examine these simultaneous effects using both field observations and experimental manipulations. We identify the associated fungus as belonging to the subphylum Ustilaginomycetes and show linear lesion expansion rates on individual hosts can reach 6.5 mm per day. Further, we demonstrate for the first time, to our knowledge, that ocean-warming events could increase the frequency of CFD outbreaks on coral reefs, but that OA-induced lowering of pH may ameliorate outbreaks by slowing lesion expansion rates on individual hosts. Lowered pH may still reduce overall host survivorship, however, by reducing calcification and facilitating fungal bio-erosion. Such complex, interactive effects between simultaneous extrinsic environmental stressors on disease dynamics are important to consider if we are to accurately predict the response of coral reef communities to future climate change.     

Marine reserves help coastal ecosystems cope with extreme weather

Natural ecosystems have experienced widespread degradation due to human activities. Consequently, enhancing resilience has become a primary objective for conservation. Nature reserves are a favored management tool, but we need clearer empirical tests of whether they can impart resilience. Catastrophic flooding in early 2011 impacted coastal ecosystems across eastern Australia. We demonstrate that marine reserves enhanced the capacity of coral reefs to withstand flood impacts. Reserve reefs resisted the impact of perturbation, whilst fished reefs did not. Changes on fished reefs were correlated with the magnitude of flood impact, whereas variation on reserve reefs was related to ecological variables. Herbivory and coral recruitment are critical ecological processes that underpin reef resilience, and were greater in reserves and further enhanced on reserve reefs near mangroves. The capacity of reserves to mitigate external disturbances and promote ecological resilience will be critical to resisting an increased frequency of climate‐related disturbance.