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The coral conservation crisis: interacting local and global stressors reduce reef resiliency and create challenges for conservation solutions

• Review Paper
• Open access
• Published: 12 February 2021
• Volume 3 , article number  312 , ( 2021 )

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• Alexandra M. Good   ORCID: orcid.org/0000-0003-2561-8248 1 &
• Keisha D. Bahr 1  

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Coral reefs are one of the most productive and biodiverse ecosystems in the world. Humans rely on these coral reef ecosystems to provide significant ecological and economic resources; however, coral reefs are threatened by numerous local and global anthropogenic factors that cause significant environmental change. The interactions of these local and global human impacts may increase the rate of coral reef degradation. For example, there are many local influences (i.e., sedimentation and submarine groundwater discharge) that may exacerbate coral bleaching and mortality. Therefore, researchers and resource managers cannot limit their narratives and actions to mitigating a sole stressor. With the continued increase in greenhouse gas emissions, management strategies and restoration techniques need to account for the scale at which environmental change occurs. This review aims to outline the various local and global anthropogenic stressors threatening reef resiliency and address the recent disagreements surrounding present-day conservation practices. Unfortunately, there is no one solution to preserve and restore all coral reefs. Each coral reef region is challenged by numerous interactive stressors that affect its ecosystem response, recovery, and services in various ways. This review discusses, while global reef degradation occurs, local solutions should be implemented to efficiently protect the coral reef ecosystem services that are valuable to marine and terrestrial environments.

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1 Status of coral reefs

Reef-building corals have existed for over 200 million years, preserving through few challenges in the Holocene, but are now facing new, human-induced challenges in Anthropocene [ 1 , 2 , 3 ]. In the Holocene (11,000 years ago), reefs were resilient, experiencing rapid recovery and prevalence of acroporids; however, since transitioning into the Anthropocene, reef systems have lost resilience as disturbances increased in frequency and duration [ 4 , 5 , 6 ]. The importance of the diverse scleractinian family Acroporidae in providing extensive structurally complex habitat across the Indo-Pacific and their dramatic loss observed across the Caribbean makes them a sensitive but important taxon to study under global climate change patterns [ 7 ]. Reefs in the Anthropocene have shifted to more dynamic and patchier reef systems where stressors are not purely additive but are interacting in more complex ways [ 8 ].

Over the last 3 decades, living coral cover has declined roughly 53% in the Western Atlantic, 40% in the Indo-Pacific, and 50% on the Great Barrier Reef (GBR) [ 9 , 10 ]. These declines in live coral cover are accompanied by a loss in structural complexity resulting in alterations in trophic structure and reductions in ecosystem services [ 11 ]. Globally, 39% of reefs are classified as low risk, and 52% of those reefs are found in the Pacific [ 12 ]. Overall, coral reefs in the Central Pacific experience lower rates of decline than those in the Atlantic, Indian, and Southeast-Asian Pacific oceans [ 12 ]. Therefore, understanding these drivers' relative influence, local and global, is vital in assessing mechanisms for managing and protecting coral reef systems and reducing secondary stressors during repeated marine heatwaves that cause coral bleaching [ 13 ].

While it is estimated that 6% of reefs across the globe will not be affected by either local or global stressors, 11% of reefs will be threatened solely by global factors alone, 22% solely from local factors, and 61% from the combined effects of local and global drivers of environmental change [ 14 ]. Globally, ocean warming and acidification are compromising carbonate accretion of coral reefs, resulting in less diverse reef communities [ 15 , 16 ]. Highly complex coral architecture is relied upon by a diverse array of marine organisms; therefore, reduction in complexity of reefs has severe consequences for biodiversity, ecosystem functioning, and environmental services [ 17 ]. Locally, human impacts (i.e., pollution, coastal development, dredging, tourism, etc.) are causing dramatic phase shifts from coral-dominated to algal-dominated systems [ 18 , 19 , 20 , 21 ]. Some of these factors of environmental changes are co-occurring, potentially amplifying coral reef decline, and creating cascading effects for coral reef organisms and human populations who rely on the reefs for many ecosystem services [ 22 ].

The ongoing, rapid transformation of coral reefs creates challenges for conservation and management strategies due to a growing spatial mismatch between the scale of threats and planned responses. Additionally, coral reefs are not solely challenged by a single stressor. The various local, anthropogenic factors degrading reefs exacerbate the global effects of warming and acidification [ 8 ]. Global climate change has profound implications on reef health; however, the potential synergies between climate, human pressure, and biogeochemical factors must be alleviated for successful restoration and rehabilitation. The interactions between multiple stressors can be defined as synergistic (the combined effects exceed their individual effects), additive (the combined effect is equal to the sum of their individual effects), or antagonistic (the combined effect is less than the additive) [ 8 , 23 ]. The ongoing increase of local and global threats on coral reefs highlights a critical gap in our knowledge of how these stressors may interact and shape future coral reefs [ 24 ]. Therefore, there is a need to reform management and conservation strategies that combat both local and global drivers of environmental change.

Coral reef status and resilience can be location-specific due to interactions of localized environmental stressors. For example, in Hawaiʻi, it has been suggested that regional management of multiple factors will benefit fish biomass and coral resistance to elevated temperatures [ 25 , 26 , 27 , 28 ]. In the Philippines, reefs have experienced a continued decline in hard coral cover over the past three decades, not solely due to the third global bleaching event (2014–2017) [ 29 ]. In Malaysia, coral reefs that contained high levels of live coral cover (> 25 colonies) were geographically isolated and experienced less coastal development and human activity [ 30 ], highlighting the importance of land use management practices. Across the Western Caribbean, four decades of coastal development has significantly reduced coral cover (15–20% in most regions). In turn, these reefs experienced increased fleshy macroalgae and herbivorous fish abundance, particularly between 2006 and 2016 [ 31 ]. In the Florida Keys, a 30-year study suggests that local nutrient enrichment and discharge from the Everglades contributes to eutrophication that has exacerbated coral stress and decline [ 32 ]. Results of this long-term monitoring suggest a balanced nitrogen to phosphorus (N:P) stoichiometry ratio would reduce the risk of coral bleaching disease and mortality in the future [ 32 ]. The disease occurrence on key coral species in the 1970s ( Acropora spp.) and 2004 ( Orbicella spp.) was linked to an increase of climate change impacts, including the intensity and frequency of hurricanes within the same regions. While climate stressors play a role, reef status and coral cover decline trends were significantly impacted at sites with increased coastal development and human-induced pollution [ 33 ]. Globally, there have been documented synergies between different environmental changes (i.e., anthropogenic stress, bleaching events, disease outbreaks, and hurricane damage) driving coral decline [ 4 ].

2 Global impacts

Projected increases in carbon dioxide (CO 2 ) over the next 50 years will exceed the conditions coral reefs have survived over the past half-million years [ 15 ]. The industrial revolution has led to rapid increases in atmospheric greenhouse gas emissions, which have caused dramatic shifts in environmental conditions [ 34 ]. In particular, global changes in ocean chemistry and sea surface temperatures have promoted significant ecological decline in coral reef ecosystems [ 35 , 36 , 37 ]. In response, the 2015 Paris Agreement was developed to globally manage greenhouse gas emissions, which is vital for coral reefs' persistence [ 38 ]. Without radically reducing carbon emissions, the ocean is predicted to be 1–3 °C warmer, 0.2 pH units more acidic, and up to 1 m higher by 2050 [ 39 ].

2.1 Ocean warming

Corals worldwide live between 1 and 2 °C below their maximum summer temperature [ 40 ]. As the ocean continues to warm, corals are being pushed into their upper lethal temperature tolerances [ 41 ]. The resulting coral stress response includes the breakdown in the symbiosis between the coral host and its algal symbiont, commonly referred to as coral bleaching [ 36 ]. Other extreme changes in environmental conditions (e.g., irradiance, salinity sedimentation) can also cause coral bleaching; however, there has been an increase in the frequency and severity of mass coral bleaching events that are linked to increases in ocean temperatures [ 4 , 36 ]. Additionally, coral bleaching events can be episodic and can coincide with ocean–atmosphere phenomena, such as El Niño-Southern Oscillation (ENSO) events [ 42 ]. To date, there have been three global bleaching events from 2014 to 2017 [ 43 ]. The number of areas (~ 6%) that have previously escaped bleaching will decrease each year as the potential for bleaching and mortality increases with or without ENSO events [ 42 ]. Examining recovery and adaptation rates of various reef systems over time has proved that bleaching events are likely to become chronic stress in the coming decades. Consequently, many coral communities will not recover quickly enough to maintain stable, coral-covered communities [ 44 ].

Before the third global coral bleaching event (2014–2017), many “low risk reefs” were situated in Australian waters [ 12 , 43 ]. One year following the 2016 bleaching event, these reefs experienced large reductions (51%) in live coral cover, but recovery varied by region due to functional changes in the coral and fish community compositions [ 45 ]. The reefs in the northern half of the GBR were severely impacted (40%) [ 12 , 45 ]. Community-wide trophic restructuring, specifically fish that scrape algae from reef surfaces, reduces competition between stressed corals and algae overgrowth and is critical for reef-scale recovery from bleaching [ 45 ].

Ocean warming has devastating effects on reef systems across the globe, regardless of protection or isolation. No reef is safe from the unprecedented rate of warming. Hawaiʻi suffered in 2014 and 2015 with 90% bleaching and 50% mortality due to elevated sea surface temperatures. The documented mortality from the warm water events was greater than documented mortality due to visitor trampling [ 46 ]. Even the most remote reef ecosystems, such as the Papahānaumokuākea Marine National Monument (PMNM), have suffered significant mortality levels from elevated sea surface temperatures [ 47 ]. Although the PMNM has a higher latitude and is far from human pollution and overfishing, historical satellite data confirmed the 2014 bleaching event exposed corals to heat stress that has increased significantly since 1982, confirming the continued, growing threat of climate change [ 47 ]. Similar widespread bleaching event scenarios have occurred on reef systems in the Coral Sea and the Gulf of Mexico that were previously known to be isolated and protected [ 48 , 49 ]. A Coral Sea study showed that after the third global bleaching event, bleaching was less severe compared to other reefs across the globe, indicating that isolation cannot provide refuge from bleaching, but low nutrient levels, high wave energy, and proximity to deeper cooler water can allow reefs to be more resistant to mortality [ 48 ].

Alongside bleaching, thermal anomalies cause shifts in the coral microbiome by increasing viral production, which in return increases the carbon and nitrogen flux in the water column and benthos, and enhances rates of coral disease and mortality [ 50 ]. This viral production triggers a positive feedback loop that enhances coral decline. White syndrome, a common disease affecting Pacific reef-building corals, is exacerbated by thermal anomalies on reefs with > 50% coral cover [ 51 ]. This same disease was recorded dramatically reducing the abundance of Acropora palmata and Acropora cervicornis in the Caribbean. Moreover, data from the GBR supports the detrimental temperature-disease hypothesis while also implying that disease transmission is rapid on healthy reefs where coral cover is high, putting healthy reefs at high risk as warm temperature anomalies increase [ 51 , 52 ]. Stony Coral Tissue Loss Disease (SCTLD), first occurring at high levels in 2014 along the Florida reef tract and coinciding with summer bleaching events, has since rapidly spread through Caribbean reefs causing unprecedented declines [ 53 ]. Using long-term data, there was no SCTLD prevalence in the Mexican Caribbean region before 2018, concluding that the disease was able to spread through the entire region within a few months, severely changing reef community structure [ 54 ]. While these diseases are decimating reefs at rapid rates, research has shown reefs containing high densities of coral feeding chaetodontid butterflyfish, from white band disease in the Philippines' to SCTLD in the Florida Keys, has positive correlations with disease prevalence [ 55 , 56 ]. This suggests that stable, healthy reefs with functionally diverse fish abundances may ameliorate the impact of coral disease [ 55 , 56 ].

2.2 Ocean acidification

Nearly 30% of the atmospheric CO 2 emissions dissolve into the ocean. As CO 2 dissociates, it releases hydrogen ions and increases the acidity of the seawater. This increase in the acidity of the ocean, ocean acidification, has several impacts on the marine environment [ 34 , 57 , 58 ]. Corals secrete calcium carbonate skeletons to maintain the ecologically important three-dimensional reef matrix. A change in ocean chemistry affects the shallow, sunlit, alkaline waters corals need to build and sustain their reef structure that provides habitat for many organisms and protects shorelines from bioerosion and storm damage [ 35 , 59 ].

While ongoing changes in ocean chemistry directly influences coral physiology and accretion, it is difficult to quantify the rate at which ocean acidification is degrading reefs due to a lack of data at large spatial, temporal, and biogeochemical scales. Most acidification studies are conducted on single species, therefore, results are difficult to forecast across ecologically relevant scales [ 58 ]. Additionally, there are many assumptions and large discrepancies in coral reef response to ocean acidification [ 58 ]. For example, biogeochemical feedback in the open ocean could buffer some effects of acidification; therefore, we must understand this potential feedback and discrepancies to accurately predict the impact of acidification on coral reefs [ 60 ]. Also, reef-associated structure, location, hydrodynamics, and biogeochemical processes may vary across reefs and should be considered when calculating net community calcification rates [ 61 ].

2.3 Sea level rise

As atmospheric CO 2 concentrations increase and our planet continues to warm, ice sheets are melting, causing sea level fluctuations worldwide. In the twenty-first century alone, global sea surface levels are predicted to rise 2 m, creating considerable alterations in coastal shoreline morphology with larger implications (20%) in tropical and subtropical habitats [ 62 ]. Low-lying coral atolls are of immediate concern; as the climate continues to change, atolls will be subject to wave-driven flooding and fluctuations in freshwater availability as the reef platforms change [ 63 , 64 ]. Since the last glacial maximum (30,000 years ago), geologic records from the GBR suggest that the reef has been more resilient to sea-level rise and warming temperatures but was highly affected by increased sediment input [ 65 ]. While historical sea-level rise forces a landward migration of shallow-reef habitats, the GBR transitioned from a fringing to a barrier reef system [ 65 ]. Although there is evidence that coral reefs can transition as sea level rises, the uncertainty comes from the additive effects of a continued increase in carbon emissions and fishing pressures that prevent reefs from keeping up with rises in sea level expected by 2100 [ 66 ].

The structural complexity and integrity of coral reefs supports millions of people worldwide through coastal protection from storm damage and flooding. Coral reefs serve as natural barriers that protect nearly 200 million people worldwide from coastal flooding hazards and associated flooding risk costs (~ $0.8 million km −1 of reef); however, it is predicted that coastal communities are at greater risk if reef structural complexity is not maintained than if sea level continues to rise [ 64 ]. The vertical accretion and variation in topographic complexity, along with local rates of sea-level rise, will determine wave height and sediment transport damage. Nonetheless, the wave energy dissipation is determinant on complexity rather than sea level [ 3 ]. Future projections indicate that coral reef erosion rates will exceed accretion rates due to unprecedented global climate change, thereby increasing the risk and associated costs of coastal flooding [ 16 , 67 ]. Current water depths have increased past predicted levels for the year 2100, and regional-scale degradation of coral reefs due to sea-level rise puts many coastal communities in danger [ 68 ]. In conclusion, there is no singular solution to combatting global climate change and the negative impacts it has on coral reef ecosystems and the communities that rely on them. As humans continue to amplify greenhouse gas emissions and atmospheric carbon dioxide concentrations, coral reefs will become increasingly vulnerable [ 69 ].

3 Local impacts

While global stressors independently affect 11% of reefs worldwide, twice as many (22%) coral reefs are impacted by local impacts. Local disturbances (i.e., water quality, sedimentation, human use, fishing pressure) may potentially influence coral reef responses to and recovery from climatic threats [ 32 ]. However, the potential of local action to offset global consequences on coral reefs is relatively unknown because it is difficult to assess across ecological scales in an experimental setting. Therefore, it becomes increasingly important to implement management and monitoring strategies that document the interaction of local and global drivers of environmental change to identify potential mitigation strategies [ 14 ]. The primary sources of human-induced impacts result from land-use change and terrestrial runoff, which have increased sedimentation and eutrophication on nearshore coral reefs [ 70 ]. Documentation dating back to the 1970s shows many areas are impacted by multiple local impacts and experiencing extensive coral mortality [ 70 , 71 ]. The reduction of resilience in each area is highly location specific and depends on the type, duration, and magnitude of that impact, local environmental conditions, and overall ecosystem resiliency [ 72 , 73 , 74 ].

3.1 Human use: tourism and coastal development

Local anthropogenic stressors increase in number, severity, and frequency simultaneously with increasing human population densities [ 21 ]. Excess tourism and urban development such as land-use change, sedimentation, untreated sewage discharge, physical damage, and pollution are significant environmental stress sources for corals and coral reefs. Although physical space for development in coastal areas is limited, state governments and commercial companies continue to support urban development, increasing environmental stress on corals [ 75 ]. Although coral reef-based tourism is crucial for economic benefits, if degradation continues, socioeconomic services will decline and threaten many reef-dependent sectors of that society [ 76 ].

Coral reef-related tourism generates revenues in over 100 countries across the globe [ 77 ]. In the United States, the National Ocean and Atmospheric Administration (NOAA) estimated the total economic value of coral reef services to be over USD 3.4 billion [ 78 ]. In the Coral Triangle, marine tourism contributes to 36% of the overall tourism market; however, 85% of reefs in the region are threatened by local human activity [ 79 ]. Coral reef ecosystems in Hawaiʻi are estimated at USD 360 million a year, acting as an asset that supports many goods and services [ 80 ]. Many people rely on coral reefs for food, identity, and wealth in the Dominican Republic [ 81 ]. However, alongside the benefits of coral reef-related tourism comes significant impacts on the adjacent coral reefs. A health assessment of local reefs in the Dominican Republic has revealed significant nutrient-based pollution, human-related structural damage, and overfishing that increases coral bleaching, mortality, and disease abundance. Therefore, the Dominican Republic has implemented sustainable, land-based, and marine management practices through ecotourism to sustain economic growth [ 81 ]. Likewise, urgent action is necessary to maintain coral reefs on the GBR. Tourism operators have begun acting as stewards to engage their guests on climate change threats and how they can take action to protect the GBR [ 82 ]. While Australia and other countries attempt to educate their tourists on environmentally conscious actions, the stress from increasing human impact has decoupled biophysical relationships in coral reefs, causing dominant species to shift due to human-induced selective pressure [ 83 , 84 ].

Land alteration and coastal development influence several cascading effects that cause perturbations and environmental change within the nearshore coral reef environment. Land-based sediment smothers corals, inhibiting them from receiving adequate light for photosynthesis, and triggers physiological stress that hinders coral recruitment, growth, and other ecosystem services [ 85 , 86 , 87 ]. Severe sedimentation due to harbor construction caused dramatic ecological declines in Pelekane Bay, Hawaiʻi [ 87 ]. Nonetheless, recovery and stabilization of coral cover was attributed to reduced sedimentation from watershed restoration [ 87 ]. While recovery is possible, certain taxonomic groups of corals have different thresholds of sediment exposure, including concentration, duration, and frequency; therefore, coral community composition may be determined by species-specific sediment tolerance thresholds [ 88 ]. Alongside coastal development, sediment exposure is amplified from dredging activity and has both synergistic and antagonistic effects with thermal stress from global climate change [ 89 ]. For example, a long-term coral health monitoring survey was conducted before, during, and after a 530-day dredging project in Barrow Island in Western Australia. This dredging project coincided with a warm water coral bleaching event. The data revealed that suspended sediment had both positive and negative effects on corals during the period of warm water. Under low sediment loads, the cumulative impact of sediment load and thermal stress was antagonistic, but the combined stressors were synergistic [ 89 , 90 ]. As uncontrolled human pressure continues to have a detrimental effect on coral cover, land to sea management is essential to enhance reef protection and resiliency [ 89 , 91 ]. The interplay between multiple local and global stressors is not well understood, thereby creating management responses to individual stressors at the community level challenging [ 73 ]. In many regions, the cumulative stressors from increased human populations do not receive the attention they require [ 73 ]. It is suggested that cumulative impact assessments are the best way to plan conservation strategies to mitigate the effects of coastal development and global climate change [ 31 , 73 ].

Since early settlement, human use and disturbance have disrupted the unique physical, chemical, and biological features of coral reef ecosystems. In Kāneʻohe Bay, Hawaiʻi, a well-documented coral reef ecosystem, anthropogenic disturbance began with the first European settlers in 1778. By the 1960s, the coastal reefs were devastated by extensive dredging, increased sewage discharge, and excess sedimentation, leading to a loss in coral cover [ 26 ]. A reconstruction of the social–ecological relationships in Hawaiian coral reef systems over the past 700 years showed that reefs were able to recover from human impacts when the stressors were reduced over long periods (decades+) and over large spatial scales (> entire island systems or regions) [ 92 ]. To this day, across the Hawaiian Archipelago, there is a strong gradient of human impact on fish assemblages and hard coral cover with a few remote areas with small human populations acting as a refuge for fisheries production and biodiversity functioning [ 93 ]. A land to sea management technique in West Maui improved coastal water quality through reducing sediment runoff and cesspool effluent, overall enhancing snorkeling experience [ 94 , 95 ]. Similarly, in Brazil, strategic management actions helped protect refugee areas from stressors (i.e., fishing intensity, land-based activities, coastal development) [ 73 ]. These joint integrated land to sea management efforts are the interplay of multiple stressors.

3.2 Pollution

Nearly 25% of coral reefs around the world are threatened by agricultural pollutants [ 96 ]. Agriculture is a highly erosive process that passes sediment, inorganic and organic nutrients, and other human contaminants to waterways leading to the ocean and ultimately vulnerable reefs [ 96 , 97 , 98 ]. Poor watershed management and land-based runoff have been found to cause eutrophication, defined as the excessive richness of nutrients, which creates a dense growth of plant life and an overall decline of oxygen [ 96 , 99 ]. On coral reefs, eutrophication can cause excessive growth of algae and the suffocation of coral reefs due to a lack of oxygen and being outcompeted for resources by the macroalgae whose growth is being supported by the excessive rich nutrient source [ 75 , 96 ].

Along with agricultural pollution, sewage effluent is another major source of human pollution, posing significant risks to coral reefs [ 96 ]. Sewage pollution sources include domestic and industrial wastewater and urban development from tourism and residential activities. Many coastal communities with fringing coral reef ecosystems, such as Puakō in the Hawaiʻi, rely on cesspools, septic tanks, or aerobic/anaerobic sewage treatments that contribute significantly to the decline in coral reefs [ 100 ]. Septic tank location and corresponding sewage pollution aggregates along the coastline, through the surface and benthic waters, increasing fecal indicator bacteria (FIB) and nutrient concentrations that contribute to harmful levels of eutrophication [ 100 , 101 ]. A study on the effects of increased, wastewater-derived nutrients found that increases in sewage nutrient enrichment from hotel seepage pits could be responsible for lowering coral reef resilience leading to higher degradation rates at heavily affected sites [ 75 ]. Human derived sewage, primarily from increased tourism, creates inshore water enrichment from urban wastewater nutrient sources and has led to a reduction in benthic coral reef health and rugosity [ 59 , 75 ]. It is believed that nutrient-enriched waters from sewage-derived sources are a major local stressor responsible for threatening coral reef ecosystems by reducing their resilience and stability [ 75 ].

With the global decline of coral reef ecosystems and a global increase in human populations along coastal areas, there have been management pushes to support wastewater treatment that will protect coral reefs in high-risk areas. Sewage and nitrogen pollution in Hawaiʻi not only led to decreased coral calcification and reproduction but was also a dominant driver in reef fish biomass changes, altering ecosystem function [ 102 ]. In the Florida Keys, the local and regional variability of nitrogen enrichment increased the risk of coral bleaching, mortality, and disease under temperature stress [ 32 ]. Numerous studies confirm that appropriate wastewater treatment would mitigate local eutrophication and, in response, increase reef refugia areas by 28% across the globe, giving reefs time while climate change is addressed at a global scale [ 14 , 25 ].

3.3 Fishing pressure

Fishing, combined with other localized human drivers, leads to changes in fish biomass and is used as a direct indicator of reef health status and human disturbance level [ 103 ]. Pollution, fishing, and habitat drivers led to an overall decrease in 45% of total fish biomass over 10 years (2008–2018) on the west coast of Hawaiʻi [ 28 ]; however, regional management of these multiple factors could benefit fish functional groups. For example, a ban on scuba spearfishing and fishing nets increased grazer populations after a year of management. This confirmed that both recreational and commercial fishing are negatively affecting fish populations, but consistent management will aid in recovery [ 28 , 66 , 104 ]. Additionally, several areas across the Main Hawaiian Islands still support high standing fish stocks, which can be refugia for maintaining fisheries resources [ 93 ]. A decline in fish stocks can be attributed to numerous interactive factors, such as nutrient pollution and overfishing [ 104 ]. Therefore, management strategies should be implemented (e.g., quantifying fish biomass) to sustain the reefs and the livelihoods of the communities that rely on them [ 105 ]. In conclusion, the global decline of reefs is caused by two categories of localized human threats: overfishing and coastal development [ 106 ]. Managers must re-examine these threats and create risk assessments to effectively allocate resources and protect coral reefs for generations to come.

4 Actionable science advancements

There is a critical knowledge gap regarding how to deal with these multiple stressors that are causing various environmental changes and a growing need for them to be managed at multiple scales across different regulatory agencies. The increase in the severity and frequency of marine heatwaves challenges conventional management strategies [ 59 , 107 ]. Therefore, there is a critical need to re-assess restoration and management strategies to sustain coral reef ecosystems under these continuing challenging conditions [ 108 ]. The global coral reef degradation that has occurred over the last 30–40 years has shifted coral reef resilience and therefore requires focused science and management efforts to prevent the loss of valuable social, ecological, and cultural resources [ 109 ].

This section discusses (1) advances in science through assisted evolution, (2) creating risk assessments through collaboration with local communities, scientists, managers, and policymakers, and (3) focused management strategies that can be technically and economically achieved (Fig.  1 ). We aim to synthesize actionable, science-based solutions and collaborations that could benefit the future of coral reefs and the communities that rely on them.

A synthesis of actionable, science-based solutions (assisted evolution, risk assessments, and focused management strategies) that regulatory agencies can utilize when addressing the multiple, interacting stressors driving coral reef decline

4.1 Advances in science

Science advancements have shifted to promote coral reef resilience through an adaptation-focused intervention that will account for a suite of multiple stressors [ 57 , 108 ]. Assisted evolution, the acceleration of evolutionary processes through the enhancement of specific traits, includes four mechanisms to increase environmental stress tolerance: (1) epigenetic programming and exposing adult colonies to high levels of environmental stress, (2) manipulation of the microbes associated with the coral holobiont, (3) culturing coral-associated endosymbiotic algae ( Symbiodinium spp.) under future environmental conditions to increase bleaching resistance, or (4) selective breeding of the coral host itself (Fig.  1 ) [ 38 , 110 ].

Adaptive actions and restoration techniques could address various environmental change drivers, but all stressor interactions and environmental alterations must be considered when analyzing the emergent ecological effects [ 57 ]. New interventions, such as genetic engineering, could be added to the coral reef restoration toolbox, but there are challenges in managing risks and uncertainties (Fig.  1 ) [ 108 ]. Therefore, while advances in science are important to consider when making a restoration plan, it is imperative to create a risk assessment outlining all possible options, consequences, uncertainties, and trade-offs to fully understand the goals and objectives in the short and long-term [ 111 ].

4.2 Creating risk assessments

The structured decision-making framework, created by Anthony et al., 2020, can help develop a management plan for high-risk ecosystems or watersheds [ 108 ]. This framework allows for the creation of a risk-assessment that integrates both local and global management efforts (Fig.  1 ). For example, the GBR has had approximately 40% coral cover decline on inshore reefs adjacent to human influence and requires a management plan that addresses local and global anthropogenic impacts [ 21 ]. Of the funding allocated to threats harming the reefs, some are used inadequately and can be why change or mitigation is not happening quickly (Fig.  1 ) [ 106 ]. It is essential to continue to work towards mitigating local factors because local threats to corals add to the effects seen by global threats and may inhibit recovery [ 32 ]. Creating a strategic plan for long-term conservation allows for clear guidelines and strategic investing (Fig.  1 ) [ 39 ]. A risk assessment can also be useful in less vulnerable, more protected reefs, which can be a conservation investment and help to repopulate degraded reefs in the climate becomes stabilized [ 39 , 112 ].

The carbon emissions crisis has been globally recognized in the Paris Climate agreement; however, the goals are ambitious, and if achieved, coral reefs are still predicted to decline by 70–90% across the globe [ 112 ]. However, not all reefs, or species of coral, are at equal risk of global climate change. Coral reefs vary in resilience, defined as the net effect of resistance and recovery following a disturbance [ 113 ]. Predicting tipping points to environmental change is common in complex environmental systems, like coral reefs, when there are changes in climate, land-use, biodiversity, and biogeochemical cycles (Fig.  1 ) [ 114 ]. Therefore, strategic management of local factors through risk-sensitivity planning can improve the long-term conservation and persistence of coral reefs under climate pressure [ 39 ]. Studies from Kāneʻohe Bay, Hawaiʻi, previously under immense anthropogenic pressure from the 1930s to the 1970s, showed that different species have different pH, temperature, and sediment tolerances [ 115 , 116 , 117 ]. On the GBR, spatial resilience was determined by water quality levels and could inform strategic planning for future conservation goals [ 113 ]. A similar risk assessment was conducted in the Maldives to assess resilience by depth and confirmed bleaching events were too frequent and delayed reef recovery. Therefore, reducing local pressure was suggested to be the only effective way to improve resilience to thermal stress [ 118 ]. Resilience can vary region–region [ 19 ], reef–reef [ 113 ], and species–species [ 1 ]. It is imperative to understand multiple responses to both natural and anthropogenic change when conducting assessing management responses (Fig.  1 ) [ 119 ].

Modeling thermal thresholds and environmental influence is an effective way to understand past and future responses to human impact across larger spatial gradients (Fig.  1 ). In Japan, coral bleaching events were recorded from 2004 to 2016 and revealed multiple factors contributing to bleaching, including a selection of thermal indices and multiple environmental influences [ 120 ]. The coral mortality and bleaching output (COMBO) model was created as a tool to calculate the impact of increased greenhouse gas emissions and sea surface temperature on local and regional scales [ 121 ]. In the past decade, advancements are now developing more complex ways in which human impacts disrupt and degrade coral reef ecosystem function [ 83 ]. Quantifying the types of human impacts and their severity across our gradient would likely improve future interpretation of the spatial patterns on the benthic cover [ 83 ]. However, more information about the types of human impacts occurring across our large spatial gradient is required to predict “social–ecological macroecology” accurately [ 122 ]. Simulation modeling in the Philippines concluded that increased local water quality management and less management designated to fishing would significantly impact future reef state. The stressors examined interacted antagonistically; therefore, highlighting the importance of combining multiple stressors in a simulation model for supporting management (Fig.  1 ) [ 119 ]. In Karimunjawa National Park, Indonesia, a multivariate statistical model was applied to examine community composition changes and concluded that water quality management across the park is critical to improving resiliency [ 123 ]. Lastly, statistical models were used to investigate various coral taxa's responses to local stressors and climate variability in the Red Sea. This model concluded that fishing pressure and eutrophication's synergistic interactions exacerbated the impact of climate change [ 22 ]. While policymakers rely on models to predict regional climatic changes, they are non-linear in nature and often contain a high level of uncertainty [ 124 ]. Therefore, reliable multivariate models must have a well-monitored design and detailed calibration method [ 124 , 125 ]. Modeling and incorporating multiple environmental variables that are both natural and human-induced environmental change allows for management and policy to be focused and science-based, improving resiliency of reef communities to future climatic events (Fig.  1 ).

4.3 Focused management strategies

There are several benefits to implementing focused management strategies that can assess benthic composition status and trends to mitigate local factors [ 126 ]. It is essential to consider local factors in management strategies because they play a role in resiliency to global climate change (Fig.  1 ) [ 21 ]. For example, when synthesizing multiple stressor interactions, it was concluded that managing sedimentation and nutrient loading could reduce coral bleaching [ 8 ]. To reduce regional threats, managers and other governance authorities should consider a holistic approach [ 119 ]. Management efforts should not focus on restoring historical baseline assemblages but should instead adapt to support natural recovery processes and embrace new and evolving conditions on a reef (Fig.  1 ) [ 127 ]. Ecosystem governance needs to shift to a new paradigm that embraces rapid change due to the unprecedented global heatwaves from 2014 to 2017 and continued anthropogenic pressures [ 128 ].

The suggested themes to improve governance in complex ecosystems are to address proximal and distal drivers, reduce those drivers' levels, and weaken positive feedback responses contributing to degradation [ 128 ]. It is also suggested for coral reefs to prioritize areas that demonstrate fewer bleaching signs than predicted by degree heating weeks recorded in that area [ 129 ]. Over the long term, those are the reefs that may be more resilient to thermal stress [ 129 ]. Spatial prioritization is also important when implementing marine protected areas (MPAs) (Fig.  1 ) [ 130 ]. Along with providing refuge to corals from human impact (i.e., tourism, fishing, etc.), the systematic conservation planning of an MPA allows for larval connectivity that self-sustains coral and reef fish recruitment (Fig.  1 ) [ 71 , 131 ]. For example, zoning was implemented in the GBR protected areas to regulate the overexploitation of valuable resources [ 130 , 132 ]. There needs to be a fundamental restructuring of institutional governance towards planetary stewardship to navigate the Anthropocene and capitalize on sustainable ecosystem management across the globe. Sustainable development and collaboration needs to be accelerated to mitigate and adapt to the planet's current and future transformations [ 133 ].

Recent developments of resilience-based management (RBM) plans aim to sustain the natural reef processes that support valuable ecological and social systems in a localized area, rather than focusing on global climate disturbances such as bleaching events (Fig.  1 ). RBM highlights reducing local pollution sources, protecting diversity, and maintaining connectivity pathways on reefs to adapt to change while simultaneously supporting resilience [ 127 ]. Apart from ecological disturbances, various socioeconomic factors can transform coral reef communities [ 134 ]. Participatory planning should be promoted to increase social acceptance and strengthen conservation strategies by considering the community's social and cultural characteristics [ 134 , 135 ]. Management strategies that foster social adaptive capacity are better fit to address the complex changes in coastal marine socio-ecological systems, such as coral reefs, and should be accompanied by cost–benefit analysis to secure incomes, livelihoods and food security benefits for coastal communities (Fig.  1 ) [ 136 , 137 ].

These collaborative, proactive management strategies are crucial for coral reef persistence because prevention is more effective and efficient than repair after the damage is done [ 138 ]. Even the GBR, one of the most well-managed systems, has lost a significant percentage of live coral color [ 9 ]. Therefore, it is crucial to pursue ecosystem-based management that is adaptive to fully understand the ecological processes that maintain coral reefs at large scales (Fig.  1 ) [ 12 ]. Ecosystem-based management can combat climate change by reducing local anthropogenic stressors and highlighting human-assisted evolution for change-ready MPAs [ 139 ]. With climate-induced coral bleaching being the main threat to coral reefs, it is important that management focus on how reefs respond to and recover from these devastating events. Predicting these regime shifts and identifying critical thresholds will guide managers through reef-specific management and adaptation tools (Fig.  1 ) [ 140 ]. Alongside predicting stress tolerances and thresholds, management of coral reef ecosystems will benefit from integrated land to sea models and scenario planning that includes human-induced change (Fig.  1 ). Planning strategies need to ensure the local human impacts will be minimized to assist in coral reef recovery under the future projected climate change impacts. Awareness of natural resources has led many local communities to implement place-based management enclosures and sustainable practices [ 141 ]. This place-based management strategy aims to reduce human impacts on coral reefs in a changing climate (Fig.  1 ) [ 141 ]. Overall, while managers and decision-makers attempt to create management strategies to mitigate global environmental change and its impact on reefs, there is still a research gap surrounding the assessment of the different strategies being utilized to understand the trade-offs and synergies [ 69 ]. Collaboration and cooperation across countries to re-organize the scientific research surrounding coral reef management is crucial to ensure science-based solutions lead to coral reef protection moving forward through the Anthropocene.

5 The path forward

Multiple environmental stressors significantly impact coral reefs. There is a global disparity in reef resilience across the globe; therefore, their persistence depends on conservation and management strategies specific to impacts experienced within that ecosystem [ 8 , 19 ]. Therefore, local and regional managers should work together to mitigate the effects of climate change based on local conditions and responses [ 22 , 121 ]. For example, large declines in reef populations across the Hawaiian Archipelago raised concerns of dangerous levels of overfishing and led to a local, watershed-based framework for resource management to protect key species [ 93 ]. Since global factors require numerous countries' assistance, it will be difficult and timely to get a proper collaboration or agreement that is agreed upon by all parties. In contrast, local factors can be dealt with immediately and directly. For example, appropriate wastewater treatments can mitigate local eutrophication and increase temporary refugia areas to 28%, allowing coral reefs to be relieved of the local stressor while international agreements are found to abate global stressors [ 14 ]. It is suggested that managers spend time identifying coral reef locations that, in the absence of other impacts, are most likely to have a heightened chance of surviving projected climate changes relative to other reefs and protect those reefs (Fig.  1 ) [ 39 ]. Multiple environmental variables are simultaneously interacting on coral reefs causing widespread degradation and understanding climate change impacts on reefs starts with managing local stressors that will, in return, help mitigate the global drivers of change.

The advancements outlined in this review have created a debate between scientists and resource managers about whether focusing efforts on mitigating local impacts will increase the resiliency of coral reef ecosystems to global climate change. This lack of clarity surrounding the recent disagreements on coral reef conservation practices has created many challenges in implementing actionable, science-based solutions that will benefit the communities that rely on them (Fig.  1 ). For example, some researchers argue that global warming is the universal threat to coral reef integrity and function [ 12 , 37 , 142 ]. In contrast, others believe local activities and land-based sources of pollution are the most critical threats [ 83 , 96 , 109 ]. Lastly, some believe local and global threats act in combination [ 66 , 104 ]. To plan, mitigate, and restore the future of coral reefs, it is essential to acknowledge that 61% of reefs are simultaneously affected by local and global stressors. It cannot be a ‘one size fits all’ solution for reef protection [ 14 ]. Our review recommends actionable science-based advancements based on a local risk assessment that are unique to each region or reef system.

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Good, A.M., Bahr, K.D. The coral conservation crisis: interacting local and global stressors reduce reef resiliency and create challenges for conservation solutions. SN Appl. Sci. 3 , 312 (2021). https://doi.org/10.1007/s42452-021-04319-8

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Interventions to help coral reefs under global change—A complex decision challenge

* E-mail: [email protected]

Affiliations Australian Institute of Marine Science, QLD, Australia, School of Biological Sciences, The University of Queensland, St. Lucia, QLD, Australia

Affiliation ARC Centre of Excellence in Mathematical and Statistical Frontiers, School of Mathematical Sciences, Queensland University of Technology, QLD, Australia

Affiliation Australian Institute of Marine Science, QLD, Australia

Affiliation Centre for Policy Futures, The University of Queensland, QLD, Australia

Affiliation Great Barrier Reef Foundation, QLD, Australia

Affiliation TropWATER, James Cook University, QLD, Australia

Affiliation School of Biological Sciences, The University of Queensland, St. Lucia, QLD, Australia

Affiliation ARC Centre of Excellence for Environmental Decisions, The University of Queensland, QLD, Australia

• Kenneth R. N. Anthony, 
• Kate J. Helmstedt, 
• Line K. Bay, 
• Pedro Fidelman, 
• Karen E. Hussey, 
• Petra Lundgren, 
• David Mead, 
• Ian M. McLeod, 
• Peter J. Mumby, 

Published: August 26, 2020

• https://doi.org/10.1371/journal.pone.0236399
• Reader Comments

Climate change is impacting coral reefs now. Recent pan-tropical bleaching events driven by unprecedented global heat waves have shifted the playing field for coral reef management and policy. While best-practice conventional management remains essential, it may no longer be enough to sustain coral reefs under continued climate change. Nor will climate change mitigation be sufficient on its own. Committed warming and projected reef decline means solutions must involve a portfolio of mitigation, best-practice conventional management and coordinated restoration and adaptation measures involving new and perhaps radical interventions, including local and regional cooling and shading, assisted coral evolution, assisted gene flow, and measures to support and enhance coral recruitment. We propose that proactive research and development to expand the reef management toolbox fast but safely, combined with expedient trialling of promising interventions is now urgently needed, whatever emissions trajectory the world follows. We discuss the challenges and opportunities of embracing new interventions in a race against time, including their risks and uncertainties. Ultimately, solutions to the climate challenge for coral reefs will require consideration of what society wants, what can be achieved technically and economically, and what opportunities we have for action in a rapidly closing window. Finding solutions that work for coral reefs and people will require exceptional levels of coordination of science, management and policy, and open engagement with society. It will also require compromise, because reefs will change under climate change despite our best interventions. We argue that being clear about society’s priorities, and understanding both the opportunities and risks that come with an expanded toolset, can help us make the most of a challenging situation. We offer a conceptual model to help reef managers frame decision problems and objectives, and to guide effective strategy choices in the face of complexity and uncertainty.

Citation: Anthony KRN, Helmstedt KJ, Bay LK, Fidelman P, Hussey KE, Lundgren P, et al. (2020) Interventions to help coral reefs under global change—A complex decision challenge. PLoS ONE 15(8): e0236399. https://doi.org/10.1371/journal.pone.0236399

Editor: Chaolun Allen Chen, Academia Sinica, TAIWAN

Copyright: © 2020 Anthony et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All data referred to in this paper are available via a web portal associated with the Reef Restoration and Adaptation Program: https://www.gbrrestoration.org/reports#technical-reports .

Funding: The work is supported by a grant from the Australian Government to the Reef Restoration and Adaptation Program ( https://www.gbrrestoration.org ). The funding body played no role in the writing of this paper. Opinions expressed in the paper is that of the authors in their individual capacity.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Climate change is impacting tropical coral reefs globally. Solutions are needed urgently to help reefs cope—and for three reasons. First, coral reefs are biologically the richest ecosystem in the world’s oceans [ 1 , 2 ]. Second, they provide ecosystem services that support livelihoods, recreation and economic activities worth hundreds of billions of dollars annually [ 3 – 6 ]. Third, coral reefs are among the most climate-sensitive ecosystems on Earth [ 7 , 8 ].

The recent marine heat wave exacerbated by the 2015/16 El Niño event led to extensive episodes of coral bleaching [ 9 , 10 ]. On Australia’s Great Barrier Reef, back-to-back bleaching in 2016 and 2017 led to unprecedented loss of coral cover [ 11 , 12 ]. While corals, the reef ecosystem engineers, can recover from severe disturbances [ 13 ], the projected shortening of interludes between increasingly severe bleaching events under even optimistic climate futures [ 14 , 15 ] will diminish the scope for net reef recovery. Growing pressure from ocean acidification, a chemical consequence of carbon emissions, will further diminish this scope [ 16 ].

Reducing greenhouse gas emissions will be necessary to sustain coral reefs in the long term. However, global emissions increased in 2017, 2018 and 2019 [ 17 , 18 ]. Current unconditional climate-mitigation pledges would see the world warm by 2.9 to 3.4°C above pre-industrial levels this century [ 19 ]. Even if global warming could be kept below 1.5°C–currently with less than 1% chance given pledges [ 20 ]–the surface waters of tropical oceans would warm another 0.3°C in coming decades [ 16 ]. Even such minimal continued warming would damage the sensitive coral species [ 21 ] that drive reef recovery [ 22 ] and form critical habitats [ 23 ]. Thus, as it currently stands, the Paris Accord will not protect coral reefs.

Another avenue is to build ecosystem resilience by further improving conventional management interventions and their governance [ 6 ]. Reducing nutrient pollution [ 24 , 25 ], limiting herbivore overfishing [ 26 ] and removing coral predators [ 27 ] can support resilience by enhancing coral growth and survival. This is so because (i) sediments have direct negative effects on coral recruitment and growth [ 28 , 29 ], and (ii) nutrient run-off in combination with herbivore overfishing reduce coral resilience by favouring the growth and survival of algae which prevent coral recruitment [ 30 , 31 ]. Reducing nutrient run-off may also reduce bleaching risks [ 32 – 34 ] and dampen outbreak risks of coral-eating crown-of-thorns starfish [ 35 ]. A problem, however, is that climate change—in addition to causing increased mortality via bleaching events [ 11 ] and storms [ 36 ]—erodes two key biological processes that underpin coral resilience: growth rate [ 37 , 38 ] and recruitment rate [ 39 , 40 ]. Thus, increasing conventional management action cannot compensate for the climate-driven decline in coral survival, growth and recruitment of many coral species in many places [ 16 , 22 , 41 , 42 ]. The situation is analogous to that of a cancer patient: good care helps, but it is only a solution when combined with a cure.

Both climate mitigation and intensified conventional management are indispensible to sustaining healthy coral reefs into the future. But more is needed. While natural processes of physiological acclimation may improve coral heat tolerance [ 43 , 44 ] genetic adaptation generally acts on longer timescales [ 45 ]. Warm-adapted traits may not spread fast enough in most coral species to keep up with the rate of global warming, even under strong carbon mitigation [ 14 , 46 – 48 ].

To build the biological resilience required to tolerate and recover from the projected escalation of marine heat waves [ 49 ] and increasing pressure from ocean acidification [ 50 ], high rates of coral adaptation will be needed. Active interventions to assist adaptation include ways to enhance coral performance including thermal tolerance [ 51 – 53 ] and/or lowering the exposure of corals to bleaching conditions–i.e. dampening heat waves locally and shading against strong solar radiation. A recent review by the National Academy of Sciences, Engineering and Medicine identified 23 candidate interventions with varying scope to become effective, feasible and safe [ 54 ]. While such measures are often referred to as restoration, they go beyond classical restoration techniques by altering biological and ecological resilience or stress exposure, or both. A similar review completed for the Australian Government’s Reef Restoration and Adaptation program (RRAP) examined 160 such interventions across a range of scales (from a few square metres to hundreds of reefs), concluding that 43 warranted more research and development (Box 1 ) and that the possibilities for positive impact overall were promising enough to warrant further investment [ 55 ].

Box 1. Categories of intervention based on functional objective as used in the Reef Restoration and Adaptation Program (RRAP) on the Great Barrier Reef [ 55 ]

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https://doi.org/10.1371/journal.pone.0236399.t001

The questions are then: what new interventions should be developed and added to the management toolbox for coral reefs? And once developed, when and where should they be deployed? How should performance expectations, risks and uncertainties be managed? We argue that an expanded intervention toolbox, as an adaptation strategy, presents at least three core challenges for reef managers, policy-makers and regulators: (1) framing the problem and setting the right objectives, (2) managing risks and uncertainties given the urgency, and (3) assessing and making necessary trade-offs ( Fig 1 ). Here we address each of these challenges. We close with a discussion of how fast and effective research and development (R&D) strategies provide options in a time of crisis and how the governance of on-reef intervention will face unprecendented challenges of coordination and integration. We conclude that the sooner we step up to this challenge, the closer we will be to producing solutions.

The framework is centred on an adaptive management cycle of intervention research and development (R&D), stakeholder and regulatory consultation, and governance. Two-way arrows indicate that steps in the structured decision-making framework form adaptive links with R&D, consultation and the governance of how resources are allocated and actions implemented given updated information. Adapted from: [ 56 – 58 ].

https://doi.org/10.1371/journal.pone.0236399.g001

Challenge 1: Setting the right objectives to solve the right problem

Pristine coral reefs are no more [ 59 , 60 ]. Even under best-case emissions trajectories, coral reefs will likely be transformed by climate change [ 11 ], so striving to retain or recreate historical levels of biodiversity and richness in a warming world may be futile. The most a conservation program may hope to deliver are sustained, yet altered, ecosystem services and priority values. And the results of any program will ultimately depend on how successful emission reductions become. These considerations affect our problem framing and the objectives we can achieve ( Fig 1A ). For example, is the objective to stem the decline in reef biodiversity, is it to sustain ecosystem services, or perhaps to create new ones? Is the objective to stem the decline of key (prized) species, or to sustain the key ecological functions they underpin? Perhaps provocatively, is it really coral reefs we seek to sustain, or is it the benefits they provide for society? We can’t have one without the other, but asking the question helps clarify objectives, and ultimately what we are willing to trade off. Different answers to these questions would lead to very different reef conservation programs.

Defining multiple, and often conflicting, objectives for complex social-ecological systems such as coral reefs is challenging, but critical. Within objectives, which values can be sustained with the capabilities and resources available? Coral reefs produce numerous value streams to society [ 61 , 62 ]. Bona fide adaptation solutions would be those that strike a balance across such value streams–monetary and otherwise. Altered, but functionally resilient, ecosystems are increasingly being embraced in terrestrial and freshwater conservation programs [ 63 – 66 ]. The time may now be right to explore such options for coral reefs also. We revisit this challenge under Prioritisation and trade-offs . With a clear understanding of objectives and values, the decision-making process around developing and applying new and potentially contentious intervention options, in combination with mitigation and conventional management ( Fig 1 , step B), can become informed and transparent [ 57 ].

Challenge 2: Balancing benefits and risks in the face of uncertainty

Developing new technologies for environmental management and conservation is risky: it is expensive, takes a long time, and success is not guaranteed. Risks associated with emerging technologies, whether perceived or real, and their potential side effects, costs, and uncertainties trigger precaution [ 67 ]. There is good reason for this as history is replete with examples of how interventionist management can result in destructive outcomes [ 68 ]. The managers who introduced cane toads to Australia in 1935 to manage the cane beetle did neither have experience nor foresight to consider the catastrophic invasive potential of the toads. Today, the scientific and regulatory communities are much more informed about the biological, ecological, ethical, legal and social implications of new and emerging technologies [ 69 ]. Examples of advancement in the management of risk and uncertainty across a diversity of fields include the protection of nature reserves against invasive species [ 70 ], managed readiness levels of new technologies that enter aviation and space programs [ 71 ], risk assessments of new drugs prior to approval [ 72 , 73 ] and the adoption of driverless cars [ 74 ]. Applied coral reef research and development can and should learn from these and other fields. Doing so can help identify options that, when implemented in a coordinated approach after rigorous development and consultation ( Fig 1 , step C), are effective, safe, acceptable to the public and regulators, and economically rational.

Critically, in a time of rapid climate change, being risk averse can be risky [ 75 ]. Delaying new interventions because of uncertainty around side effects could mean losing key species and functions. However, the risk associated with status quo under different climate futures must be balanced against the risk of premature intervention, especially with technologies that are not yet ready for deployment [ 76 , 77 ]. Premature deployment of untested interventions (e.g. genetic engineering, assisted migration, solar radiation management) may cause ecosystem disruptions [ 54 , 78 , 79 ]. The sooner research and development programs evaluate the potential risks and benefits of interventions, the more informed policy decisions can be about whether to deploy, delay, or dismiss an intervention. This approach is the basis for NASA’s assessment of readiness levels of new technologies entering space programs [ 80 ], for expanding the number of options for medical treatments [ 81 ], and most recently for Australia’s Reef Restoration and Adaptation Program for the Great Barrier Reef [ 55 ]. Unfortunately, the motivation and social license to start conservation programs typically come when ecosystems or species are already in advanced decline [ 75 ]. Such delayed action represents a lost opportunity as interventions take time to develop, and because damage-prevention and restoration are now both needed to sustain ecosystems [ 82 , 83 ]. For example, coral populations in the northern Great Barrier Reef (GBR) are adapted to 1–2°C higher temperatures than populations in the central section [ 84 ], but the North-to- South larval spread is limited by diverging currents [ 47 , 85 ]. Under expectations of escalated GBR-wide warming [ 86 ], building resilience in the central and south using warm-adapted coral stock from the north will be a race against time as both donor reefs and receiving reefs are at risk. While classical reef-restoration approaches using local coral stock or larvae may enhance reef recovery following disturbances [ 87 , 88 ], enhanced climate tolerance is needed to support coral resilience under climate change [ 54 ].

Precaution is central to policy and regulation, but social science research indicates the need to interpret and understand risks more broadly [ 68 ]. Risk assessments of new interventions need to consider views that go beyond those of scientists and regulatory experts. Thus, decision makers and management agencies need to consult reef stakeholders (e.g. tourism operators, commercial and recreational fisheries, conservation groups), Traditional Owners and the wider community. Risk assessments in this context need to be tackled at three levels (1) the risk regime of future climatic conditions, (2) whether interventions will really produce the intended benefits, and (3) risks and costs versus benefits of early vs delayed implementation ( Fig 1 , step D). Such assessments are complicated by the fact that different future conditions will require different solutions, timing and risk tolerance [ 53 ]. What would constitute premature intervention deployment under the expectation of 1.5°C warming this century could be too-little-too-late under the expectation of 3°C warming. Further, picking intervention solutions that are robust to climate change could be a blunt strategy because both timing and intervention type could be misaligned with the conditions that eventually unfold. The most effective solution from a risk-management perspective could be a combination of intervention hedging and improved forecasting, not unlike an investment portfolio strategy [ 89 ].

Challenge 3: Prioritisation and tradeoffs–we can’t save everything

The gap between resources available and resources needed for conservation is widening [ 90 , 91 ]. Consequently, investment prioritisation is necessary [ 92 , 93 ]. How this is done needs to be anchored in the problem framing and by clearly defined ecological, economic and social objectives. Further, prioritisation needs to have line of sight to outcomes that can be achieved given climate uncertainty and funding contraints ( Fig 1 , step E). As an example, consider two extreme yet realistic prioritisation alternatives for a large reef system such as the Great Barrier Reef. Should we aim to sustain a minimum of 5% coral cover over a 1000 km 2 area of reef, or a minimum of 25% coral cover over a 200 km 2 area? Logistics will differ, but the net result is the same in terms of coral area sustained: 50 km 2 . However, depending on the spatial configuration of the saved corals, these alternatives would produce very different ecological outcomes and values for society. Spreading efforts across a large area would speak to system integrity and perhaps the Outstanding Universal Value of the Great Barrier Reef World Heritage Area [ 94 ]. Downsides of spreading efforts thinly include reduced capacity to sustain critical ecological functions such as net reef accretion [ 95 ], and reduced fitness via a reduced demographic Allee effect [ 96 , 97 ]. Conversely, concentrating efforts on a selection of just a few but glorious reefs could sustain parts or all of the GBR’s tourism industry, which is spatially concentrated [ 98 ]. It would enable managers to support ecological functions and services on those focal reefs more easily, and perhaps create spill-over effects to other reefs [ 99 ]. Taken to the extreme under severe climate change, spatial prioritisation under resource constraints could reduce the Great Barrier Reef to a fragmented (and therefore vulnerable) network of coral oases in an otherwise desolate seascape.

Other options might involve targeting reefs that are gateway nodes in the spatial reef network–in other words, investing in well-connected reefs located in the least thermally stressed environments [ 100 ]. Here, efforts to support population growth of climate-hardy corals on source reefs (larval donors) may allow export of their beneficial traits to reefs downcurrent through paths of natural dispersal [ 99 , 101 ]. But risks are that disease agents and potentially invasive species arising from either translocation or assisted gene flow may also spread via similar routes [ 47 ]. Selection criteria should thus favour the dispersal of desirable species only [ 99 ]. The decision challenge associated with spatial prioritisation is therefore one of maximising the spread of genes or traits that produce benefits and minimising those that represent risks. Another option may be to assemble a portfolio of reefs that have less risk of being exposed to the most damaging climate stressors [ 48 , 102 ]. Combining these options may both enhance resilience and reduce stress on priority reefs.

Prioritisation of species adds to the decision challenge for reef restoration and adaptation. Without significant climate mitigation, sensitive coral species will give way to naturally hardier ones [ 11 ], or to species that can adapt faster [ 45 , 103 ]. Picking who should be winners, and ultimately who will be losers, under continued but uncertain climate change is perhaps the biggest challenge facing R&D programs tasked with developing reef rescue interventions. Unfortunately, sensitive coral species tend to be the ones underpinning high-value ecosystem services, including habitat provision for a rich biodiversity [ 23 ] that in part underpin tourism [ 5 ]. Should we invest in making sensitive species hardier but risk failing by not making them hardy enough, thereby wasting resources? Or should we pursue a potentially less risky pathway and support the more climate-hardy species and help them adapt to the consequently altered ecosystems and the different goods and services they provide? Importantly, our best efforts to build coral resilience under severe climate change will not prevent reefs from transitioning to altered ecosystems [ 6 , 60 ]. Strategies to help humans adapt to a changed ecosystem need to combine with strategies that help reefs [ 104 ]. Lastly, can robust keystone species be found that can give climate protection to many other dependent species [ 105 ], thereby sustaining ecosystem services? The latter may ultimately be the most effective choice if species compositions allow the ecosystem to remain functionally resilient [ 64 ]. How these priorities are set ultimately depends on what society wants (objectives and values), what options can be achieved technically, institutionally and socially, and what compromises and risks we are willing to accept. The preferred strategy would be the one that delivers the most positive outcomes to priority objectives (and the values they encompass) with low or manageable risks and within resource constraints [ 57 , 58 , 106 ].

R&D provides options, but choose carefully

The likelihood that the world will warm more than 2°C (air) since preindustrial levels this century was recently 95 percent [ 17 , 20 ]. With this outlook, new intervention options for coral reefs will be in growing demand. Importantly, however, no new intervention can be added to the operational management toolset without significant R&D; it is the prerequisite for intervention effectiveness, safety and cost efficiency [ 67 ]. How interventions are chosen for R&D and progressed through to deployment is both complex and critical because it will determine what options will ultimately be available for managers and when ( Fig 1 , steps B-E). Three questions are at the centre of reef intervention R&D. First, which interventions should be prioritised for development? Second, how should they be queued in time? Third, should intervention strategies be robust or targeted?

Limited resources for R&D means not all interventions can be assessed nor progressed. Complicating this problem is that the more the world warms, and the more ecosystems become affected, the greater the overall demand for intervention resources will be. Misguided investment choices can lock up vital resources in inferior solutions, hampering or preventing the development of superior ones [ 107 ]. Prioritising no-regrets options because they are inexpensive or less challenging technologically [ 77 ] could lead to regrets downstream by preventing or delaying the development of more effective solutions. Prioritisation of interventions for R&D should ideally be a fast adaptive process (indicated by multiple adaptive cycles in Fig 1 ) whereby combinations of interventions are continuously assessed for their combined benefits and risks against environmental, social and economic objectives [ 53 ]. In general terms, the right time to implement an intervention strategy following R&D would be when the cumulative (time-integrated) benefit-to-risk ratio of deployment exceeds the cumulative benefit-to-risk ratio risk of not deploying. Here, benefits are defined as positive outcomes (as likelihood and consequence) for ecosystem services and values for society, and risks as negative outcomes. The benefit-to-risk ratio of these contrasting strategies, however, will depend on the climate future ( Fig 1 , step D).

Robust strategies work across a range of climate change scenarios. While investing in a robust R&D strategy will give some return regardless of climate future, the strategy may eventually underperform because it trades off effectiveness for reduced risk. In contrast, targeted strategies are tuned to different climate scenarios. This involves betting on, and planning for, a specific climate trajectory. This represents high risk, but potentially also high reward. For example, a strategy that buys 1°C thermal tolerance for sensitive and valued coral species (on top of today’s 1°C global warming) may give high ecological, social and economic returns if global warming is kept below 2°C relative to preindustrial. If the world warms much more than 2°C, however, the strategy will be ineffective unless these species continue to adapt. Conversely, a strategy that bets on severe climate change and focuses on helping the hardiest species only (or develops artificial reefs) will miss the opportunity to protect biodiversity if a milder climate scemario unfolds in reality. Developing a portfolio of interventions that allows hedging and a staged roll-out of interventions as climate change unfolds may be ideal, but may again be constrained by resource availability for R&D, and the demands of urgency—real or perceived.

Get people on board

Environmental problems are social problems [ 108 ]. Climate change, mass coral bleaching events and consequent coral reef decline are human-induced and require solutions from science and society. The dynamics of the current coral disease outbreak in the Caribbean are also consistent with ocean warming patterns [ 109 – 111 ]. While interventions that can build resistance to coral disease will differ from those that can build resistance to coral bleaching, a similar approach to solutions is needed. Solutions require innovative thinking and coordination between science, management and policy, and public engagement. There are concerns that restoration and adaptation are distractions from tackling global climate change, the main driver of coral reef decline [ 112 ]. Communication and engagement strategies must reinforce the message that restoration and adaptation are a health-care strategy that can only work in tandem with a cure: urgent global action to address climate change.

Any new interventions on coral reefs, in particular radical ones, will be up against hurdles to achieve social acceptance and to overcome regulatory constraints [ 104 , 105 ], leading to uncertainties that become barriers for solutions ( Fig 1 , step D). Existing regulations operate under a retrospective model that crowbars coral restoration and adaptation into existing policy and legislation. However, future policy development should accommodate risks of future climatic conditions (see challenge two above) whilst simultaneously adapting to the emerging opportunities and challenges of coral restoration and adaptation.

A handful of countries are currently developing or revising existing policy and regulatory processes to assist coral restoration and adaptation in the face of climate change: Australia, USA, Netherlands, France, Costa Rica, Japan, Columbia, and Thailand. The United Nations Environment Program have declared 2021–2030 as the UN Decade of Ecosystem Restoration. The aim is to “support and scale up efforts to prevent, halt and reverse the degradation of ecosystems worldwide and raise awareness of the importance of successful ecosystem restoration” [ 87 ].

To get people on board will require coordinated consulation and transparent decision making that considers all risks, benefits and value consequences of reef intervention in a structured way [ 106 ]. Open communication and engagement around objectives, options and trade-offs will be key.

Strong and coordinated governance needed

Applying a coordinated and well-conceived coral reef intervention program which sets the right objectives, identifies and balances risks, and aims to make optimal tradeoffs, in the face of uncertainty while getting community buy-in and support, will depend on robust and appropriate governance [ 113 , 114 ]. First, at the R&D stage, researchers will need to be provided with the resources to do the job, and the mandate to take risks. For something as new and potentially controversial as large-scale coral reef intervention, consultation and co-development mechanisms must involve regulators, reef stakeholders, Traditional Owners and the public. Internal processes must be agreed on at the outset, to allow ongoing, effective prioritisation while maintaining flexibility in the face of changing conditions and unexpected setbacks. Some of the tested interventions to be examined will simply not work. Strong governance will be particularly important if political pressure for quick action (just do something) mounts in the face of worsening climate conditions. Next, as R&D results yield prospective options for at-scale intervention, governance must adapt to a situation where the costs, profile, and risk associated with failure of the effort have grown substantially. Again, at this stage, costs, benefits, risks and community desires will have to be balanced and trade-offs made, for at-scale deployment to occur.

Conclusions

An expanded toolbox of interventions will provide opportunities to build reef resilience against continued climate change. Without carbon mitigation, no intervention strategy will be successful in the long run. And no single intervention can produce adaptation solutions. A portfolio of new and existing interventions must be combined with mitigation.

New interventions come with risks, but so does the status quo. If the potential of new interventions can be unlocked and their benefits exceed risks for reef, people and economies, they should be developed and deployed. The challenge for science, management and policy, in consultation with communities, is to develop and adopt technologies that will be both safe and effective—and within years rather than decades.

What climate trajectory will unfold is uncertain. But what is certain is that we need an expanded set of options to safeguard coral reefs and dependent people and industries. Research and development can help, but only if efforts are focused, coordinated and highly integrated. To do this will require a level of organisation, collaboration and integration across disciplines never seen before in natural sciences, conservation and policy.

Acknowledgments

The work was conducted as part of the Reef Restoration and Adaptation Program (RRAP, https://www.gbrrestoration.org ). RRAP data referred to in this paper can be accessed via: https://www.gbrrestoration.org/reports#technical-reports . We thank Prof Allen Chen and Prof Bob Steneck for insightful reviews and comments that improved the paper. Opinions expressed in the paper are those of the authors in their individual capacity.

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The Evolution of Coral Reef under Changing Climate: A Scientometric Review

Chandra segaran thirukanthan.

1 Institute of Marine Biotechnology (IMB), Universiti Malaysia Terengganu (UMT), Kuala Nerus 21030, Terengganu, Malaysia

Mohamad Nor Azra

2 Research Center for Marine and Land Bioindustry, Earth Sciences and Maritime Organization, National Research and Innovation Agency (BRIN), Pemenang 83352, Indonesia

Fathurrahman Lananan

3 East Coast Environmental Research Institute, Universiti Sultan Zainal Abidin (UniSZA), Gong Badak Campus, Kuala Nerus 21300, Terengganu, Malaysia

Gianluca Sara’

4 Laboratory of Ecology, Earth and Marine Sciences Department, University of Palermo, 90133 Palermo, Italy

Inga Grinfelde

5 Laboratory of Forest and Water Resources, Latvia University of Life Sciences and Technologies, LV-3001 Jelgava, Latvia

Vite Rudovica

6 Department of Analytical Chemistry, University of Latvia, LV-1004 Riga, Latvia

Zane Vincevica-Gaile

7 Department of Environmental Science, University of Latvia, LV-1004 Riga, Latvia

Juris Burlakovs

8 Mineral and Energy Economy Research Institute of the Polish Academy of Sciences, 31-261 Krakow, Poland

Associated Data

No data was generated from the study.

Simple Summary

Coral reefs are vital ecosystems with high biodiversity and ecological services for coastal communities. Climate change is accelerating, with detrimental consequences on coral reefs and related communities, but it is challenging to keep up with the literature given its current rapid expansion. The current review foresees three future trends in the area of coral reefs and climate change, including (i) incorporating future scenarios, (ii) climate-induced temperature changes, and (iii) adaptation strategies, which are expected to move society closer to the following Sustainable Development Goal: 13 Climate Action.

In this scientometric review, we employ the Web of Science Core Collection to assess current publications and research trends regarding coral reefs in relation to climate change. Thirty-seven keywords for climate change and seven keywords for coral reefs were used in the analysis of 7743 articles on coral reefs and climate change. The field entered an accelerated uptrend phase in 2016, and it is anticipated that this phase will last for the next 5 to 10 years of research publication and citation. The United States and Australia have produced the greatest number of publications in this field. A cluster (i.e., focused issue) analysis showed that coral bleaching dominated the literature from 2000 to 2010, ocean acidification from 2010 to 2020, and sea-level rise, as well as the central Red Sea (Africa/Asia), in 2021. Three different types of keywords appear in the analysis based on which are the (i) most recent (2021), (ii) most influential (highly cited), and (iii) mostly used (frequently used keywords in the article) in the field. The Great Barrier Reef, which is found in the waters of Australia, is thought to be the subject of current coral reef and climate change research. Interestingly, climate-induced temperature changes in “ocean warming” and “sea surface temperature” are the most recent significant and dominant keywords in the coral reef and climate change area.

1. Introduction

Scleractinians, or stony corals, emerged during the Cambrian period and constructed the earliest reefs, dating to approximately 410 million years ago [ 1 , 2 , 3 ]. Five major coral extinctions have occurred since then, all of which have been linked to rising temperatures and higher levels of carbon dioxide in the atmosphere [ 2 , 4 ].

While coral reef research commenced more than 100 years ago, concern over the state of coral reefs is relatively recent, occurring only in the last four decades. In 1981, at the 4th International Coral Reef Symposium, Edgardo Gomez initiated the conversation on threats to coral reefs by presenting his concerns to the scientific community [ 5 , 6 ]. Coral reefs are considered an important marine resource for coastal communities, and the conference participants were mainly focused on coral reef management and environmental impacts and related fisheries activities [ 5 , 7 , 8 ]. In addition to the natural stresses that have always existed on coral reefs, such as storms, freshwater inundation, and seismic and volcanic events, there is growing evidence of new emerging threats potentially causing global damage to coral reefs [ 7 , 8 , 9 , 10 ].

At current extinction rates, it is estimated that we are commencing the sixth mass extinction event [ 11 , 12 , 13 ], with individual extinctions occurring approximately 1000-fold faster than the expected background extinction rate. Theoretically, species extinctions occur at a rate proportional to the rate of speciation or the creation of new species [ 14 ]. Current extinction rates are much higher than speciation rates. This is largely due to the fact of anthropogenic factors [ 15 , 16 ], such as habitat destruction [ 17 ], deforestation [ 18 ], pollution [ 7 ], ocean acidification, climate change resulting from greenhouse gas emissions, and overexploitation of ecological resources [ 19 , 20 , 21 ]. It is estimated that 75% of species will go extinct unless human pressures on the environment are scaled back soon [ 20 , 22 , 23 , 24 , 25 ]. Further management efforts are required to reduce the impacts of climate change and human anthropogenic stress towards coral reef communities [ 7 ].

Anthropogenic pressures on reefs have been the dominant factor damaging coral reefs through a range of stresses ( Figure 1 ). Unsustainable land-based human activities, such as deforestation, poorly regulated agriculture, and urban/industrial development, are major contributors to the release of excessive sediments and nutrients into the environment [ 26 , 27 , 28 ]. Increases in human-caused greenhouse gas emissions are the primary factor in the current climatic shift around the world [ 29 , 30 ]. The ocean acts as a massive sink that absorbs carbon dioxide, resulting in the acidification of the oceans [ 31 , 32 ]. Coral bleaching and widespread damage to the coral reef ecosystem have become increasingly common because of thermal stress brought on by rising ocean temperatures [ 33 ]. Lack of food to sustain the coral reef ecosystem and disruption of larvae dispersal are both attributable to altered currents, upwelling, and/or vertical mixing brought on by changing currents and winds [ 34 ]. Storms and cyclones are “agents of mortality” on coral reefs and can have a direct impact on the structure and local distribution of coral reef assemblages, especially through the large waves they produce [ 35 ]. Reduced salinity caused by heavy rainfall and enhanced surface run-off onto nearshore reefs during cyclones, storms, and heavy precipitation rates can lead to algal blooms and other devastating results [ 36 , 37 ]. The rise in sea level, caused by thermal expansion and the melting of ice on land, has varied across different regions of the world over the past century, with an average increase of approximately 20 cm [ 38 ]. The sedimentary mechanisms triggered by the rising sea levels have the potential to intensify and jeopardize crucial physiological reef processes, such as photosynthesis, feeding, and recruitment, thereby posing a severe threat to coral reefs and related ecosystems, such as seagrass meadows and mangrove forests [ 39 , 40 ]. This threat, coupled with increasing carbon dioxide (CO 2 ) emissions, can negatively impact these vital ecosystems. Without effective local measures and a concerted effort to reduce carbon dioxide emissions, these effects are projected to intensify, leading to an unprecedented degradation of marine biodiversity and ecological balance [ 41 , 42 ].

Threats to coral reefs posed by factors related to climate change.

Given the length of time that scientists have been studying climate change [ 43 ], the sheer volume of published research in the field can make it difficult for scientists to develop an overview of the topic [ 44 ]. Bibliometric analysis can be used to provide an overview of voluminous scientific literature [ 45 ]. Research output in each field can be charted in terms of its characteristics and evolution through quantitative examination of publication data [ 45 , 46 ]. Performance and research patterns of authors, journals, countries, and institutions can all be evaluated with the help of bibliometric methods, and patterns of collaboration between these entities can be identified and quantified [ 47 ]. A research domain’s multidisciplinary nature and the variety of journals publishing on a given topic can be inferred from the subject categories assigned to publications and the number of journals publishing on a given topic. The most recent developments, research directions, and top-of-mind issues in a particular field can be gleaned from bibliometrics [ 48 ]. In addition, bibliometrics can be a useful tool for guiding scientific policy. Findings from bibliometric analyses not only inform researchers and policymakers but also aid in the distribution of funds for scientific investigation [ 49 ].

2. Scientometric Analysis

Software programs, such as VOSviewer (Centre for Science and Technology Studies (CWTS), Leiden University, Leiden, The Netherlands), Pajek (University of Ljubljana, Ljubljana, Slovenia), and CiteSpace (Drexel University, Philadelphia, PA, USA) can be used to create scientometric visualizations. CiteSpace is a scientometric-based analysis tool that provides two main outputs for researchers. Firstly, it includes three central concepts: burst detection, betweenness centrality, and heterogeneous networks. Secondly, CiteSpace addresses three practical issues: identifying the nature of a research front, labeling specialties, and detecting emerging trends and abrupt changes in a timely manner. Identifying these outputs involves six main procedures: time slicing, thresholding, modelling, pruning, merging, and mapping. CiteSpace’s functionalities, such as dual map overlay, burst detection, cluster explorer, and timeline view, are particularly helpful in identifying the current research trends of a specific field. Researchers can use this information to gain insights into the overall state of research in a given field, the pace of advancement, and the most prominent areas of interest [ 50 , 51 ].

Briefly, the dual map overlay graphically identifies both original documents and cocited networks and expresses their relationships by connecting them with lines. Burst detection refers to a frequency surge of a specific knowledge domain. A cluster is defined as the frequency of citations of cited references. A timeline arranges papers in chronological rows, with each cluster represented by one row and papers represented as nodes [ 52 ].

3. Objective of the Review

This review addresses the question, “How have coral reefs been affected by climate change and their interactions using bibliometrics?”. Specific objectives were to assess the literature in terms of (i) the annual number of articles published, (ii) countries/regions involved in the field, (iii) research topics, (iv) cocited networks (i.e., frequency of two different documents are cited together in other documents), (v) cluster networks, (vi) research topic (i.e., keywords) burstiness, (vii) dual map overlay, and (viii) the future trends of the knowledge domain (i.e., coral reef and climate change). The main article structure diagram is shared in Figure 2 .

Article structure diagram.

4. Systematic Data Collection

This study was analyzed based on the Web of Science database Core Collection (WOSCC) on 16 November 2022. Keywords used for data collection comprised terms related to climate change [ 53 ] and coral reefs [ 54 ]. CiteSpace, 6.1.4, version 64-bit for Windows, was used to visualize current trends. The search string are as follows: CLIMATE CHANGE: (“climat* chang*”) OR (“global warm*”) OR (“seasonal* variat*”) OR (“extrem* event*”) OR (“environment* variab*”) OR (“anthropogenic effect*”) OR (“greenhouse effect*”) OR (“sea level ris*”) OR (erosio*) OR (“agricult* run-off”) OR (“weather* variab*”) OR (“weather* extrem*”) OR (“extreme* climat*”) OR (“environment* impact*”) OR (“environment* chang*”) OR (“anthropogenic stres*”) OR (“temperature ris*”) OR (“temperature effect*”) OR (“warm* ocean”) OR (“sea surface* temperat*”) OR (heatwav*) OR (acidific*) OR (hurrican*) OR (“el nino”) OR (“el-nino”) OR (“la nina”) OR (la-nina) OR (drought*) OR (flood*) OR (“high precipit*”) OR (“heavy rainfall*”) OR (“CO 2 concentrat*”) OR (“melt* of the glacier*”) OR (“melt* ice*”) OR (“therm* stress*”) OR (“drought”) OR (“hypoxia”) AND CORAL REEF: (“coral reef*”) OR (“barrier reef*”) OR (“atolls”) OR (“fring* reef*”) OR (“coral island*”) OR (“atoll lagoon*”) OR (“biogenic deposit*”).

5. Evolution of the Literature

5.1. global publication.

The coral reef and climate change field showed an increase in published articles, indicating that the research is in rising momentum ( Figure 3 ). Since 2006, studies on coral reef and climate change have been published, amounting to approximately 1.5% to almost 10% of total articles on the WoS platform in 2021, especially in the WoS Core Collection (WOSCC) database. The field entered an accelerated uptrend phase in 2016, and it is anticipated that this phase will last for the next 5 to 10 years for research publications and citations. This could be because the WOSCC added a new edition of the Emerging Sources Citation Index (ESCI) database in 2015 [ 55 ]. The leading countries in coral reef and climate change research are shown in Figure 4 . The USA and Australia produced the most publications, with 2940 and 2933 articles, respectively, more than triple the output of third-ranked England, with approximately 719 articles. The USA and Australia contributed more than 75% of all publications. The study also found that there is a lack of studies conducted in the African regions. As expected, countries without coastal areas, such as Kazakhstan and Mongolia, showed no articles published in the coral reef and climate change fields. Additionally, most island nations, such as Japan, New Zealand, Australia, or Cuba, contributed to the knowledge of the coral reef and climate change.

Number of original research articles on the impact of climate change on coral reefs published annually from 1977 until 2021.

Nations publishing the most research on coral reefs and climate change generated from the freely editable map chart website ( https://www.mapchart.net/world.html (accessed on 10 January 2023)).

5.2. Leading Institutions, Funding, and Authorship Distribution

Ellegard and Wallin [ 46 ] opined that the distribution of research institutions is a useful indicator of academic support for a discipline. The network of institutions generated 948 nodes (i.e., group of entities) and 2666 collaborative links among institutions conducting research ( Figure 4 ). The 4159 documented affiliations reflect the importance of this field in academia and the intensity of the investigations. Institutions in this collaborative network (a collaborative affiliation appeared in the article) that have contributed the most to this field are shown in Figure 5 and Table 1 . An analysis of 7743 publications related to coral reefs and climate change identified a total of 29,890 affiliations. The top 20 institutions contributed to 7231 affiliations, which accounted for nearly 24% of all publications. Specifically, James Cook University was found to have contributed the highest number of publications (1119, 14% of the total), followed by the Australian Institute of Marine Science and the University of Queensland. These findings suggest that a small number of institutions have played a significant role in the research on the impact of climate change on coral reefs.

Collaborative network of institutions researching coral reefs and climate change from 1976 to 2021.

Top 20 institutions in the field of coral reef and climate change.

Table 2 lists the major funding agencies cited by publications in this field. The Australian Research Council funded 1001 publications, or nearly 13% of the total. Australian institutions have been at the forefront of climate change research partly because they have had greater access to funding. For instance, the Great Barrier Reef Foundation (GBRF) was awarded USD 443.3 million for the Reef Trust project between 2018 and 2019, the largest investment in reef protection to date. In 2019 and 2020, the budget allocated USD twenty-three million dollars for water quality projects, USD 4.33 million for Crown-of-Thorns (COT) control, USD 16.3 million for reef protection aimed at supporting traditional owners, USD 2.6 million for community reef protection, and USD 1.5 million for integrated monitoring and reporting. This funding allocation was based on the 2019 Great Barrier Reef Foundation’s budget plan (GBRF, 2019). In addition to these investments, the Australian Government also dedicated USD 6 million in 2018 to support the Reef Restoration and Adaptation Program’s concept feasibility phase. This program aimed to investigate the most effective science and technology options for restoring the reef, including methods for cooling and shading reef structures, coral reproduction and recruitment, biocontrol, field treatments, and coral plantation initiatives [ 56 ]. The ARC Centre of Excellence for Coral Reef Studies, located at James Cook University, conducts cutting-edge research on coral reefs. With strong collaborative ties to 24 other institutions in nine countries, it is Australia’s top contributor to coral reef sciences. Five of the ten most prominent scientists identified by CiteSpace analysis are associated with the ARC Centre of Excellence for Coral Reef Studies.

Top 20 funding agencies related to coral reef and climate-change-related studies.

The network of authors generated in CiteSpace is a valuable tool for understanding collaborations and identifying potential future collaborations within a given field. In this study, the network of authors in the field of coral reefs and climate change generated 1680 nodes and 6931 links, where nodes represent authors with the number of publications, and links between nodes represent collaborations between authors. As a general rule, a higher number of nodes generated from CiteSpace indicates a greater degree of collaboration between authors.

The top authors in Table 3 are crucial indicators of further scientific collaboration and advancement within the field of coral reefs and climate change. However, it is important to note that while first authorship is typically assigned to the individual who made the most significant contribution to the research, this does not mean that coauthors’ contributions are any less significant or valuable. Coauthors can provide specialized expertise, contribute to data analysis and interpretation, or support the project through funding, logistical support, or other means. The authorship order and the number of authors on a publication may vary based on the specific circumstances of the research project and the agreed-upon conventions of the discipline. Ultimately, understanding the network of authors and their collaborations can help identify potential areas of future research and scientific collaboration within the coral reefs and climate change.

Top 20 authors in the field of coral reef and climate change.

Emeritus Professor Terry Hughes of James Cook University, who served as the ARC Centre of Excellence for Coral Reef Studies Director from 2005 to 2020, topped the list. In 2016, Nature named Hughes one of the “10 people who mattered this year” for addressing the widespread coral bleaching event brought on by climate change. Hughes’s research has led to practical solutions to improve marine environmental management [ 57 ]. His work on the effects of climate change on coral reefs has been widely cited, especially his paper on the resistance of some coral reefs to climate change and anthropogenic factors [ 58 ]. Second on the list was Professor Ove Hoegh-Guldberg from the University of Queensland (UQ), Australia. He serves as Director of the Global Change Institute at UQ and also as a Chief Investigator at the ARC Centre of Excellence for Coral Reef Studies [ 59 ]. Dr. Katharina Fabricus is a coral reef ecologist and a Senior Principal Research Scientist at the Australian Institute of Marine Science [ 60 ]. Many of her highly cited publications are on topics related to ocean acidification [ 61 , 62 , 63 , 64 ], the impacts of water quality on coral reefs [ 65 , 66 ] and understanding the effects of terrestrial run-off on coral reefs [ 67 , 68 ].

Dr. Peter W. Glynn, from the National Center for Coral Reef Research, University of Miami, was among the pioneers in analyzing and reporting the impacts of the 1982–1983 El Niño warming event on Eastern Pacific coral reefs [ 69 ]. This was followed by Tim McClanahan, a senior conservation zoologist at the Wildlife Conservation Society and also an associate at the ARC Centre of Excellence for Coral Reef Studies [ 70 ]. His global study of more than 2500 reefs produced a Bayesian hierarchical model to predict how reef fish biomass is related to 18 socioeconomic drivers and environmental conditions [ 71 ]. Dr. Peter Mumby is a coral reef biologist from the University of Queensland and also a Chief Investigator at the ARC Centre of Excellence for Coral Reef Studies [ 72 ]. He collaborated with Professor Ove Hoegh-Guldberg to publish “Coral Reefs under Rapid Climate Change and Ocean Acidification”, which is one of the most cited papers in the field (see Table 4 ) [ 22 ]. Another study published in Nature reported the resilience of Caribbean coral reefs against moderate hurricanes [ 73 ]. Dr. David Bellwood, an Australian Laureate Fellow and Distinguished Professor at James Cook University [ 74 ], has reported on the effects of climate change on coral reef ecosystems, even though his primary research interests are in biology and the evolution of reef fish [ 58 , 75 , 76 ].

The most highly cited references about coral reefs and climate change.

* Burst index: the value generated from the CiteSpace indicates the level of importance of each article in the field. ** Centrality: the main focused article between cited references in the publications.

Dr. John Pandolfi from the University of Queensland is a paleoecologist and a Chief investigator at ARC. His research integrates long-term ecological and environmental time series data to discover past and future influences of natural variability, human impact, and climate change on coral reef resilience. Among his highly cited works is a projection of the future of coral reefs under global warming and ocean acidification [ 20 ]. Dr. Kenneth RN Anthony, an associate scientist at the Australian Institute of Marine Science and director of Environmental Strategies ES5, has published widely on ocean acidification [ 77 , 78 , 79 ]. Dr. John Bruno, from the University of North Carolina, is a marine ecologist focusing on the impacts of climate change on marine ecosystems, particularly coral reef ecology. His publication with Dr. Ove Hoegh-Guldberg, on the effects of climate change on global marine ecosystems is one of his most cited works [ 80 ].

Next on the list is Emeritus Professor Barbara E. Brown from Newcastle University, who conducted extensive research on coral bleaching, specifically on the role of zooxanthellae [ 81 ]. Next on the list is Professor Andrew C. Baker, a marine biologist at the University of Miami, who studies coral reefs and climate change. He leads the Coral Reef Futures Lab and focuses on developing and testing methods to increase coral reef resilience [ 82 ].

Glenn De’ath and Ray Berkelmans, both from The Australian Institute of Marine Science, are also highly cited for their research on coral reefs. De’ath’s work involves statistics and ecology, specifically on the Great Barrier Reef coral cover decline [ 83 ], while Berkelmans’ research focuses on thermal stress, adaptation to climate warming, the resilience of reef communities, and upwelling [ 84 ].

Joan Kleypas, a Senior Scientist from the National Center for Atmospheric Research, is also on the list, and her highly cited works revolve around the impact of ocean acidification on coral reefs [ 85 , 86 ]. Next is Professor Nick Graham from Lancaster University, who assesses the impacts of climate-induced coral bleaching on coral reef fish assemblages, fisheries, and ecosystem stability [ 87 ].

Emeritus Professor Michael Lesser from the University of New Hampshire is also highly cited for his work on climate change-related stressors’ biochemical and physiological impacts on coral reefs [ 88 ]. Professor Joseph Loya from Tel Aviv University quantifies changes in biodiversity and assesses reef health [ 89 , 90 ], while Professor Peter Edmunds focuses on the physiological ecology of tropical coral reefs [ 91 ].

Lastly, Toby Gardner is a Senior Research Fellow from Stockholm Environment Institute, known for his extensive work on Caribbean corals. He co-leads SEI’s Initiative on producer-to-consumer sustainability and the transparency for sustainable economies platform. His long-term observations revealed that the coral cover of the Caribbean basin declined by 80% in just thirty years [ 92 ].

5.3. Emerging Research Disciplines

CiteSpace’s “Category” node type was used to generate a visual map showing research disciplinary categories represented by papers addressing issues related to climate change’s impact on coral reefs. The centrality of a network (i.e., the center of collaborative activities) comprising 135 nodes and 336 links was computed after the data were simplified and merged (i.e., automatically generated from the CiteSpace algorithm and programming) ( Figure 6 ). The five disciplines with the most publications in descending order were marine and freshwater biology, environmental sciences, ecology, oceanography, and geosciences. The study of coral reefs is a multifaceted research topic that includes many fields of study, as demonstrated by the distribution map. Disciplines in related subjects such as biodiversity conservation, geography, physical sciences, biology, evolutionary biology, geology, paleontology, and water resources, show strong connections, represented by the sizes of the nodes. The number of published papers is comparably low in some research disciplines, such as toxicology, biotechnology and applied microbiology, green and sustainable science and technology, and biochemistry and molecular biology. However, the relatively high betweenness centrality values of these fields suggest their significant contribution to interdisciplinary research, signifying their pivotal position in the scientific network. This centrality may also hint at their potential for future development and advancement in the field.

Network of linked research disciplines. The sizes of the modes are proportional to the frequency of the subject category cooccurrence. The thickness of the lines between the two nodes is proportional to the strength of the linkages between the two research disciplines.

5.4. Research Cluster Analysis

Cluster analysis is a popular method of statistical data analysis and knowledge discovery because of its ability to uncover latent semantic themes in textual data [ 93 , 94 ]. Cluster analysis can divide a large body of research data into various units based on the relative degree of term correlation, making it easier to identify the research themes, trends, and connections within a given field of study [ 94 , 95 ]. A cluster’s homogeneity can be quantified using an index called the mean silhouette, with values ranging from −1 to 1. The average silhouette value for each cluster was determined using CiteSpace. The higher the value, the more similar the cluster’s members are to one another [ 96 ]. The network showed 24 clusters in the context of the scientometric analysis mapping the link between climate change and coral reefs ( Figure 7 ).

The reference co-citation research cluster network. Based on a one-year interval, a 24-cluster network of document co-citation with burst detection from 1976 to 2021. Node sizes are proportional to the frequency of the publications’ co-citations.

The largest cluster (#0) has 291 members (i.e., number of publications) and a silhouette value of 0.863 and is labeled as “coral reef.” The most cited article of this cluster is by Gilmour et al. [ 97 ]. They monitored and assessed the impacts of the 2016 heat stress event on Western Australian coral reefs. They found that mass bleaching in 2016 reduced coral cover by 70% at Scott Reef and caused widespread mortality (>30%) at Christmas Island, Ashmore Reef, and inshore reefs in southern Kimberley. A coral phase shift is characterized by a rapid decline in coral abundance or cover and an accompanying rise in non-reef-building organisms, like algae and soft corals [ 98 , 99 ]. The second largest cluster (#1) has 247 members and a silhouette value of 0.876, labeled as “phase shift.” This publication by Brodie et al. [ 100 ], entitled “Terrestrial pollutant run-off to the Great Barrier Reef: An update of issues, priorities and management responses”, is the most cited article in this cluster. They addressed findings from studies of problems caused by surface run-off of pollutants like nitrates from fertilizers, herbicides from crops, etc. Within the cluster of the study, there are three different types of management generated automatically and have mentioned (i) Reef Plant 2009, (ii) Reef Rescue, and the (iii) Reef Protection Package in the analysis. These topics are just some of the initiatives set up to continuously monitor and report on levels of discharges into the Great Barrier Reef. Multiple observations of specific facets of the topic have been published; Hughes [ 101 ]; McManus and Polsenberg [ 102 ]; Idjadi et al. [ 103 ]; Norström et al. [ 104 ]; Graham et al. [ 105 ]; Crisp et al. [ 106 ]. Many anthropogenic stressors have been linked to this phenomenon [ 106 , 107 , 108 ]. Nutrients play a pivotal role in conceptual models of how coral reef communities form. These studies show that corals have a competitive advantage over macroalgae in low nutrient conditions but that the advantage shifts to macroalgae in higher nutrient conditions [ 102 , 109 ]. Siltation, resulting in mud-bacterial complexes, collectively known as “marine snow,” is another factor that hinders coral growth. In addition, excess nutrients resulting in plankton blooms reduce light, thereby inhibiting coral growth [ 110 ].

The fourth largest cluster (#3), “ocean acidification”, has 233 members and a silhouette value of 0.959. The most cited article of this cluster is Bates [ 111 ], which reported twenty years (1996 to 2016) of marine carbon cycle observations at Devils Hole, Bermuda. Her findings shed light on the dynamic nature of biogeochemical processes like primary production, respiration, calcification, and CaCO 3 deposition in the Bermuda reef system. During this period, neither warming nor cooling of any significance was observed. However, increases in inorganic carbon in onshore waters were primarily due to increased salinity (45%), uptake of anthropogenic CO 2 (25%), and changes in Bermuda reef biogeochemical processes (30%). Increases in atmospheric carbon dioxide concentrations result in the absorption of more carbon dioxide by oceans, which in turn causes a decrease in pH [ 112 , 113 , 114 , 115 ]. The majority of research on ocean acidification has focused on the impact of changes in ocean chemistry towards suboptimal states of aragonite and calcite saturation on the calcification processes of pelagic and benthic organisms [ 77 , 116 , 117 , 118 , 119 ]. However, it is likely that ocean acidification also has an effect on other physiological processes, such as growth and reproduction in significant reef-building species [ 77 ].

The Indo-Pacific region’s Coral Triangle, the world’s epicenter of marine biodiversity [ 120 , 121 ], is predicted to become a “marginal” coral habitat between 2020 and 2050 unless CO 2 emissions are reduced [ 122 , 123 ]. In addition to reducing coral diversity, acidification also results in a decline in shellfish and fish species due to the loss of reef structure, which provides habitat for these other species and reduces the reefs’ capacity to mitigate the effects of storm waves and erosion [ 122 , 124 ]. Ocean acidification has a devastating impact on the economies of ocean-dependent sectors of the global economy. Previous studies have provided estimates of the economic impact of ocean acidification on marine mollusk and shellfish production, as well as the bioeconomic costs associated with coral reef damage [ 125 ]. These studies have shed light on the detrimental effects of ocean acidification on marine ecosystems, which in turn, can have severe economic implications. Estimating these costs can aid in developing policies aimed at reducing the negative effects of ocean acidification and promoting the sustainable use of marine resources. For instance, according to a study by Narita et al. [ 126 ], the global annual loss of mollusk production due to the fact of ocean acidification could amount to between USD 6 billion and USD 100 billion. Commercially valuable finfish populations will suffer as a result of global ocean changes that reduce coral reef coverage, resulting in a loss of habitat, reduced availability of prey, and increased predation [ 125 , 127 , 128 ]. The scientometric analysis has identified four prominent clusters, also referred to as topics, which represent distinct research areas based on their geographic location. These clusters include the “central red sea” (#3), the “eastern pacific” (#5), the “great barrier reef” (#8), and the “Dominican Republic” (#18). These geographic regions are frequently cited in scientific research as they represent the study location of many relevant studies.

The most cited article of the “Red Sea” cluster is by Osman et al. [ 129 ], which mapped coral microbiome composition along the northern Red Sea. The Red Sea is a distinctive body of water that is an evaporative basin with a high salinity above 38 ppt [ 130 , 131 ]. It is home to some of the world’s most thriving and productive coral reef ecosystems [ 132 ]. Osman et al. [ 129 ] research offered a fresh understanding of the coral microbiome’s exclusive and endemic characteristics along the northern Red Sea refugia. They looked into the surface mucus layer (SML) for bacterial communities from six dominant coral species and discovered five novel algal endosymbionts. Over the past four decades, the average annual sea surface temperature in most of the world’s tropics and subtropics has risen between 0.4 °C and 1 °C. However, in the central Red Sea, where reef growth and scleractinian coral diversity are abundant, warming is more extensive than the observed mean tropical temperature increase [ 133 ]. The 2010 “Thuwal bleaching” in the central Red Sea was caused by a temperature rise of 10–11 °C, the largest coral bleaching event ever recorded. Furby et al. [ 131 ] conducted a survey and found that the “Thuwal bleaching” event caused more severe bleaching of inshore reefs (74% of hard corals were bleached) than offshore reefs (14% of hard corals were bleached). One mechanism that can lead to higher tolerance is repeated exposure to thermal stress [ 134 , 135 ]. Based on current knowledge, it is hypothesized that the reefs in the Red Sea will be relatively resistant to bleaching as sea temperatures rise, as noted in a study by Grimsditch and Salm [ 136 ]. However, reports indicate that bleaching is beginning to occur in the Red Sea, as documented by Kleinhaus et al. [ 137 ]. For instance, Rich et al. [ 138 ] reported a winter bleaching event in the central Red Sea in January 2020 due to sea surface temperatures (SSTs) falling below 18 °C. Additionally, inshore bleaching events in the central Arabian Red Sea were observed during the “3rd global coral bleaching event” in 2015, as reported by Monroe et al. [ 139 ].

The Eastern Tropical Pacific (ETP) comprises the ocean basin extending from the Gulf of California in México to Peru and includes areas of the continental shelf and offshore islands (Coco Island, the Galápagos Islands, the Revillagigedo Archipelago and Clipperton Atoll). The most cited article of the cluster “Eastern Pacific” is Spencer [ 140 ], which discussed potentialities, uncertainties and complexities in the response of coral reefs to future sea-level rise of reef islands in the Pacific Ocean and the Caribbean Sea. Throughout the Holocene, sea levels rose without being stabilized, and reefs in the Caribbean grew in tandem with these elevation changes [ 141 ]. The once structurally complex coral reefs in the Caribbean have suffered a dramatic decline since the 1970s, with only a minority of reefs maintaining a mean live coral cover of 10% or more [ 142 ]. A strong hurricane season brought on by unusually warm waters in the tropical Atlantic, and the Caribbean in 2005 caused the worst bleaching event ever observed in the basin [ 143 ]. There was a 60% decline in coral cover on reefs in the US Virgin Islands due to the fact of a severe disease outbreak brought on by the 2005 bleaching events in the Caribbean region, as reported by Miller et al. [ 144 ].

The Great Barrier Reef is the largest coral reef ecosystem, with over 348,000 km 2 of coverage consisting of 2900 individual reefs and 900 islands stretching over 2300 kilometers [ 145 ]. Three major coral bleaching events within a span of five years (2016, 2017, and 2020) along with the effects of severe tropical cyclones, poor water quality from catchment run-off, population growth and urbanization, overexploitation of marine resources, and habitat loss have all been the factors towards the degradation of coral reefs in the Great Barrier Reefs [ 56 , 146 ]. Cluster #4, which is the fifth largest cluster, contains 176 publications and has a silhouette value of 0.9. This cluster is strongly associated with cluster #6, “symbiotic dinoflagellate,” and cluster #12, “coral disease”. The high silhouette value of 1.0 indicates that there is a focused field of study in the context of coral reefs and climate change. The most cited article in cluster #4 is by Reaser et al. [ 147 ] on scientific findings and policy recommendations for coral bleaching and global climate change. Coral bleaching, which is the ability of animals with a symbiotic relationship with Symbiodinium to turn white, is an important issue associated with climate change-based literature. According to Douglas [ 148 ], all animals that have a symbiotic association with the dinoflagellate algae of the Symbiodinium genus, which are also referred to as zooxanthellae, have the ability to undergo bleaching. Symbiodinium have been reported to form extracellular symbioses with giant clams and intracellular symbioses with various organisms, including corals, anemones, jellyfish, nudibranchs, ciliophora, foraminifera, zoanthids, and sponges [ 149 , 150 ].

Fujise et al. [ 151 ] reported that the expulsion mechanisms of Symbiodinium were temperature-dependent; however, under non-thermal stress conditions, the expulsions of this algae were part of a regulatory mechanism to maintain a constant Symbiodinium density. In response to moderate thermal stress, Symbiodinium becomes damaged, and corals either selectively digest or expel the damaged cells. During extended periods of thermal stress, damaged Symbiodinium may accumulate in coral tissues, resulting in coral bleaching. Multiple factors have been shown to cause bleaching, including high oxidative stress [ 152 ], intense light [ 153 ], high temperature [ 154 ], low salinity [ 155 ], sedimentation [ 156 ], pollutants [ 157 ], decreased seawater temperature [ 158 ], diseases [ 159 ], bacterial infection [ 160 , 161 ], and ENSO-related marine heatwave events [ 162 , 163 ]. Degree heating weeks (DHW), defined as 1°C above the long-term climate level for the warmest month at a given locality, have become a common global predictor of bleaching [ 164 ]. Severe bleaching is typical at 8 DHW and above [ 165 , 166 ]. A global analysis report of coral bleaching from 1998 to 2017 [ 166 ] found that coral bleaching was most prevalent in regions with high-intensity and high-frequency thermal-stress anomalies. In areas where sea-surface temperature (SST) anomalies varied greatly, such as the Gulf of Aqaba region [ 167 ], the Caribbean Sea [ 168 ], and the Indo-Pacific [ 169 ], coral communities were significantly less susceptible to coral bleaching [ 166 ].

Globally, coral reefs have been threatened by coral disease, which is now recognized as one of the biggest threats to these ecosystems [ 170 ]. Similar to bleaching, coral disease was not considered a severe threat to coral reefs until recently [ 170 ], despite its first documentation in 1965 [ 171 ]. Since their initial descriptions, both the variety of coral diseases and the number of reported cases have skyrocketed [ 172 , 173 ]. Approximately 76% of all coral diseases described worldwide are found within this relatively small basin, leading experts to label the Caribbean a “hot spot” for disease [ 174 ]. For example, two dominant Acropora species in the Caribbean have been replaced by low-encrusting Agaricia due to the fact of coral disease [ 175 , 176 ]. Common coral diseases include Black band disease, which is caused by increased seawater temperature and anthropogenic factors, ciliates cause the Brown band disease, Cyanobacteria cause the Red band disease, and the White plague is caused by a bacterial infection [ 177 ].

5.5. Timeline Co-citation Analysis

The timeline for the document co-citation analysis is an important indicator to explain the period when the study got the attention of the researcher worldwide ( Figure 8 ). From 2010 to 2021, there have been bursts in citations for research clusters on (#0) “coral reefs”, (#2) “ocean acidification”, (#3) “central sea”, (#11) “sea level rise”, and (#5) “eastern pacific”. When taken as a whole, these studies shed light on the growing interest in studying the effects of ocean acidification and sea level rise on coral reefs, with particular attention paid to the plight of these ecosystems within the eastern pacific area, such as in the central Red Sea and the Dominican Republic.

A timeline co-citation analysis. Nodes represent references, whereas lines represent connections between those references. Larger nodes indicate higher frequencies of citations. References with strong citation bursts are shown as red circles, whereas references with high centrality are shown as yellow circles. Longer line segments indicate longer time spans.

5.6. Highly Cited Articles in the Field

CiteSpace’s visualized analysis of 7743 publications yielded a co-citation network (frequency of two different documents are cited together in other documents) with 2525 cited documents (nodes) and 5440 links or connections indicating co-citations between nodes [ 178 ]. The larger the node, the more often a document is cited, demonstrating its impact on coral reef and climate change research. Document co-citation analysis locates essential literature. The given references (in the article) were the most cited among 7743 Web of Science references. Table 4 presents the twenty most cited references based on co-citation analysis along with their frequency, burstiness, and centrality indices. An increase in citations reflects increased interest in that topic. “Citation bursts” demonstrate correlations between publications and sudden increases in citations. When comparing clusters, the centrality index indicates how well they are connected (i.e., coral reef and climate change). An elevated centrality score indicates that the publication is located between two or more sizable subclusters [ 179 ]. Dr. Terry Hughes’s research was widely cited, with three of his Nature and one of his Science publications ranking among the top five most-cited references. The publication entitled Global warming and recurrent mass bleaching of corals topped the list with a frequency index of 546, a burst index of 157 and a centrality index of 0.7. The burst in citation period of this publication was from 2018 to 2021. The findings were based on the third global-scale pan-tropical coral bleaching episode that occurred between 2015 and 2016. The reef ecosystem of eastern and western Australia was studied using aerial and underwater surveys along with sea surface temperatures obtained from satellites. According to their findings, the devastating bleaching event in 2016 was only slightly impacted by water quality and fishing pressure, indicating that local reef protection offers little to no protection against extreme heat.

The second paper on the list, with a frequency index of 359 and burst index of 125, was a global study analyzing the bleaching records of 100 globally distributed reefs from 1980 to 2016 [ 28 ]. According to their findings, mass coral bleaching events happen every year regardless of the presence or absence of El Nino. They forecast that the intervals between recurrent events will eventually become too short to permit a complete recovery of mature coral assemblages, typically taking 10 to 15 years to reach the fastest-growing species. They warned that if temperatures rise by 1.5 or 2 degrees Celsius above preindustrial levels, it will exacerbate the already severe decline of coral reefs around the world. Similar findings were found in another study of his that also appeared on the list of the most-cited research. Research into the effects of climate change on coral reef ecosystems, with a special emphasis on the Great Barrier Reef, ranked fifth [ 28 ]. They found that the Great Barrier Reef’s 2016 record-breaking heatwave had caused widespread loss of functionally diverse corals across the reef’s most remote and pristine regions. Ranked third on the list was the study by Hoegh-Guldberg et al. [ 22 ], which investigated the effects of climate change and ocean acidification on coral reefs. This study was closely linked to the 3rd (#2) research cluster, also known as “ocean acidification”. The research review presented future scenarios for coral reefs, which suggested increasingly detrimental impacts on various sectors, including tourism, coastal protection, and the fisheries industry. These predictions were based on the assumption that global temperatures would rise by at least 2 °C between 2050 and 2100, coupled with atmospheric carbon dioxide concentrations exceeding 500 ppm. The findings of this study emphasize the urgent need for effective measures to mitigate climate change and ocean acidification to ensure the long-term survival and sustainability of coral reefs and the associated ecosystems. The article by LaJeunesse et al. [ 180 ] on coral endosymbionts has garnered significant attention, with a citation frequency of 134, a burst index of 68, and a burst period spanning from 2013 to 2017. This publication is associated with cluster (3), also known as “symbiotic dinoflagellate”. The article describes Symbiodinium clades and proposes that the divergent evolutionary Symbiodinium “clades” correspond to genera within the Symbiodiniaceae family. The study affirms that the long evolutionary history of the Symbiodiniaceae family is appropriately acknowledged within the suggested framework. The findings of this study provide valuable insights into the evolutionary relationships and ecological functions of these endosymbionts, highlighting the critical role they play in the health and survival of coral reefs.

The list of 11 to 20 top-cited articles on climate change on coral reefs cover a wide range of topics, including ocean acidification, declining coral cover, Symbiodinium diversity, and coral reef resilience. Several studies indicate that warming trends and bleaching stress are increasing, and coral bleaching protection mechanisms are becoming less effective, ultimately leading to significant declines in coral populations. Research on the impacts of ocean acidification and warming on marine organisms, as well as the interactions between these factors, has also shed light on the mechanisms underlying the sensitivity of coral reefs to climate change [ 79 , 181 , 182 ]. Studies on the diversity, distribution and stability of Symbiodinium [ 183 ] have provided insights into the potential for coral resilience, while research on the decline of coral cover in the Indo-Pacific region has highlighted the extent and timing of this phenomenon [ 183 , 184 ]. These studies demonstrate that collaborative research efforts are essential to understanding the impacts of climate change on coral reefs and developing more efficient conservation and management strategies.

5.7. Distribution of Keywords

Using the co-cited keyword analysis performed in CiteSpace, 963 unique keywords were generated. In order to better understand the connections between these terms, a clustering tool was used to categorize them into groups ( Figure 9 ). This generated seven major clusters consisting of “sea surface temperature”, “Symbiodinium”, “coral reef fish”, “marine protected area”, “water quality”, “ocean acidification”, and “hydrocorals”. Each of these clusters can be analyzed independently to determine which descriptors are most applicable. The major keywords used to discuss “sea surface temperature”—record, Indian ocean, and reef; “Symbiodinium”—scleractinian coral, diversity, zooxanthellae, population, nutrient enrichment, elevated pressure, and oxidative stress; “coral reef fish”—phase shift, ecosystem, disturbance, fish, dynamics, community, recruitment, abundance, thermal tolerance, Stylophora pistillata , and ecology; “marine protected area”—management, assemblage, biodiversity, susceptibility, degradation, adaptation, response, and recovery; “water quality”—sea level, Great barrier reef, rate, transport, coral bleaching, French Polynesia, and fringing reef; “ocean acidification”—climate, El Niño, impact temperature, coral reef, calcification, and carbon; and “hydrocorals”—seawater and carbon dioxide.

Distribution of co-cited keywords in the field of coral reef and climate change.

Table 5 displays the top 10 keywords with the strongest citation burst. With the exception of “ocean warming,” all the most frequently cited keywords emerged in the early 1990s and experienced a citation burst that extended until the late 2000s. The keywords identified were “French Polynesia,” “record,” “El Niño,” “Australia,” “Indian Ocean,” “Continental,” “Shelf,” “Sea level,” “Sea surface,” “temperature,” and “Island.” Notably, the keyword “ocean warming” only gained popularity in 2017, with citations peaking from 2018 to 2021. This demonstrates the significance of research on climate-related temperatures in the field of coral reefs and climate change. The keywords “Australia” and “Continental shelf” demonstrated citation bursts lasting over 15 years. In contrast, “French Polynesia” had the highest frequency of citations during a relatively shorter period, commencing in 1992 and concluding in 2006. French Polynesia, situated in the westernmost region of the South Pacific, comprises 118 islands and atolls, classified into five main clusters: the Marquesas, Society, Tuamotu, Gambier, and Austral islands [ 191 ]. These regions exhibit a north–south gradient for variables such as sea surface temperature (SST), solar insolation, evaporation, and humidity. The Millennium Coral Reef Mapping Project (MCRMP) has successfully mapped the Austral, Gambier, Society, and Tuamotu islands and atolls; however, significant research remains to be undertaken in this extensive region, which accounts for the enduring citation burst for this keyword. The findings of this study highlight the scientific interest and importance of French Polynesia as a unique and diverse region for further research and conservation efforts.

Top 10 keywords with the strongest citation bursts.

5.8. Dual Map Overlay

Figure 10 illustrates the dual-map overlay of the number of articles pertaining to the type or focus of the journal. The map labels represent the research subjects covered by the journals, with the citing journals displayed on the left side and the cited journals on the right. The trajectory of the citation links provides valuable insights into inter-specialty relationships. A shift in trajectory from one region to another would indicate the influence of articles from another discipline on a specific field. In the domain of coral reef and climate change interaction, the dominant fields were found to be “ecology, earth, and marine”. The most influential discipline was “plant, ecology, and zoology”, with a z-score of 7.66, followed by “earth, geology, and geophysics”, with a z-score of 4.99 and, lastly, “molecular, biology, and genetics”, with a z-score of 2.80. These findings provide a valuable understanding of the interdisciplinary relationships within the field of coral reef and climate change research, highlighting the influence of various disciplines in shaping the current research landscape.

Dual-map overlay on the impact of climate change on coral reefs research.

6. General Discussions

Coral reefs are a vital marine ecosystem service, providing high biodiversity and supporting the livelihoods of coastal communities. However, ocean warming and temperature are the largest threats to corals from anthropogenic climate change [ 192 ]. Between 1997 and 2018, the global average percentage of coral cover was approximately 32%, but by 2100, RCP 8.5 predicts a global decline in coral cover of 5 and 15%, equating to a relative global decline of more than 40% [ 115 , 193 ]. This decline is due to the fact that sea surface temperatures (SSTs) are projected to increase by more than 3 °C by the turn of the century [ 194 ]. These declines could have significant ecological and socioeconomic impacts, particularly in coastal communities that rely on coral reefs for food, tourism, and other ecosystem services.

For example, The Republic of Palau, a small Micronesian nation, has already experienced significant losses in coral reef cover [ 195 ]. Over 87% of Palau’s households are linked to coral reef-associated activities, which are critical to the country’s economic and social well-being. While tourism, particularly ecotourism, is a significant contributor to GDP growth, tax revenue, and employment, climate change-related stressors have caused a steady decline in coral reef cover. This decline has indirectly caused a major decline in tourism, threatening the country’s economic sustainability [ 196 ]. According to Barnett [ 197 ], climate change is a significant threat to food security for people in Pacific SIDS, primarily due to the decline in fisheries output resulting from the impact of climate change on total coral cover.

Apart from impacting the socioecological structure, the impact of climate change can have cascading effects on the entire reef ecosystem, affecting the abundance and diversity of other marine species that depend on corals for food and shelter. Up to 14% of species may be in imminent danger of extinction at a warming of 1.5 °C and up to 29% at a warming of 3 °C. This rise in ocean temperature will probably force coral to colonize higher latitudes that currently lack reefs [ 198 , 199 , 200 ]. However, various factors, including the need for a suitable substrate [ 201 ], connectivity to other reefs [ 202 ], ocean acidification [ 203 ], and light intensity [ 204 ], may outweigh the advantages of reefs as they expand to high latitudes [ 193 ].

Through the timeline co-citation analysis, we have observed a significant increase in research interest in the topic of climate change impacts on coral reefs between 2010 and 2022. The analysis identified several research clusters that gained traction in the scientific community, including those related to “coral reefs,” “ocean acidification,” “central red sea”, “Great Barrier Reef”, and “sea level rise”. These clusters have evolved to become research hotspots under the overarching topic of climate change impacts on coral reefs. For example, the research clusters related to the central red sea and the Great Barrier Reef have emerged as prominent research areas, given their unique characteristics and ecological importance. Similarly, the impact of ocean acidification and sea level rise on coral reefs has gained significant research interest, given their severe consequences on the health and survival of coral reefs. To better understand the impact of these research clusters, our overall discussions have been designed to incorporate the subtopics “climate change threats to coral reefs” and “adaptive strategies for coral resistance and resilience”.

6.1. The Threat of Climate Change to Coral Reefs: Investigating the Impacts of Temperature and Ocean Acidification

Climate-induced changes in temperature are a major threat to coral reef ecosystems, and extensive research has highlighted several key areas for investigation [ 53 , 205 ], with marine heatwaves, solar radiation, heat tolerance, and thermal thresholds representing the most promising areas for future research. Marine heat waves have become increasingly prevalent and intense as a result of climate change. These extreme events, characterized by prolonged periods of elevated water temperatures, significantly impact coral reef ecosystems. For instance, the mass global coral bleaching event of 2016–2017 was the most extensive and long lasting on record, as documented by Eakin et al. [ 206 ]. The event, which was associated with the El Niño Southern Oscillation (ENSO), had varying impacts on coral reefs worldwide [ 207 ], with some regions experiencing more severe bleaching than others, as reported by Kim et al. [ 208 ].

Corals are thermophilic, but their thermal tolerance is narrowly defined [ 169 , 209 ]. For instance, the rate of calcification increases with temperature up to a threshold level, beyond which it declines [ 210 , 211 , 212 ]. Tropical corals live close to their upper thermal limits and are, therefore, highly sensitive to periods of elevated sea surface temperatures and ocean warming [ 187 , 213 ]. Coral reefs in the Persian Gulf have been observed to have the highest upper-temperature thresholds of approximately 35–36 °C [ 214 ]. However, it has also been noted that these corals remain highly vulnerable to thermal stress when temperatures surpass their local maximum summer temperatures [ 215 ]. The escalating frequency and gravity of thermally induced mass bleaching events have sparked worldwide attention to the elevated temperature impacts on corals [ 28 ]. As a result, research endeavors have focused on establishing maximum thermal tolerance thresholds and variations in diverse coral species and regions and exploring potential coral refugia to brace for future ocean warming [ 216 ].

Corals rely on their symbiotic relationship with unicellular algae of the genus Symbiodinium for photosynthesis, and over 90% of their energy budget is needed for essential functions, such as calcification, tissue growth, and reproduction [ 212 ]. This critical association is threatened when corals experience thermal stress, such as elevated sea surface temperatures (SST), resulting in coral bleaching, where the algal endosymbionts are expelled. The resulting impairment and expulsion of the algal symbionts are linked to reactive oxygen species (ROS) generation from the host, the algal symbiont, or both, triggering a host immune response [ 217 ].

Protracted coral bleaching can lead to extensive coral mortality, severely affecting the ecosystem and associated reef fauna. Based on the timeline cocitation analysis, it was evident that the Red Sea (Cluster #3) and Great Barrier Reef (GBR) (cluster #8) are major research hotspots in terms of geographic regions. Although the Persian Gulf is a hot sea that supports coral reef ecosystems, the Red Sea harbors corals with greater thermal stress tolerance, with some coral genotypes capable of surviving temperatures over 5 °C above their summer maxima [ 216 , 218 ]. Corals in the southern end of the Red Sea are more heat resistant, surviving prolonged high temperatures, while the northern Red Sea benefits from heat-resistant genotypes that have migrated from the south [ 219 ]. The importance of broad latitudinal temperature gradients in promoting adaptation to high temperatures and exchanging heat-resistant genotypes across latitudes for genetic rescue in coral reefs is exemplified in the evolutionary history of coral reefs in the northern Red Sea [ 9 , 216 ]. On the other hand, the GBR, known as the world’s largest coral ecosystem, was severely impacted by the 2015–2016 climate change-amplified strong El Niño event that triggered the warmest temperatures on record. This resulted in a massive bleaching event affecting nearly 90% of reefs along the northern region, leading to a loss of approximately 30% of live coral cover in the following six months [ 28 , 220 , 221 ]. Research has increasingly linked climate change to a rise in coral diseases. Bruno et al. [ 222 ] used a high-resolution satellite dataset to investigate the relationship between temperature anomalies and coral disease on a large spatial scale of 1500 km in Australia’s Great Barrier Reef. Their findings showed a significant positive correlation between warm temperature anomalies and the incidence of the white syndrome, an emergent disease in Pacific reef-building corals. In a similar vein, Tignat-Perrier et al. [ 223 ] noted a decline in populations of two gorgonian species ( Paramuricea clavata and Eunicella cavolini ) found in the Mediterranean Sea due to the fact of microbial diseases during thermal stress events. These studies illustrate the growing concern that climate change is contributing to the increased incidence and severity of coral diseases, which could ultimately lead to a decline in the health of marine ecosystems.

In the past, studies on the impact of climate change on coral reefs primarily centered on the thermal tolerance of corals and the consequences of massive, abrupt coral loss on organisms associated with reefs [ 224 ]. However, research has recently shifted towards investigating the distinct and synergistic effects of ocean warming and ocean acidification resulting from increased atmospheric CO 2 levels. The timeline co-citation analysis reveals that these emerging research fields are highly significant with recent citation bursts, as evidenced by their identification as Cluster #2 (Ocean acidification) and Cluster #10 (Elevated CO 2 ), respectively.

The escalation of atmospheric carbon dioxide (CO 2 ) concentrations has resulted in ocean acidification, which is among the foremost threats to coral reef ecosystems. Forecasts for 2100 anticipate a rise in CO 2 concentrations to between 540 and 970 ppm, leading to a global decrease in seawater pH by 0.14 to 0.35 units [ 31 , 68 , 116 , 225 ]. As demonstrated by Fabricius et al. [ 68 ], ecological traits of coral reefs will gradually transform as seawater pH decreases to 7.8, and a decline below this level (at 750 ppm pCO 2 ) would be catastrophic for these ecosystems. Ocean acidification reduces the availability of carbonate ions that corals require to form their calcium carbonate skeletons, ultimately leading to a decrease in coral calcification rates [ 33 ]. Ocean acidification has also been shown to decrease the ability of coral larvae to settle and survive [ 226 ] and increase their susceptibility to disease [ 227 ]. Research has shown that even modest increases in ocean acidity can impact the physiological processes of corals. For example, exposure to high levels of CO 2 reduces coral growth and calcification rates [ 68 , 226 ]. In addition to the direct effects on coral physiology, ocean acidification can have cascading impacts on the entire coral reef ecosystem. For instance, reduced calcification by corals can reduce the complexity of the coral reef structure, potentially leading to the loss of important habitats for fish and other marine organisms [ 228 ]. Furthermore, ocean acidification can impact the symbiotic relationship between corals and their algal symbionts, potentially leading to a decline in the productivity of the reef ecosystem as a whole [ 229 ]. The combination of ocean warming and acidification is particularly concerning, as they act synergistically to exacerbate the negative impacts on coral reef ecosystems [ 22 ]. With continuing increases in atmospheric CO 2 levels, the effects of ocean acidification on coral reefs are expected to become even more pronounced, highlighting the need for urgent action to reduce greenhouse gas emissions and protect these valuable and vulnerable ecosystems.

The rate of atmospheric CO 2 increase continues to accelerate, with emission scenarios predicting CO 2 concentrations of 540–970 ppm and a decline in seawater pH by 0.14–0.35 units globally for 2100 [ 68 , 225 ]. Fabricius et al. [ 68 ] demonstrated that many ecological properties in coral reefs will gradually change as pH declines to 7.8 and that it would be catastrophic for coral reefs if seawater pH dropped below 7.8 (at 750 ppm pCO 2 ).

6.2. Adaptive Strategies for Enhancing Coral Resistance and Resilience in the Face of Climate Change

Coral resistance and resilience are scientific constructs that pertain to the capacity of coral reefs to withstand and recuperate from various stressors. Coral resistance is defined as the ability of corals to endure or tolerate perturbations and stressors, such as variations in water temperature, ocean acidification, pollution, and physical injury. Corals that possess a greater resistance to these stressors exhibit a greater ability to sustain their structure and function despite disturbances and are less prone to suffering from coral bleaching, disease, or mortality [ 229 , 230 ]. A myriad of studies has reported on the bleaching thresholds of corals inhabiting the Persian Gulf, despite conditions at least 2 °C higher than other coral reef ecosystems worldwide [ 231 ]. Additionally, corals from the Indo-Pacific and Caribbean regions have been found to maintain calcification rates even in low aragonite saturation states, present in naturally acidified locales [ 68 , 232 ]. The eastern Pacific region of Palau has revealed the thriving of reefs in waters with natural acidification, resulting from biological processes and reef system circulation patterns [ 232 , 233 ]. However, it is noteworthy that coral communities in Palau’s relatively acidic reef zones developed over thousands of years, fostering an inherent resistance that differs from coral communities in regions affected by higher anthropogenic interventions.

Coral resilience, in contrast, refers to the ability of coral reefs to recover from disturbances and stressors. Corals that exhibit higher resilience can reproduce, regenerate, and rebuild their structural complexity after experiencing bleaching [ 234 ]. These mechanisms are attributable to genetic diversity within coral populations and their symbiotic association with Symbiodinium algae, which are critical to their health and survival [ 235 , 236 ]. Genetic adaptation in corals is mediated through various factors, including the activation of heat-shock proteins, oxidoreductase enzymes, and microsporine-like amino acids. The coral surface micro-layer that absorbs UV radiation has also been identified as a significant mechanism for adaptation [ 180 , 237 , 238 ]. In-depth research on corals that thrive in the warm waters of the Persian Gulf has demonstrated their capacity for resilience, attributable to metabolic trade-offs, unique physiological characteristics, and specific genetic signatures, including a heat-specialist algal endosymbiont, Symbiodinium thermophilum [ 236 , 239 ]. S. thermophilum can thrive in high-temperature and high-salinity environments, allowing the coral to develop a temperature-stress-resistant phenotype [ 239 ].

Symbiodinium, a diverse group of dinoflagellates, is classified into nine clades (A–I) based on their phylogenetic characteristics [ 240 ]. Among these clades, Symbiodinium clade D has garnered attention for its exceptional thermal resilience ability, despite its relatively low representation (less than 10%) in the endosymbiotic community of coral hosts [ 241 ]. Various coral species, including fast-growing branching types, such as Acropora, Stylophora, and Pocillopora, as well as slow-growing massive, encrusting, and solitary corals, have been associated with Symbiodinium clade D [ 242 ]. The prevalence of clade D Symbiodinium in corals from the Persian Gulf has been linked to their higher thermal tolerance, particularly in comparison to corals associated with clade C, which is the dominant lineage in corals from the Great Barrier Reef and other Pacific coral reef ecosystems [ 243 ], and clade B in corals from the Atlantic [ 244 ]. These findings highlight the significance of Symbiodinium diversity in understanding the thermal resilience of coral reefs and the potential mechanisms underlying their adaptation to changing environmental conditions.

McCulloch et al. [ 234 ] explored the ability of coral species to withstand the adverse impacts of ocean acidification and global warming on coral reefs. Their study revealed that some coral species (i.e., Stylophora pistillata and Porites spp.) exhibit the capacity to increase pH levels within their calcifying fluid, crucial for the deposition of calcium carbonate and maintenance of the coral structure, even in the face of declining seawater pH levels. The study demonstrated the significance of acid-base regulation mechanisms for corals’ resilience to the effects of ocean acidification, allowing them to maintain or increase their calcification rates despite rising ocean acidification. Moreover, the study indicated that corals could acclimate to extended acidification, which enables them to maintain or increase their calcification rates by upregulating their internal pH levels, thus providing insight into potential strategies for mitigating the effects of climate change on coral reefs. A similar adaptation resilience strategy against ocean acidification was observed in cold-water scleractinian corals (i.e., Caryophyllia smithii , Desmophyllum dianthus , Enallopsammia rostrata , Lophelia pertusa , and Madrepora oculate ) [ 245 ].

Oceanographic processes, such as upwelling and tidal currents, also play a significant role in helping corals avoid bleaching. In areas where upwelling events mix deeper, cooler water with shallow warmer water, thermal stress is reduced [ 246 , 247 ]; for example, in northern Galapagos during the 2015/16 ENSO [ 248 ] and Nanwan Bay, southern Taiwan, during summer [ 249 ]. Similarly, a coral reef’s ability to resist bleaching is bolstered by the elimination of potentially damaging oxygen radicals due to the swift water flow associated with tidal currents [ 230 , 250 , 251 ].

Therefore, in summary, the scientific community has identified various adaptive strategies that could enhance the resilience and resistance of coral reefs to these challenges. Going forward, it is crucial to continue ongoing research efforts to better understand the mechanisms underlying coral resilience and resistance, identify research gaps, and develop new management strategies for protecting these vital ecosystems. This can be achieved through a multidisciplinary approach that combines laboratory-based experimentation, field research, and community engagement. In addition, collaborations between the scientific community and policymakers can facilitate the implementation of evidence-based management practices that promote the resilience and resistance of coral reefs to climate change and other stressors.

7. Conclusions

The scientometric analysis that is presented in this article demonstrates that research on coral reefs in relation to climate change has emerged as one of the potential fields, with interest in this topic has grown steadily since the 2000s. The increasing global temperatures are posing a significant threat to coral reefs, leading to widespread coral bleaching and mortality. Moreover, changes in ocean chemistry brought on by an increase in carbon dioxide levels lead to ocean acidification, which can worsen the effects of rising temperatures on corals [ 22 ]. In addition, sea level rise and coastal development are transforming the physical structure of coral reef ecosystems, exacerbating the negative effects of the other stressors [ 252 ]. These changes are harmful not only to the coral reefs but also to the plethora of species that rely on them for survival and the communities that rely on them for livelihoods and for protecting the coast. Future challenges for developing countries like those within the coral reef triangle initiative (i.e., Indonesia, Malaysia, the Philippines, Papua New Guinea, Timor Leste, and the Solomon Islands) will center on access to funding for conservation-restoration efforts and continued monitoring studies. There are several ways that ongoing research and coordinated action can help coral reefs cope with the effects of climate change:

• Monitoring: Regular coral reef monitoring can reveal vital details about the well-being and state of the reefs as well as the effects of climate change. These data can be used to pinpoint especially vulnerable regions and monitor long-term changes. Scientists and environmentalists can detect early warning signs of coral bleaching and other detrimental effects by monitoring coral reefs, which enables them to take action before it is too late;
• Research: Collaborative research efforts can contribute to a better understanding of the impacts of climate change on coral reefs and the mechanisms underlying these impacts and can also aid in developing and rigorously testing intervention and restoration techniques for coral reefs. Given that the preservation of coral reef ecosystems requires a range of interventions, including biological, ecological, and social strategies for mitigation and adaptation [ 19 ], such research can help create more efficient restoration, conservation and management strategies;
• Conservation and management: Collaborative conservation and management efforts can assist in mitigating the effects of climate change on coral reefs. Protected areas and marine reserves, for instance, can aid in mitigating the effects of overfishing and pollution, thereby making coral reefs more resilient to the effects of climate change;
• Mitigation: joint efforts can also aid in lowering atmospheric greenhouse gas concentrations, which are primarily responsible for climate change, for instance, by collaborating with regional organizations and authorities to advance sustainable development and lower carbon emissions;
• Public education and awareness: Raising public understanding of the effects of climate change on coral reefs can encourage support for management and conservation initiatives.

Funding Statement

The present study was supported by the Department of Higher Education, Ministry of Higher Education Malaysia, under the LRGS program (LRGS/1/2020/UMT/01/1; LRGS UMT Vot No. 56040) entitled “Ocean Climate Change: Potential Risk, Impact and Adaptation Towards Marine and Coastal Ecosystem Services in Malaysia’. The work was also supported by PASIFIC program GeoReco project funding from the European Union’s Horizon 2020 Research and Innovation programme, under the Marie Sklodowska-Curie grant agreement No. 847639, and from the Ministry of Education and Science.

Author Contributions

Conceptualization, C.S.T. and M.N.A.; methodology, M.N.A.; software, C.S.T.; validation, J.B., Z.V.-G. and V.R.; formal analysis, F.L.; investigation, G.S.; resources, I.G.; data curation, J.B.; writing—original draft preparation, C.S.T.; writing—review and editing, M.N.A.; visualization, F.L., G.S., I.G., V.R. and Z.V.-G.; supervision, M.N.A.; project administration, G.S.; funding acquisition, J.B., Z.V.-G., V.R. and I.G. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Data availability statement, conflicts of interest.

The authors declare no conflict of interest.

Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Deep parts of Great Barrier Reef 'insulated' from global warming -- for now

Some deeper areas of the Great Barrier Reef are insulated from harmful heatwaves -- but that protection will be lost if global warming continues, according to new research.

High surface temperatures have caused mass "bleaching" of the Great Barrier Reef in five of the last eight years, with the latest happening now.

Climate change projections for coral reefs are usually based on sea surface temperatures, but this overlooks the fact that deeper water does not necessarily experience the same warming as that at the surface.

The new study -- led by the universities of Exeter and Queensland -- examined how changing temperatures will affect mesophotic corals (depth 30-50 metres).

It found that separation between warm buoyant surface water and cooler deeper water can insulate reefs from surface heatwaves, but this protection will be lost if global warming exceeds 3°C above pre-industrial levels.

The researchers say similar patterns could occur on other reefs worldwide, but local conditions affecting how the water moves and mixes will mean the degree to which deeper water coral refuges exist and remain insulated from surface heatwaves will vary.

"Coral reefs are the canary in the coalmine, warning us of the many species and ecosystems affected by climate change," said Dr Jennifer McWhorter, who led the research during a QUEX PhD studentship at the universities of Exeter and Queensland.

"Coral bleaching is a dramatic sign of the impact humans are having on the planet.

"Our study offers both hope and a warning -- hope that some reefs are resilient to current levels of climate change, and a warning that this resilience has its limits."

The study finds that 3°C of global warming would push mesophotic temperatures in the Great Barrier Reef past 30°C -- a recognised threshold for coral mortality.

This does not necessarily mean that all coral would die, but it would place the reef in a state of stress that would increase mortality and possibly cause it to collapse.

Dr McWhorter, now at NOAA's Atlantic Oceanographic & Meteorological Laboratory, said: "Some shallow-water species are not found in deeper areas -- so mesophotic reefs can't provide refuges for them as shallow reefs are degraded.

"And, as our study shows, mesophotic corals are themselves threatened if global warming continues."

To calculate their projections of mesophotic reefs warming, the research team considered factors such as wind and tidal mixing of water, and local complexities.

They estimate that, by 2050-60, bottom temperatures on the Great Barrier Reef (30-50 metres) will increase by 0.5-1°C under lower projected greenhouse gas emissions, and 1.2-1.7°C under higher emissions.

Dr Paul Halloran, from Exeter's Global Systems Institute, said: "To protect coral reefs, we need to understand them better.

"Reefs face multiple threats -- not just climate change. By targeting management of these threats on reefs that have the best chance of escaping the worst impacts of climate change, hopefully some healthy reefs can be maintained.

Professor Peter Mumby, from the University of Queensland, said: "There is so much to learn about deeper, tropical coral reefs, especially as we cannot assume that their depth provides a persistent refuge from the consequences of rising global carbon emissions."

• Global Warming
• Coral Reefs
• Environmental Issues
• Environmental Awareness
• Gulf Stream
• Global warming
• Sulfur hexafluoride
• Global warming controversy
• Artificial reef
• Climate change mitigation

Story Source:

Materials provided by University of Exeter . Original written by Alex Morrison. Note: Content may be edited for style and length.

Journal Reference :

• Jennifer K. McWhorter, Paul R. Halloran, George Roff, Peter J. Mumby. Climate change impacts on mesophotic regions of the Great Barrier Reef . Proceedings of the National Academy of Sciences , 2024; 121 (16) DOI: 10.1073/pnas.2303336121

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Deep parts of Great Barrier Reef 'insulated' from global warming, for now

by University of Exeter

Some deeper areas of the Great Barrier Reef are insulated from harmful heat waves—but that protection will be lost if global warming continues, according to new research.

High surface temperatures have caused mass "bleaching" of the Great Barrier Reef in five of the last eight years, with the latest happening now.

Climate change projections for coral reefs are usually based on sea surface temperatures , but this overlooks the fact that deeper water does not necessarily experience the same warming as that at the surface.

A new study—led by the universities of Exeter and Queensland—examined how changing temperatures will affect mesophotic corals (depth 30–50 meters). The paper, published in the journal Proceedings of the National Academy of Sciences , is titled, "Climate change impacts on mesophotic regions of the Great Barrier Reef."

It found that separation between warm buoyant surface water and cooler deeper water can insulate reefs from surface heat waves, but this protection will be lost if global warming exceeds 3°C above pre-industrial levels.

The researchers say similar patterns could occur on other reefs worldwide, but local conditions affecting how the water moves and mixes will mean the degree to which deeper water coral refuges exist and remain insulated from surface heat waves will vary.

"Coral reefs are the canary in the coalmine, warning us of the many species and ecosystems affected by climate change," said Dr. Jennifer McWhorter, who led the research during a QUEX Ph.D. studentship at the universities of Exeter and Queensland.

"Coral bleaching is a dramatic sign of the impact humans are having on the planet.

"Our study offers both hope and a warning—hope that some reefs are resilient to current levels of climate change, and a warning that this resilience has its limits."

The study finds that 3°C of global warming would push mesophotic temperatures in the Great Barrier Reef past 30°C—a recognized threshold for coral mortality.

This does not necessarily mean that all coral would die, but it would place the reef in a state of stress that would increase mortality and possibly cause it to collapse.

Dr. McWhorter, now at NOAA's Atlantic Oceanographic & Meteorological Laboratory, said, "Some shallow-water species are not found in deeper areas—so mesophotic reefs can't provide refuges for them as shallow reefs are degraded.

"And, as our study shows, mesophotic corals are themselves threatened if global warming continues."

To calculate their projections of mesophotic reefs warming, the research team considered factors such as wind and tidal mixing of water, and local complexities.

They estimate that, by 2050–60, bottom temperatures on the Great Barrier Reef (30–50 meters) will increase by 0.5–1°C under lower projected greenhouse gas emissions, and 1.2–1.7°C under higher emissions.

Dr. Paul Halloran, from Exeter's Global Systems Institute, said, "To protect coral reefs, we need to understand them better.

"Reefs face multiple threats—not just climate change. By targeting management of these threats on reefs that have the best chance of escaping the worst impacts of climate change, hopefully some healthy reefs can be maintained.

Professor Peter Mumby, from the University of Queensland, said, "There is so much to learn about deeper, tropical coral reefs, especially as we cannot assume that their depth provides a persistent refuge from the consequences of rising global carbon emissions."

Journal information: Proceedings of the National Academy of Sciences

Provided by University of Exeter

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Great Barrier Reef

The biodiversity of the Great Barrier Reef is threatened. Scientists are working to find ways to protect it.

Biology, Ecology, Earth Science, Climatology

barrier reef

Coral reefs like the Great Barrier Reef off the coast of Queensland, Australia, support diverse marine populations in unique underwater ecosystems.

Photograph by vlad61

The Great Barrier Reef , which extends for over 2,300 kilometers (1429 miles) along the northeastern coast of Australia, is home to over 9,000 known species. There are likely many more—new discoveries are frequently being made, including a new species of branching coral discovered in 2017. This richness and uniqueness make the reef crucial for tourism and the Australian economy—it attracts at least 1.6 million visitors every year. Yet the reef’s true value, its biodiversity, extends far beyond dollars and cents.

The Great Barrier Reef consists of about 3,000 individual reefs of coral, and the biodiversity they contain is remarkable. There are animals you would probably recognize, such as dolphins, turtles, crocodiles, and sharks. There are also venomous sea snakes, brightly colored worms, and large algae. These species interact to form a complex and delicate ecosystem dependent on the coral reef for survival. Yet today the coral—and therefore all the organisms that depend on it—is gravely at risk.

Coral is made up of many small animals. These tiny animals build a hard external skeleton to make the vibrant structures that we recognize. When healthy, coral has a symbiotic relationship with algae. The coral produces fluorescent chemicals that protect the algae from bright sun—almost like a sunscreen. The algae use photosynthesis to harness solar energy to make sugars. In this way, the algae provide food and oxygen (a byproduct of photosynthesis) for the coral, and the coral protects and provides nutrients for the algae. The algae also give coral its many colors.

The coral and algae have evolved together to survive within a particular temperature range. As sea temperatures rise due to climate change , the algae begin to produce products toxic to the coral , which in turn expel the algae. This process is called bleaching because the coral becomes white. A 2018 study showed that about one-third of the Great Barrier Reef had experienced substantial damage from bleaching. The researchers also found that large amounts of coral had died in the warming water almost immediately—even before there was time to expel their algal partners. This suggests even greater risks from climate change than scientists had previously thought.

Climate change is not the only threat to the reef. Chemical runoff and other forms of pollution , coastal development, and overfishing all can harm coral and reduce biodiversity. So can large storms such as cyclones. Species that live in the reef can also cause damage. One major pest species is the crown-of-thorns starfish (Acanthaster planci) . A starfish may sound harmless, but these venomous creatures voraciously eat coral. Every so often, their numbers spike. Some scientists think these starfish caused over half of the reef damage from 1985 to 2012.

Fortunately, many people are passionate about protecting the Great Barrier Reef. National Geographic Explorer Dr. Erika S. Woolsey conducts research on coral reefs. Dr. Woolsey is the CEO of the nonprofit organization, The Hydrous. (The adjective hydrous means “containing water.”) Woolsey and her colleagues use virtual reality to create 3D versions of specimens that can be viewed in a laboratory. Scientists can see damage to the reef over time and take detailed measurements of every nook and cranny—without having to get wet! People around the world can access images of reef structures to study, thereby contributing to our knowledge of the reef.

So, is there still hope for the Great Barrier Reef? People are making a determined effort to help, and there are things that you can do right at home. Because climate change is an important cause of damage to the reef, efforts to fight it matter. In 2015, 195 countries signed the Paris Climate Agreement, committing to work to reduce carbon emissions and taking other steps to address climate change. You can contact your representatives in Congress to urge the United States to rejoin the Paris Climate Agreement.

You can also make changes in your own life to use less energy, produce less waste, choose environmentally friendly products, and be informed. Even your diet can make a difference: eating locally sourced foods that don’t have to be shipped to your neighborhood reduces carbon emissions. You can even be a citizen scientist and collect data for scientists if you visit the reef.

In a 2017 presentation, Dr. Woolsey explained why it is so important to protect reefs: “ Coral reefs . . . provide food and livelihoods for hundreds of millions of people around the world, they protect shorelines from erosion, and they contain compounds that are used to treat human ailments. . . . Even though they cover less than one percent of the sea floor, they harbor about a quarter of all marine biodiversity.”

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• Description

The Great Barrier Reef is a site of remarkable variety and beauty on the north-east coast of Australia. It contains the world’s largest collection of coral reefs, with 400 types of coral, 1,500 species of fish and 4,000 types of mollusc. It also holds great scientific interest as the habitat of species such as the dugong (‘sea cow’) and the large green turtle, which are threatened with extinction.

Description is available under license CC-BY-SA IGO 3.0

La Grande Barrière

Au nord-est de la côte australienne, le plus grand ensemble corallien du monde offre, avec ses 400 espèces de coraux, ses 1 500 espèces de poissons et ses 4 000 espèces de mollusques, un spectacle d’une variété et d’une beauté extraordinaires et d’un haut intérêt scientifique. C’est aussi l’habitat d’espèces menacées d’extinction, comme le dugong et la grande tortue verte.

حاجز الشعب المرجانية الكبير

في شمال شرق الساحل الأسترالي، تجد أكبر مجمع مرجاني في العالم يعرض، بالإضافة إلى أجناسه ال400 من المرجان، 1500 نوع من أنواع السمك و 4000 نوع من الحيوانات الرخوية ضمن مشهد كثير التنوع والجمال وشديد الأهمية من الناحية العلمية. إنه أيضاً مسكن لأجناس مهدّدة بالانقراض مثل الدودونغ والسلحفاة الخضراء الكبيرة.

source: UNESCO/CPE Description is available under license CC-BY-SA IGO 3.0

大堡礁位于澳大利亚东北海岸，这里物种多样、景色迷人，有着世界上最大的珊瑚礁群，包括400种珊瑚、1500种鱼类和4000种软体动物。大堡礁还是一处得天独厚的科学研究场所，因为这里栖息着多种濒临灭绝的动物，比如儒艮（“美人鱼”）和巨星绿龟。

La Gran Barrera

A lo largo de la costa noroccidental de Australia se halla el conjunto de arrecifes coralíferos más extenso del mundo. Con sus 400 tipos de coral, sus 1.500 especies de peces y sus 4.000 variedades moluscos, la Gran Barrera ofrece un espectáculo de variedad y belleza extraordinarias, así como un gran interés científico. Además, este sitio es el hábitat de algunas especies en peligro de extinción como el dugongo y la gran tortuga verde.

グレート・バリア・リーフ

source: NFUAJ

Groot Barrièrerif

Het Groot barrièrerif is een plek van opmerkelijke verscheiden- en schoonheid. Het rif ligt aan de noordoostkust van Australië en bevat de grootste collectie koraalriffen ter wereld. Zo zijn er 360 soorten harde koralen, 1.500 soorten vis en 5.000 soorten weekdieren te vinden. Daarnaast is het gebied de thuisbasis van meer dan 175 soorten vogels en biedt het een grote diversiteit aan sponsdieren, anemonen, zeewormen en schaaldieren. Het Groot barrièrerif is ook van groot wetenschappelijk belang als habitat van diersoorten als de dugong ('zeekoe') en de grote groene schildpad, die met uitsterven worden bedreigd.

Source: unesco.nl

Outstanding Universal Value

Brief synthesis

As the world’s most extensive coral reef ecosystem, the Great Barrier Reef is a globally outstanding and significant entity. Practically the entire ecosystem was inscribed as World Heritage in 1981, covering an area of 348,000 square kilometres and extending across a contiguous latitudinal range of 14 o (10 o S to 24 o S). The Great Barrier Reef (hereafter referred to as GBR) includes extensive cross-shelf diversity, stretching from the low water mark along the mainland coast up to 250 kilometres offshore. This wide depth range includes vast shallow inshore areas, mid-shelf and outer reefs, and beyond the continental shelf to oceanic waters over 2,000 metres deep.

Within the GBR there are some 2,500 individual reefs of varying sizes and shapes, and over 900 islands, ranging from small sandy cays and larger vegetated cays, to large rugged continental islands rising, in one instance, over 1,100 metres above sea level. Collectively these landscapes and seascapes provide some of the most spectacular maritime scenery in the world.

The latitudinal and cross-shelf diversity, combined with diversity through the depths of the water column, encompasses a globally unique array of ecological communities, habitats and species. This diversity of species and habitats, and their interconnectivity, make the GBR one of the richest and most complex natural ecosystems on earth. There are over 1,500 species of fish, about 400 species of coral, 4,000 species of mollusk, and some 240 species of birds, plus a great diversity of sponges, anemones, marine worms, crustaceans, and other species. No other World Heritage property contains such biodiversity. This diversity, especially the endemic species, means the GBR is of enormous scientific and intrinsic importance, and it also contains a significant number of threatened species. Attime of inscription, the IUCN evaluation stated "… if only one coral reef site in the world were to be chosen for the World Heritage List, the Great Barrier Reef is the site to be chosen".

Criterion (vii): The GBR is of superlative natural beauty above and below the water, and provides some of the most spectacular scenery on earth. It is one of a few living structures visible from space, appearing as a complex string of reefal structures along Australia's northeast coast.

From the air, the vast mosaic patterns of reefs, islands and coral cays produce an unparalleled aerial panorama of seascapes comprising diverse shapes and sizes. The Whitsunday Islands provide a magnificent vista of green vegetated islands and spectacular sandy beaches spread over azure waters. This contrasts with the vast mangrove forests in Hinchinbrook Channel, and the rugged vegetated mountains and lush rainforest gullies that are periodically cloud-covered on Hinchinbrook Island.

On many of the cays there are spectacular and globally important breeding colonies of seabirds and marine turtles, and Raine Island is the world’s largest green turtle breeding area. On some continental islands, large aggregations of over-wintering butterflies periodically occur.

Beneath the ocean surface, there is an abundance and diversity of shapes, sizes and colours; for example, spectacular coral assemblages of hard and soft corals, and thousands of species of reef fish provide a myriad of brilliant colours, shapes and sizes. The internationally renowned Cod Hole near Lizard Island is one of many significant tourist attractions. Other superlative natural phenomena include the annual coral spawning, migrating whales, nesting turtles, and significant spawning aggregations of many fish species.

Criterion (viii): The GBR, extending 2,000 kilometres along Queensland's coast, is a globally outstanding example of an ecosystem that has evolved over millennia. The area has been exposed and flooded by at least four glacial and interglacial cycles, and over the past 15,000 years reefs have grown on the continental shelf.

During glacial periods, sea levels dropped, exposing the reefs as flat-topped hills of eroded limestone. Large rivers meandered between these hills and the coastline extended further east. During interglacial periods, rising sea levels caused the formation of continental islands, coral cays and new phases of coral growth. This environmental history can be seen in cores of old massive corals.

Today the GBR forms the world’s largest coral reef ecosystem, ranging from inshore fringing reefs to mid-shelf reefs, and exposed outer reefs, including examples of all stages of reef development. The processes of geological and geomorphological evolution are well represented, linking continental islands, coral cays and reefs. The varied seascapes and landscapes that occur today have been moulded by changing climates and sea levels, and the erosive power of wind and water, over long time periods. 

One-third of the GBR lies beyond the seaward edge of the shallower reefs; this area comprises continental slope and deep oceanic waters and abyssal plains.

Criterion (ix): The globally significant diversity of reef and island morphologies reflects ongoing geomorphic, oceanographic and environmental processes. The complex cross-shelf, longshore and vertical connectivity is influenced by dynamic oceanic currents and ongoing ecological processes such as upwellings, larval dispersal and migration. 

Ongoing erosion and accretion of coral reefs, sand banks and coral cays combine with similar processes along the coast and around continental islands. Extensive beds of Halimeda algae represent active calcification and accretion over thousands of years.

Biologically the unique diversity of the GBR reflects the maturity of an ecosystem that has evolved over millennia; evidence exists for the evolution of hard corals and other fauna. Globally significant marine faunal groups include over 4,000 species of molluscs, over 1,500 species of fish, plus a great diversity of sponges, anemones, marine worms, crustaceans, and many others. The establishment of vegetation on the cays and continental islands exemplifies the important role of birds, such as the Pied Imperial Pigeon, in processes such as seed dispersal and plant colonisation. 

Human interaction with the natural environment is illustrated by strong ongoing links between Aboriginal and Torres Strait Islanders and their sea-country, and includes numerous shell deposits (middens) and fish traps, plus the application of story places and marine totems.

Criterion (x): The enormous size and diversity of the GBR means it is one of the richest and most complex natural ecosystems on earth, and one of the most significant for biodiversity conservation. The amazing diversity supports tens of thousands of marine and terrestrial species, many of which are of global conservation significance.

As the world's most complex expanse of coral reefs, the reefs contain some 400 species of corals in 60 genera. There are also large ecologically important inter-reefal areas. The shallower marine areas support half the world's diversity of mangroves and many seagrass species. The waters also provide major feeding grounds for one of the world's largest populations of the threatened dugong. At least 30 species of whales and dolphins occur here, and it is a significant area for humpback whale calving. 

Six of the world’s seven species of marine turtle occur in the GBR. As well as the world’s largest green turtle breeding site at Raine Island, the GBR also includes many regionally important marine turtle rookeries.

Some 242 species of birds have been recorded in the GBR. Twenty-two seabird species breed on cays and some continental islands, and some of these breeding sites are globally significant; other seabird species also utilize the area. The continental islands support thousands of plant species, while the coral cays also have their own distinct flora and fauna.

The ecological integrity of the GBR is enhanced by the unparalleled size and current good state of conservation across the property. At the time of inscription it was felt that to include virtually the entire Great Barrier Reef within the property was the only way to ensure the integrity of the coral reef ecosystems in all their diversity.

A number of natural pressures occur, including cyclones, crown-of-thorns starfish outbreaks, and sudden large influxes of freshwater from extreme weather events. As well there is a range of human uses such as tourism, shipping and coastal developments including ports. There are also some disturbances facing the GBR that are legacies of past actions prior to the inscription of the property on the World Heritage list.

At the scale of the GBR ecosystem, most habitats or species groups have the capacity to recover from disturbance or withstand ongoing pressures. The property is largely intact and includes the fullest possible representation of marine ecological, physical and chemical processes from the coast to the deep abyssal waters enabling the key interdependent elements to exist in their natural relationships.

Some of the key ecological, physical and chemical processes that are essential for the long-term conservation of the marine and island ecosystems and their associated biodiversity occur outside the boundaries of the property and thus effective conservation programs are essential across the adjoining catchments, marine and coastal zones.

Protection and management requirements

The GBR covers approximately 348,000 square kilometres.  Most of the property lies within the GBR Marine Park: at 344,400 square kilometres, this Federal Marine Park comprises approximately 99% of the property. The GBR Marine Park's legal jurisdiction ends at low water mark along the mainland (with the exception of port areas) and around islands (with the exception of 70 Commonwealth managed islands which are part of the Marine Park).  In addition the GBR also includes over 900 islands within the jurisdiction of Queensland, about half of which are declared as 'national parks', and the internal waters of Queensland that occur within the World Heritage boundary (including a number of long-established port areas).

The World Heritage property is and has always been managed as a multiple-use area.  Uses include a range of commercial and recreational activities. The management of such a large and iconic world heritage property is made more complex due to the overlapping State and Federal jurisdictions. The Great Barrier Reef Marine Park Authority, an independent Australian Government agency, is responsible for protection and management of the GBR Marine Park.  The Great Barrier Reef Marine Park Act 1975 was amended in 2007 and 2008, and now provides for “the long term protection and conservation ... of the Great Barrier Reef Region” with specific mention of meeting "... Australia's responsibilities under the World Heritage Convention".

Queensland is responsible for management of the Great Barrier Reef Coast Marine Park, established under the Marine Parks Act 2004 (Qld). This is contiguous with the GBR Marine Park and covers the area between low and high water marks and many of the waters within the jurisdictional limits of Queensland. Queensland is also responsible for management of most of the islands.

The overlapping jurisdictional arrangements mean that the importance of complementary legislation and complementary management of islands and the surrounding waters is well recognised by both governments. Strong cooperative partnerships and formal agreements exist between the Australian Government and the Queensland Government. In addition, strong relationships have been built between governments and commercial and recreational industries, research institutions and universities. Collectively this provides a comprehensive management influence over a much wider context than just the marine areas and islands.

Development and land use activities in coastal and water catchments adjacent to the property also have a fundamental and critical influence on the values within the property.  The Queensland Government is responsible for natural resource management and land use planning for the islands, coast and hinterland adjacent to the GBR. Other Queensland and Federal legislation also protects the property’s Outstanding Universal Value addressing such matters as water quality, shipping management, sea dumping, fisheries management and environmental protection.

The Federal Environment Protection and Biodiversity Conservation Act 1999 (EPBC Act) provides an overarching mechanism for protecting the World Heritage values from inappropriate development, including actions taken inside or outside which could impact on its heritage values. This requires any development proposals to undergo rigorous environmental impact assessment processes, often including public consultation, after which the Federal Minister may decide, to approve, reject or approve under conditions designed to mitigate any significant impacts. A recent amendment to the EPBC Act makes the GBR Marine Park an additional 'trigger' for a matter of National Environmental Significance which provides additional protection for the values within the GBR. 

The GBR Marine Park and the adjoining GBR Coast Marine Park are zoned to allow for a wide range of reasonable uses while ensuring overall protection, with conservation being the primary aim. The zoning spectrum provides for increasing levels of protection for the 'core conservation areas' which comprise the 115,000 square kilometres of ‘no-take’ and ‘no-entry’ zones within the GBR.

While the Zoning Plan is the 'cornerstone' of management and provides a spatial basis for determining where many activities can occur, zoning is only one of many spatial management tools and policies applied to collectively protect the GBR. Some activities are better managed using other spatial and temporal management tools like Plans of Management, Special Management Areas, Agreements with Traditional Owners and permits (often tied to specific zones or smaller areas within zones, but providing a detailed level of management not possible by zoning alone). These statutory instruments also protect the Outstanding Universal Value of the property. 

Many Aboriginal and Torres Strait Island peoples undertake traditional use of marine resource activities to provide traditional food, practice their living maritime culture, and to educate younger generations about traditional and cultural rules and protocols.  In the GBR these activities are managed under both Federal and Queensland legislation and policies including Traditional Use of Marine Resource Agreements (TUMRAs) and Indigenous Land Use Agreements (ILUAs).  These currently cover some 30 per cent of the GBR inshore area, and support Traditional Owners to maintain cultural connections with their sea country.

Similarly non-statutory tools like site management and Industry Codes of Practice contribute to the protection of World Heritage values. Some spatial management tools are not permanently in place nor appear as part of the zoning, yet achieve effective protection for elements of biodiversity (e.g. the temporal closures that are legislated across the GBR prohibit all reef fishing during specific moon phases when reef fish are spawning).

Other key initiatives providing increased protection for the GBR include thecomprehensive Great Barrier Reef Outlook Report (and its resulting 5-yearly reporting process); the Reef Water Quality Protection Plan; the GBR Climate Change Action Plan; and the Reef Guardians Stewardship Programs which involve building relationships and working closely with those who use and rely on the GBR or its catchment for their recreation or their business. 

The 2009 Outlook Report identified the long-term challenges facing the GBR; these are dominated by climate change over the next few decades. The extent and persistence of damage to the GBR ecosystem will depend to a large degree on the amount of change in the world’s climate and on the resilience of the GBR ecosystem to such change. This report also identified continued declining water quality from land-based sources, loss of coastal habitats from coastal development, and some impacts from fishing, illegal fishing and poaching as the other priority issues requiring management attention for the long-term protection of the GBR.

Emerging issues since the 2009 Outlook Report include proposed port expansions, increases in shipping activity, coastal development and intensification and changes in land use within the GBR catchment; population growth; the impacts from marine debris; illegal activities; and extreme weather events including floods and cyclones.

Further building the resilience of the GBR by improving water quality, reducing the loss of coastal habitats and increasing knowledge about fishing and its effects and encouraging modified practices, will give the GBR its best chance of adapting to and recovering from the threats ahead, including the impacts of a changing climate.

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• Published: 16 March 2017

Global warming and recurrent mass bleaching of corals

• Terry P. Hughes 1 ,
• James T. Kerry 1 ,
• Mariana Álvarez-Noriega 1 , 2 ,
• Jorge G. Álvarez-Romero 1 ,
• Kristen D. Anderson 1 ,
• Andrew H. Baird 1 ,
• Russell C. Babcock 3 ,
• Maria Beger 4 ,
• David R. Bellwood 1 , 2 ,
• Ray Berkelmans 2 ,
• Tom C. Bridge 1 , 5 ,
• Ian R. Butler 6 ,
• Maria Byrne 7 ,
• Neal E. Cantin 8 ,
• Steeve Comeau 9 ,
• Sean R. Connolly 1 , 2 ,
• Graeme S. Cumming 1 ,
• Steven J. Dalton 10 ,
• Guillermo Diaz-Pulido 11 ,
• C. Mark Eakin 12 ,
• Will F. Figueira 13 ,
• James P. Gilmour 14 ,
• Hugo B. Harrison 1 ,
• Scott F. Heron 12 , 15 , 16 ,
• Andrew S. Hoey 1 ,
• Jean-Paul A. Hobbs 17 ,
• Mia O. Hoogenboom 1 , 2 ,
• Emma V. Kennedy 11 ,
• Chao-yang Kuo 1 ,
• Janice M. Lough 1 , 8 ,
• Ryan J. Lowe 9 ,
• Gang Liu 12 , 15 ,
• Malcolm T. McCulloch 9 ,
• Hamish A. Malcolm 10 ,
• Michael J. McWilliam 1 ,
• John M. Pandolfi 6 ,
• Rachel J. Pears 18 ,
• Morgan S. Pratchett 1 ,
• Verena Schoepf 9 ,
• Tristan Simpson 19 ,
• William J. Skirving 12 , 15 ,
• Brigitte Sommer 6 ,
• Gergely Torda 1 , 8 ,
• David R. Wachenfeld 18 ,
• Bette L. Willis 1 , 2 &
• Shaun K. Wilson 20  

Nature volume  543 ,  pages 373–377 ( 2017 ) Cite this article

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• Climate-change ecology
• Marine biology

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.

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Acknowledgements

The authors acknowledge the 21 institutions that supported this research, in Australia, the UK, and the USA. Twenty-six of the authors are supported by funding from the Australian Research Council’s Centre of Excellence Program. Other funding support includes the Australian Commonwealth Government, the European Union, the USA National Oceanographic & Atmospheric Administration, and USA National Science Foundation. GlobColour data ( http://globcolour.info ) used in this study has been developed, validated, and distributed by ACRI-ST, France. The contents in this manuscript are solely the opinions of the authors and do not constitute a statement of policy, decision or position on behalf of NOAA or the US Government. We thank the many student volunteers who participated in field studies.

Author information

24 Hanwood Court, Gilston, Queensland 4211, Australia

Authors and Affiliations

Australian Research Council Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, 4811, Queensland, Australia

Terry P. Hughes, James T. Kerry, Mariana Álvarez-Noriega, Jorge G. Álvarez-Romero, Kristen D. Anderson, Andrew H. Baird, David R. Bellwood, Tom C. Bridge, Sean R. Connolly, Graeme S. Cumming, Hugo B. Harrison, Andrew S. Hoey, Mia O. Hoogenboom, Chao-yang Kuo, Janice M. Lough, Michael J. McWilliam, Morgan S. Pratchett, Gergely Torda & Bette L. Willis

College of Science and Engineering, James Cook University, Townsville, 4811, Queensland, Australia

Mariana Álvarez-Noriega, David R. Bellwood, Ray Berkelmans, Sean R. Connolly, Mia O. Hoogenboom & Bette L. Willis

Commonwealth Science and Industry Research Organization, GPO Box 2583, Brisbane, 4001, Queensland, Australia

Russell C. Babcock

School of Biology, University of Leeds, Leeds, LS2 9JT, UK

Maria Beger

Queensland Museum, 70-102 Flinders St, Townsville, 4810, Queensland, Australia

Tom C. Bridge

Australian Research Council, Centre of Excellence for Coral Reef Studies, School of Biological Sciences, University of Queensland, Brisbane, 4072, Queensland, Australia

Ian R. Butler, John M. Pandolfi & Brigitte Sommer

School of Medical Sciences, University of Sydney, Sydney, New South Wales, 2006, Australia

Maria Byrne

Australian Institute of Marine Science, PMB 3, Townsville, 4810, Queensland, Australia

Neal E. Cantin, Janice M. Lough & Gergely Torda

Australian Research Council Centre of Excellence in Coral Reef Studies, Oceans Institute and School of Earth and Environment, University of Western Australia, Crawley, Western Australia, 6009, Australia

Steeve Comeau, Ryan J. Lowe, Malcolm T. McCulloch & Verena Schoepf

Department of Primary Industries, Fisheries Research, PO Box 4291, Coffs Harbour, 2450, New South Wales, Australia

Steven J. Dalton & Hamish A. Malcolm

School of Environment, and Australian Rivers Institute, Griffith University, Brisbane, 4111, Queensland, Australia

Guillermo Diaz-Pulido & Emma V. Kennedy

Coral Reef Watch, US National Oceanic and Atmospheric Administration, College Park, Maryland, 20740, USA

C. Mark Eakin, Scott F. Heron, Gang Liu & William J. Skirving

School of Biological Sciences, University of Sydney, Sydney, 2006, New South Wales, Australia

Will F. Figueira

Australian Institute of Marine Science, Indian Oceans Marine Research Centre, University of Western Australia, Crawley, 6009, Western Australia, Australia

James P. Gilmour

Global Science & Technology, Inc., Greenbelt, 20770, Maryland, USA

Scott F. Heron, Gang Liu & William J. Skirving

Marine Geophysical Laboratory, College of Science, Technology and Engineering, James Cook University, Townsville, 4811, Queensland, Australia

Scott F. Heron

Department of Environment and Agriculture, Curtin University, Perth, 6845, Western Australia, Australia

Jean-Paul A. Hobbs

Great Barrier Reef Marine Park Authority, PO Box 1379, Townsville, 4810, Queensland, Australia

Rachel J. Pears & David R. Wachenfeld

Torres Strait Regional Authority, PO Box 261, Thursday Island, 4875, Queensland, Australia

Tristan Simpson

Department of Parks and Wildlife, Kensington, Perth, 6151, Western Australia, Australia

Shaun K. Wilson

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Contributions

The study was conceptualized by T.P.H. who wrote the first draft of the paper. All authors contributed to writing subsequent drafts. J.T.K. coordinated data compilation, analysis and graphics. Aerial bleaching surveys in 2016 of the Great Barrier Reef and Torres Strait were executed by J.T.K., T.P.H. and T.S., and in 1998 and 2002 by R.B. and D.R.W. Underwater bleaching censuses in 2016 were undertaken on the Great Barrier Reef by M.A.-N., A.H.B., D.R.B., M.B., N.E.C., C.Y.K., G.D.-P., A.S.H., M.O.H., E.V.K., M.J.M., R.J.P., M.S.P., G.T. and B.L.W., in the Coral Sea by T.C.B. and H.B.H., in subtropical Queensland and New South Wales by M.B., I.R.B., R.C.B., S.J.D., W.F.F., H.A.M., J.M.P. and B.S., off western Australia by R.C.B., S.C., J.P.G., J.-P.A.H., M.T.M., V.S. and S.K.W. J.G.A.-R., S.R.C., C.M.E., S.F.H., G.L., J.M.L. and W.J.S. undertook the analysis matching satellite data to the bleaching footprints on the Great Barrier Reef.

Corresponding author

Correspondence to Terry P. Hughes .

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Extended data figures and tables

Extended data figure 1 a generalized linear model to explain the severity of coral bleaching..

Curves show the estimated relationships between probability of severe bleaching (>30%) on individual reefs of the Great Barrier Reef in 2016 and three explanatory variables (DHWs, chlorophyll a , and reef zoning, see Extended Data Table 1 ). The DHW-only model is shown in black. For the DHW plus chlorophyll a model, the blue threshold shows the estimated relationship between probability of severe bleaching and DHW for the 25th percentile of chlorophyll a , and the brown threshold shows the same for the 75th percentile of chlorophyll a . For the DHW plus reef zoning model, the red threshold shows the relationship for fished reefs, and the green for unfished reefs. Water-quality metrics and level of reef protection make little, if any, difference.

Extended Data Figure 2 Difference in daily sea surface temperatures between the northern and southern Great Barrier Reef, before and after ex-tropical cyclone Winston.

The disparity between Lizard Island (14.67° S) and Heron Island (23.44° S) increased from 1 °C in late February to 4 °C in early March 2016.

Extended Data Figure 3 A test for the effect of past bleaching experience on the severity of bleaching in 2016.

The relationship between previous bleaching scores (in 1998 or 2002, whichever was higher) and the residuals from the DHW generalized linear model ( Extended Data Table 1 ). Each data point represents an individual reef that was scored repeatedly. There is no negative relationship to support acclimation or adaptation.

Extended Data Figure 4 Flight tracks of aerial surveys of coral bleaching, conducted along and across the Great Barrier Reef and Torres Strait in March and April 2016.

Blue colour represents land, white colour represents open water.

Extended Data Figure 5 Ground-truthing comparisons of aerial and underwater bleaching scores.

Aerial scores are: 0 (<1% of colonies bleached), 1 (1–10%), 2 (10–30%), 3 (30–60%) and 4 (60–100%) on the Great Barrier Reef in 2016 ( Fig. 1a ). Continuous (0–100%) underwater scores are based on in situ observations from 259 sites (104 reefs). Error bars indicate two standard errors both above and below the median underwater score, separately for each aerial category.

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Hughes, T., Kerry, J., Álvarez-Noriega, M. et al. Global warming and recurrent mass bleaching of corals. Nature 543 , 373–377 (2017). https://doi.org/10.1038/nature21707

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Received : 07 October 2016

Accepted : 16 February 2017

Published : 16 March 2017

Issue Date : 16 March 2017

DOI : https://doi.org/10.1038/nature21707

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