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.     

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.     

Investigating the causes and consequences of symbiont shuffling in a multi-partner reef coral symbiosis under environmental change

Dynamic symbioses may critically mediate impacts of climate change on diverse organisms, with repercussions for ecosystem persistence in some cases. On coral reefs, increases in heat-tolerant symbionts after thermal bleaching can reduce coral susceptibility to future stress. However, the relevance of this adaptive response is equivocal owing to conflicting reports of symbiont stability and change. We help reconcile this conflict by showing that change in symbiont community composition (symbiont shuffling) in Orbicella faveolata depends on the disturbance severity and recovery environment. The proportion of heat-tolerant symbionts dramatically increased following severe experimental bleaching, especially in a warmer recovery environment, but tended to decrease if bleaching was less severe. These patterns can be explained by variation in symbiont performance in the changing microenvironments created by differentially bleached host tissues. Furthermore, higher proportions of heat-tolerant symbionts linearly increased bleaching resistance but reduced photochemical efficiency, suggesting that any change in community structure oppositely impacts performance and stress tolerance. Therefore, even minor symbiont shuffling can adaptively benefit corals, although fitness effects of resulting trade-offs are difficult to predict. This work helps elucidate causes and consequences of dynamism in symbiosis, which is critical to predicting responses of multi-partner symbioses such as O. faveolata to environmental change.     

White-band disease and the changing face of Caribbean coral reefs

In recent decades, the cover of fleshy macroalgae has increased and coral cover has decreased on most Caribbean reefs. Coral mortality precipitated this transition, and the accumulation of macroalgal biomass has been enhanced by decreased herbivory and increased nutrient input. Populations of Acropora palmata (elkhorn coral) and A. cervicornis (staghorn coral), two of the most important framework-building species, have died throughout the Caribbean, substantially reducing coral cover and providing substratum for algal growth. Hurricanes have devastated local populations of Acropora spp. over the past 20–25 years, but white-band disease, a putative bacterial syndrome specific to the genus Acropora, has been a more significant source of mortality over large areas of the Caribbean region.Paleontological data suggest that the regional Acropora kill is without precedent in the late Holocene. In Belize, A. cervicornis was the primary ecological and geological constituent of reefs in the central shelf lagoon until the mid-1980s. After constructing reef framework for thousands of years, A. cervicornis was virtually eliminated from the area over a ten-year period. Evidence from other parts of the Caribbean supports the hypothesis of continuous Holocene accumulation and recent mass mortality of Acropora spp. Prospects are poor for the rapid recovery of A. cervicornis, because its reproductive strategy emphasizes asexual fragmentation at the expense of dispersive sexual reproduction. A. palmata also relies on fragmentation, but this species has a higher rate of sexual recruitment than A. cervicornis. If the Acropora spp. do not recover, macroalgae will continue to dominate Caribbean reefs, accompanied by increased abundances of brooding corals, particularly Agaricia spp. and Porites spp. The outbreak of white-band disease has been coincident with increased human activity, and the possibility of a causal connection should be further investigated.     

Towards modelling the future risk of cyclone wave damage to the world's coral reefs

Tropical cyclones generate extreme waves that can damage coral reef communities. Recovery typically requires up to a decade, driving the trajectory of coral community structure. Coral reefs have evolved over millennia with cyclones. Increasingly, however, processes of recovery are interrupted and compromised by additional pressures (thermal stress, pollution, diseases, predators). Understanding how cyclones interact with other pressures to threaten coral reefs underpins spatial prioritization of conservation and management interventions. Models that simulate coral responses to cumulative pressures often assume that the worst cyclone wave damage occurs within ~100 km of the track. However, we show major coral loss at exposed sites up to 800 km from a cyclone that was both strong (high sustained wind speeds >=33 m/s) and big (widespread circulation >~300 km), using numerical wave models and field data from northwest Australia. We then calculate the return time of big and strong cyclones, big cyclones of any strength and strong cyclones of any size, for each of 150 coral reef ecoregions using a global data set of past cyclones from 1985 to 2015. For the coral ecoregions that regularly were exposed to cyclones during that time, we find that 75% of them were exposed to at least one cyclone that was both big and strong. Return intervals of big and strong cyclones are already less than 5 years for 13 ecoregions, primarily in the cyclone‐prone NW Pacific, and less than 10 years for an additional 14 ecoregions. We identify ecoregions likely at higher risk in future given projected changes in cyclone activity. Robust quantification of the spatial distribution of likely cyclone wave damage is vital not only for understanding past coral response to pressures, but also for predicting how this may change as the climate continues to warm and the relative frequency of the strongest cyclones rises.     

Caribbean mesophotic coral ecosystems are unlikely climate change refugia

Deeper coral reefs experience reduced temperatures and light and are often shielded from localized anthropogenic stressors such as pollution and fishing. The deep reef refugia hypothesis posits that light‐dependent stony coral species at deeper depths are buffered from thermal stress and will avoid bleaching‐related mass mortalities caused by increasing sea surface temperatures under climate change. This hypothesis has not been tested because data collection on deeper coral reefs is difficult. Here we show that deeper (mesophotic) reefs, 30–75 m depth, in the Caribbean are not refugia because they have lower bleaching threshold temperatures than shallow reefs. Over two thermal stress events, mesophotic reef bleaching was driven by a bleaching threshold that declines 0.26 °C every +10 m depth. Thus, the main premise of the deep reef refugia hypothesis that cooler environments are protective is incorrect; any increase in temperatures above the local mean warmest conditions can lead to thermal stress and bleaching. Thus, relatively cooler temperatures can no longer be considered a de facto refugium for corals and it is likely that many deeper coral reefs are as vulnerable to climate change as shallow water reefs.     

Reef coral diversity and global change

Regional anthropogenic processes such as pollution, dredging, and overfishing on coral reefs currently threaten the biodiversity of stony corals and other reef-associated organisms. Global climate change may interact with anthropogenic processes to create additional impacts on coral diversity in the near future. In order to predict these changes, it is necessary to understand the magnitude and causes of variation in scleractinian coral diversity throughout their 240 million year history. The fossil record documents long periods of speciation in corals, interrupted repeatedly by events of mass extinction. Some of these events relate clearly to changes in global climate. Diversity in reef corals has increased since their last period of extinction at the end of the Cretaceous (65 My bp ), and is still rising. During the last 8 million years, the fragmentation of the once pantropical Tethys Sea separated corals into two major biogeographical provinces. Periods of glaciation also have caused major changes in sea level and temperature. Accumulated evidence supports the theory that relative habitat area and changing patterns of oceanic circulation are mainly responsible for the two observed centres of recent coral diversity at the western tropical margins of the Atlantic and Pacific oceans. At predicted rates of climate change in the near future, coral reefs are likely to survive as an ecosystem. Increases in sea level may actually benefit corals and lead to regional increases in diversity if new habitat area on back reefs is opened to increased water circulation and thus coral dispersal. Rising temperature may cause higher rates of coral mortality and even local extinction in isolated, small populations such as those on oceanic islands. The effects of increases in ultraviolet radiation (UV) are largely unknown, but likely to be negative. UV may damage planktonic coral propagules in oceanic surface waters and thus decrease rates of gene flow between coral populations. This may result in increased local extinctions, again with the strongest impact on widely separated reefs with small coral populations. The largest threats to coral diversity are regional anthropogenic impacts, which may interact with global climate change to exacerbate rates of local species extinctions. Centres of high reef coral diversity coincide with human population centres in south-east Asia and the Caribbean, and thus the greatest potential for species loss lies in these geographical areas.     

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.     

Elevated carbon dioxide affects behavioural lateralization in a coral reef fish

Elevated carbon dioxide (CO(2)) has recently been shown to affect chemosensory and auditory behaviour, and activity levels of larval reef fishes, increasing their risk of predation. However, the mechanisms underlying these changes are unknown. Behavioural lateralization is an expression of brain functional asymmetries, and thus provides a unique test of the hypothesis that elevated CO(2) affects brain function in larval fishes. We tested the effect of near-future CO(2) concentrations (880 μatm) on behavioural lateralization in the reef fish, Neopomacentrus azysron. Individuals exposed to current-day or elevated CO(2) were observed in a detour test where they made repeated decisions about turning left or right. No preference for right or left turns was observed at the population level. However, individual control fish turned either left or right with greater frequency than expected by chance. Exposure to elevated-CO(2) disrupted individual lateralization, with values that were not different from a random expectation. These results provide compelling evidence that elevated CO(2) directly affects brain function in larval fishes. Given that lateralization enhances performance in a number of cognitive tasks and anti-predator behaviours, it is possible that a loss of lateralization could increase the vulnerability of larval fishes to predation in a future high-CO(2) ocean.     

珊瑚礁区的生物多样性及其生态功能

珊瑚礁区生物多样性程度可以与陆地热带雨林相提并论,目前关于珊瑚礁物种多样性及其空间分布特征方面研究进展迅速,是生物多样性研究的重要基地。作为一种生态资源,珊瑚礁还具有重要的生态功能,近年来由于全球气候逐渐变暖、人类活动影响不断加剧,导致其生物多样性缩减、生态功能严重退化。珊瑚礁生态系统多样性、遗传多样性已成为珊瑚礁研究热点,珊瑚礁生态环境效应和保护管理方面的研究也越来越受到重视。我国珊瑚礁主要分布在广阔的南海海域和海南岛、台湾岛、香港和广东广西沿岸,礁区生物种类繁多,多样性程度较高,以往研究主要涉及地质、地貌、生物、环境等方面,现今和今后一段时间里迫切需要加强生物多样性和生态功能研究,以确保更有效地保护和管理珊瑚礁。     

Black reefs: iron-induced phase shifts on coral reefs

The Line Islands are calcium carbonate coral reef platforms located in iron-poor regions of the central Pacific. Natural terrestrial run-off of iron is non-existent and aerial deposition is extremely low. However, a number of ship groundings have occurred on these atolls. The reefs surrounding the shipwreck debris are characterized by high benthic cover of turf algae, macroalgae, cyanobacterial mats and corallimorphs, as well as particulate-laden, cloudy water. These sites also have very low coral and crustose coralline algal cover and are call black reefs because of the dark-colored benthic community and reduced clarity of the overlying water column. Here we use a combination of benthic surveys, chemistry, metagenomics and microcosms to investigate if and how shipwrecks initiate and maintain black reefs. Comparative surveys show that the live coral cover was reduced from 40 to 60% to <10% on black reefs on Millennium, Tabuaeran and Kingman. These three sites are relatively large (>0.75 km²). The phase shift occurs rapidly; the Kingman black reef formed within 3 years of the ship grounding. Iron concentrations in algae tissue from the Millennium black reef site were six times higher than in algae collected from reference sites. Metagenomic sequencing of the Millennium Atoll black reef-associated microbial community was enriched in iron-associated virulence genes and known pathogens. Microcosm experiments showed that corals were killed by black reef rubble through microbial activity. Together these results demonstrate that shipwrecks and their associated iron pose significant threats to coral reefs in iron-limited regions.     

Evidence for multiple stressor interactions and effects on coral reefs

Concern is growing about the potential effects of interacting multiple stressors, especially as the global climate changes. We provide a comprehensive review of multiple stressor interactions in coral reef ecosystems, which are widely considered to be one of the most sensitive ecosystems to global change. First, we synthesized coral reef studies that examined interactions of two or more stressors, highlighting stressor interactions (where one stressor directly influences another) and potentially synergistic effects on response variables (where two stressors interact to produce an effect that is greater than purely additive). For stressor‐stressor interactions, we found 176 studies that examined at least 2 of the 13 stressors of interest. Applying network analysis to analyze relationships between stressors, we found that pathogens were exacerbated by more costressors than any other stressor, with ca. 78% of studies reporting an enhancing effect by another stressor. Sedimentation, storms, and water temperature directly affected the largest number of other stressors. Pathogens, nutrients, and crown‐of‐thorns starfish were the most‐influenced stressors. We found 187 studies that examined the effects of two or more stressors on a third dependent variable. The interaction of irradiance and temperature on corals has been the subject of more research (62 studies, 33% of the total) than any other combination of stressors, with many studies reporting a synergistic effect on coral symbiont photosynthetic performance (n = 19). Second, we performed a quantitative meta‐analysis of existing literature on this most‐studied interaction (irradiance and temperature). We found that the mean effect size of combined treatments was statistically indistinguishable from a purely additive interaction, although it should be noted that the sample size was relatively small (n = 26). Overall, although in aggregate a large body of literature examines stressor effects on coral reefs and coral organisms, considerable gaps remain for numerous stressor interactions and effects, and insufficient quantitative evidence exists to suggest that the prevailing type of stressor interaction is synergistic.     

Global change and coral reefs: impacts on reefs, economies and human cultures

Coral reefs have reconstituted themselves after previous large sea-level variations, and climate changes. For the past 6000 years of unusually stable sea-level, reefs have grown without serious interruptions. During recent decades, however, new stresses threaten localized devastation of many reefs. A new period of global climate change is occurring, stimulated by anthropogenic increases in greenhouse gases. Coral reefs will cope well with predicted sea-level rises of 4.5 cm per decade, but reef islands will not. Higher sea levels will provide corals with greater room for growth across reef flats, but there are no foreseeable mechanisms for reef island growth to keep pace with sea-level rise, therefore many low islands may ultimately become uninhabitable. Climate change will introduce localized variations in weather patterns, but changes to individual reefs cannot be predicted. Reefs on average should cope well with regional climate change, as they have coped with similar previous fluctuations. Air temperature increases of 0.2–0.3 °C/decade will induce slower increases in sea-surface temperatures, which may cause localized, or regional increases in coral bleaching. Changes in rainfall will impact on reefs near land masses. Likewise, increased storms and variations in El Nino Southern Oscillation (ENSO) may stress some reefs, but not others. The greatest impact of climate change will be a synergistic enhancement of direct anthropogenic stresses (excessive sediment and pollution from the land; over-fishing, especially via destructive methods; mining of coral rock and sand; and engineering modifications), which currently cause most damage to coral reefs. Many of the world's reefs have been degraded and more will be damaged as anthropogenic impacts increase under the ‘demophoric’ increases in population (demos) and economic (phoric) activity. This biotic and habitat loss will result in severe economic and social losses. Reefs, however, have considerable recovery powers and losses can be minimized by effective management of direct human impacts and reducing indirect threats of global climate change.     

On the paradox of thriving cold-water coral reefs in the food-limited deep sea

The deep sea is amongst the most food-limited habitats on Earth, as only a small fraction (<4%) of the surface primary production is exported below 200 m water depth. Here, cold-water coral (CWC) reefs form oases of life: their biodiversity compares with tropical coral reefs, their biomass and metabolic activity exceed other deep-sea ecosystems by far. We critically assess the paradox of thriving CWC reefs in the food-limited deep sea, by reviewing the literature and open-access data on CWC habitats. This review shows firstly that CWCs typically occur in areas where the food supply is not constantly low, but undergoes pronounced temporal variation. High currents, downwelling and/or vertically migrating zooplankton temporally boost the export of surface organic matter to the seabed, creating ‘feast’ conditions, interspersed with ‘famine’ periods during the non-productive season. Secondly, CWCs, particularly the most common reef-builder Desmophyllum pertusum (formerly known as Lophelia pertusa), are well adapted to these fluctuations in food availability. Laboratory and in situ measurements revealed their dietary flexibility, tissue reserves, and temporal variation in growth and energy allocation. Thirdly, the high structural and functional diversity of CWC reefs increases resource retention: acting as giant filters and sustaining complex food webs with diverse recycling pathways, the reefs optimise resource gains over losses. Anthropogenic pressures, including climate change and ocean acidification, threaten this fragile equilibrium through decreased resource supply, increased energy costs, and dissolution of the calcium-carbonate reef framework. Based on this review, we suggest additional criteria to judge the health of CWC reefs and their chance to persist in the future.     

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.     

Vibrios dominate as culturable nitrogen-fixing bacteria of the Brazilian coral Mussismilia hispida

Taxonomic characterization was performed on the putative N₂-fixing microbiota associated with the coral species Mussismilia hispida, and with its sympatric species Palythoa caribaeorum, P. variabilis, and Zoanthus solanderi, off the coast of São Sebastião (São Paulo State, Brazil). The 95 isolates belonged to the Gammaproteobacteria according to the 16S rDNA gene sequences. In order to identify the isolates unambiguously, pyrH gene sequencing was carried out. The majority of the isolates (n=76) fell within the Vibrio core group, with the highest gene sequence similarity being towards Vibrio harveyi and Vibrio alginolyticus. Nineteen representative isolates belonging to V. harveyi (n=7), V. alginolyticus (n=8), V. campbellii (n=3), and V. parahaemolyticus (n=1) were capable of growing six successive times in nitrogen-free medium and some of them showed strong nitrogenase activity by means of the acetylene reduction assay (ARA). It was concluded that nitrogen fixation is a common phenotypic trait among Vibrio species of the core group. The fact that different Vibrio species can fix N₂ might explain why they are so abundant in the mucus of different coral species.     

Comparison of deep-water coral reefs and lithoherms off southeastern USA

Two types of deep-water coral bioherms occur off the coast of southeastern United States: Oculina and Lophelia/Enallopsammia. The deep-water Oculina bioherms form an extensive reef system at depths of 70–100 m along the shelf edge off central eastern Florida. These reefs are comprised of numerous pinnacles and ridges, 3–35 m in height. Each pinnacle is a bank of unconsolidated sediment and coral debris that is capped on the slopes and crest with living and dead colonies of Oculina varicosa, the ivory tree coral. In comparison, deep-water reefs of Lophelia pertusa and Enallopsammia profunda corals occur at depths of 500–850 m (maximum 150-m relief) along the base of the Florida-Hatteras slope in the Straits of Florida. On the western edge of the Blake Plateau off South Carolina and Georgia, 54-m high banks of Enallopsammia and Lophelia occur at depths of 490–550 m, whereas on the eastern edge of the plateau the reefs form structures 146 m in height and at depths of 640–869 m. The geomorphology and functional structure of both the Oculina and Lophelia reefs are similar. North of Little Bahama Bank, at depths of 1000–1300 m, a region of bioherms is dominated by the coral Solenosmilia sp.; Lophelia is reportedly absent. This paper summarizes 25 years of submersible studies on the deep-water Oculina reefs, describes submersible reconnaissance of deep-water Lophelia reefs off the southeastern United States, and contrasts these types of bioherms with the deep-water lithoherms in the Straits of Florida west of the Bahamas.     

Turbid reefs moderate coral bleaching under climate‐related temperature stress

Thermal‐stress events that cause coral bleaching and mortality have recently increased in frequency and severity. Yet few studies have explored conditions that moderate coral bleaching. Given that high light and high ocean temperature together cause coral bleaching, we explore whether corals at turbid localities, with reduced light, are less likely to bleach during thermal‐stress events than corals at other localities. We analyzed coral bleaching, temperature, and turbidity data from 3,694 sites worldwide with a Bayesian model and found that K_d490, a measurement positively related to turbidity, between 0.080 and 0.127 reduced coral bleaching during thermal‐stress events. Approximately 12% of the world's reefs exist within this “moderating turbidity” range, and 30% of reefs that have moderating turbidity are in the Coral Triangle. We suggest that these turbid nearshore environments may provide some refuge through climate change, but these reefs will need high conservation status to sustain them close to dense human populations.