Updated: Nov 18
The Great Barrier Reef is the world’s largest coral reef, supporting an enormously biodiverse community of organisms. It provides a multitude of ecosystem functions and services, both biotic and abiotic, benefitting the species of the marine ecosystem and the human population surrounding it. The effect of climate change on coral reefs has been widely studied, and multiple detrimental stressors identified. The extreme extent of recent coral bleaching events, additional stress posed by ocean acidification and other anthropogenic drivers make it hard to see a bright future for the GBR. Nevertheless, the discovery of restoration techniques such as microfragmentation and 3D reef printing give some hope to the conservation of the GBR and the ecosystem services it provides.
· New modelling technology demonstrates that the level of atmospheric CO2 concentrations are nearing a critical point for the Great Barrier Reefs survival
· The extent of recent coral bleaching on the Great Barrier Reef is considerably more severe than bleaching events of the past
· The synergistic effect of warming oceans and increasing ocean acidity on coral are compounding at an alarmingly high rate
· The recent discovery of microfragmentation gives some hope for restoring thermally tolerant reefs
· 3D printing technology opens new doors to creating structurally complex artificial reefs and maintaining the ecosystem services they provide
So what’s so ‘Great’ about coral reefs?
Tropical coral reefs possess some of the highest biodiversity of all marine habitats on the globe [1, 2]. Despite only covering 0.1% of the ocean floor, they are home to a quarter of all marine species  and provide a multitude of ecosystem services  (Box 1).
The structure of a reef is composed predominantly of calcium carbonate [CaCO3], CaCO3 is deposited in the form of aragonite by major reef-building corals as they grow and expand their skeleton . Other organisms also contribute to the accumulation of calcium carbonate structures, including invertebrates such as foraminifera and molluscs, as well as calcareous algae . A minimum marine habitat calcium carbonate concentration of 200mmol/kg is required to enable this calcification and allow shallow coral reefs to survive and grow . The majority of reef-building corals are of the order Scleractinia (hereafter use of the word corals refers to scleractinian corals) . These reef-building corals, and other key reef-building organisms which span more than five invertebrate phyla, are dependent on a symbiotic relationship with dinoflagellate algae called zooxanthellae (Box 2) [3, 5, 6]. This mutualistic endosymbiotic relationship requires a very narrow range of environmental conditions to function [7, 8]. An increase in temperature of as little as 1-2°C can result in the breakdown of the symbiosis and consequently the destruction of coral [7, 8].
The Great Barrier Reef (GBR) is the world’s largest coral reef, covering a distance of around 2300km from north to south . Its latitudinal range is approximately 9.5°S to 23.5°S along the coastline of Eastern Australia [9, 16]. The GBR Marine Park encompasses more than 348,000km2 . It has a higher species diversity than any other world heritage area on the planet, home to over 1600 fish species, 2000 sponge species, 410 hard corals, 6/7 extant marine turtles, 630 echinoderms, 4000 molluscs, 500 species of algae, 30 marine mammals, 24 seabirds and 14 species of sea snake [10, 17]. Whether from direct use or indirect, all of these organisms depend on the coral reef for survival/reproduction.
In 2016, the GBR experienced the worst coral bleaching event in history . More than 91% of its reefs were affected, this resulted in the subsequent death of 30% of coral on the GBR [16, 19]. The current combination of stressors that are driving a global loss in coral reefs are compounding at a rate never before seen on a geological scale . Once lost, the reestablishment of these glorious coral reefs can take thousands, even millions of years . Is there any hope of survival for the GBR? This report aims to synthesise the effects of (1) ocean warming, (2) ocean acidification, (3) increasing tropical cyclone intensity, and (4) multiple stressor synergism on the GBR. It will then consider potential mitigation strategies to reduce the negative effects of these stressors.
There are a vast number of anthropogenic stressors driving the risk of coral reef extinction: destructive fishing, over-fishing, mass over-tourism, decreased water quality (from herbicide and pesticide pollution, eutrophication from agriculture and sewage, sedimentation runoff from deforestation and urban development), invasive species, and climate change [10, 20-26]. Climate change (and the CO2 levels that cause it) results in many additional stressors, climate change is widely recognised as the most prominent threat to coral survival [7, 10, 20, 24, 25, 27]. This is especially true for the GBR, which has higher levels of protection against some of the destructive practices other reefs around the world are subject to [21, 28, 29].
1) Ocean warming
Climate change is driving an increase in global temperatures . In 2017 this increase surpassed 1°C above pre-industrial levels . Predictions estimate that if emissions are not reduced warming will likely reach 1.5°C at some point between 2030 and 2052 . Though the rate of ocean warming is slower than land, a large proportion of the global surface temperature increase is absorbed into the world’s oceans . As of 2012, there had been an approximate 0.6°C increase in ocean temperatures since 1901  and alarmingly, the rate of ocean warming continues to increase, predictions suggest that there will be a rise in temperature of between 1°C and 4°C by 2100 [33, 34]. Coral reefs are dependent on a symbiotic relationship with dinoflagellate algae, called zooxanthellae . Zooxanthellae are very sensitive to temperature fluctuations outside their narrow tolerance range [7, 35, 36]. In natural symbiosis with coral, zooxanthellae are already near the maximal end of their thermal tolerance range making this projected ocean warming increasingly worrying .
When the sea surface temperature (SST) thermal tolerance limit for coral-zooxanthellae symbiosis is exceeded, a response called ‘coral reef bleaching’ (hereafter referred to as ‘bleaching’) occurs [7, 35, 36]. The temperature of this tolerance limit varies between areas of the GBR and the species of coral present [37, 38]. Some areas of the GBR demonstrate a bleaching tolerance limit of 30.8°C [37, 38]. The zooxanthellae symbiont in Scleractinian corals are of the genus Symbiodinium . These contain photosynthetic pigments in their chloroplasts which give them a golden brown colour . Healthy corals possess millions of Symbiodinium in each square centimetre of tissue, in turn, these give the host coral its golden brown colour [36, 39]. When temperatures exceed the thermal tolerance limit, the Symbiodinium are expelled from their host coral and they lose the colour provided by the symbiont [35, 36]. This loss exposes the corals' white calcium carbonate skeleton (Fig. 1) and results in a white ‘bleaching’ .
Within GBR corals, differing levels of bleaching and subsequent mortality in periods of heat stress are displayed [16, 38, 43, 44]. The inter-species variation in bleaching response is more prominent when temperature stress and bleaching severity is low (Fig. 2) [43, 44]. Low levels of temperature stress that cause mild bleaching events can act as a highly selective pressure on coral reef assemblages by killing off the species with lower thermal tolerance and leaving those that are more thermally ‘hardy’ . If all incidences of bleaching were mild, and appropriate time intervals were present between these incidences, bleaching events could actively drive an increase in the resilience of coral reef assemblages to temperature stress. However, as global temperatures increase, the severity and frequency of bleaching events will also increase  likely leaving no such time for adaption. The rapid projected warming will likely exceed the rate required for recovery and development of selective advantages that would result in reef composition changes and higher warming tolerance .
Heat stress can cause immediate mortality of the host-coral if ocean temperatures greatly exceed the thermal tolerance threshold – meaning heat can kill coral in more ways than one, via bleaching as well as direct assassination . This happened to some areas of the GBR during the mass bleaching event of 2016 . If temperature increase is less severe, but still above the tolerance threshold, corals are potentially subject to a slow death following the loss of their zooxanthellae symbiont . Because the GBR spans such a large latitudinal range, differential responses of bleaching and mortality are demonstrated throughout the whole ecosystem [16, 19]. The most severe effects are evident closer to the Equator [16, 19].
New 5-km resolution SST monitoring technology was used to demonstrate the variation in heat stress along the GBR in the 2016 mass bleaching event (Fig. 3) [16, 19, 47]. The damage among distinct individual reefs within the GBR varied from a 51% reduction in coral cover on the northern GBR to a 30% reduction further south [16, 19]. Mortality response following this bleaching event showed a high correlation with the level of cumulative heat stress individual reefs were subject to . On the most extreme level, the northern reefs that were exposed to extended and intense heating saw millions of corals die within 2-3 weeks. On the least extreme level, southern reefs mostly recovered within 8 months of the event .
Coral possess some adaptive properties that may enhance survival possibilities in a continuously warming ocean [48-51]. Local adaptations may enable some coral to acclimatise to warmer oceans if the rate of warming is slow enough. Conspecific coral residing at different latitudes are subject to substantially different mean monthly maximum (MMM) temperature values [48, 49]. Nevertheless, the corals still demonstrate bleaching thresholds 1-2°C above their local MMM [48, 49]. Some species of coral harbouring multiple symbiont strains can swap their symbiont for one with a higher temperature tolerance after recovery from a bleaching event . However, the symbiont is usually reverted to their default lower temperature strain after several years . Corals around Ofu island, American Samoa can enhance their thermal tolerance limit through acclimatisation, without changing symbiont . This enhanced tolerance is comparable to a level expected from strong natural selection, however, occurring at a considerably faster rate . It is unknown whether this phenomenon is possible in GBR corals, but, if a similar mechanism occurred here it would enhance their survival chances.
Before the 2016 mass bleaching event, corals on the GBR demonstrated resilience to previous bleaching when certain pre-stress conditions were met . Where pre-bleaching temperatures were above average MMM values but below the bleaching threshold values, corals were observed to ‘brace’ themselves for higher temperatures and developed more of a resilience (that lasted 90 days) to subsequent bleaching inducing temperature rises (Fig. 4). This said, increases in sea surface temperatures have led to a reduction in this protective heating and led to an increase in the incidence of temperatures that cause bleaching itself . As a result of this, where previously higher than average MMM temperatures (but lower than bleaching temperatures) braced corals for actual bleaching events, these higher than average MMM temperatures have now become bleaching events in their own right, leading to double the bleaching, double the coral deaths, and this remarkable protective adaptation has become almost obsolete .
Despite the potential adaptive strategies of coral to ocean warming the Intergovernmental Panel on Climate Change (IPCC) categorises warm water corals under ‘very high risk of severe impacts’ from global temperature increases of > 1°C above pre-industrial levels . Frieler et al.  argue that the global warming target of 2°C above pre-industrial levels is insufficient to save coral reefs. They also suggest that to preserve >50% of global coral coverage warming must be limited to 1.2°C . In 2017, temperatures surpassed 1°C above pre-industrial levels, and some projections indicate 1.5°C could be reached as early as 2030 . Therefore, it seems that this target of >50% of coral reefs conservation is a distressingly unrealistic prospect.
2) Ocean acidification (OA)
Atmospheric carbon dioxide (CO2) concentrations have been continuously increasing since they were first recorded in 1958. Recordings (as of 5th December 2019) measured 410.27 ppm , pre-industrial levels are estimated to have been 280 ppm . All emissions scenario projections by the IPCC suggest atmospheric CO2 levels will continue to rise in the near future . If there is not drastic global change, they have the potential to reach 936 ppm by the year 2100 . The ocean is an enormous atmospheric CO2 sink, it has absorbed approximately 30-40% of all anthropogenic CO2 emissions since the industrial revolution [33, 55-57].
Hydration and hydrolysis of CO2 that is absorbed into the ocean forms carbonic acid [H2CO3] . This results in a higher concentration of oceanic hydrogen ions [H+], thus reducing ocean pH levels [7, 58-60]. Bicarbonate ions [HCO3-] and protons are formed as carbonic acid dissociates , the protons then react with carbonate ions [CO32-] to form more bicarbonate ions [7, 58-60]. This reaction decreases the concentration of oceanic carbonate ions which are essential for coral growth [7, 58-60]. Carbonate ions have not dropped below 240 mmol kg-1 in oceanic regions housing coral reefs in the past 420,000 years. That is until today, where concentrations are already less than 210 mmol kg-1 in key coral reef habitats . Projections indicate the concentration will continue to decline as atmospheric CO2 increases .
Coral utilise carbonate ions in the ocean to form and deposit the framework of aragonite [CaCO3] crystals that later become their skeleton [7, 61]. Shallow tropical seas are highly saturated with carbonate ions and aragonite, this high saturation level is essential for coral growth [58, 60, 61]. Due to OA, the GBR has already started to display evidence of a decreased rate of calcification and growth [63, 64]. Albright et al.  manipulated the ocean chemistry in two isolated coralline lagoons on the GBR. To represent more alkaline pre-industrial conditions, the carbonate ion and aragonite saturation levels in the lagoons were artificially increased. Following manipulation, calcification rates increased by approximately 6% . This indicates that OA is already negatively impacting GBR corals. At the time of this research's publishing (March 2016), CO2 concentrations were at 404.87 ppm .
The oceanic temperature and acidification response to increasing atmospheric CO2 concentrations is subject to a lag-time before the full effect is evident . The lag-time is estimated to be in the range of several decades, the lowest estimations suggest a single decade . Given this lag time, studies regarding the effects of OA on coral growth may in actuality represent the effects of atmospheric CO2 concentration at least 10 years prior. It has previously been reported by Veron et al.  that atmospheric CO2 of 350 ppm is the maximum concentration at which coral reefs can exist in a healthy state. Considering the minimum ten-year lag time, therefore we may be beyond the point of no return concerning ensuring the survival of a healthy GBR.
It has been suggested that the lethal dissolution effects of OA on coral reefs will not be witnessed under natural conditions . In some species, extreme OA has been shown to cause bleaching and subsequent mortality before disrupting calcification enough to trigger the reef to enter dissolution . Unfortunately, this is in part because the atmospheric CO2 concentrations required to generate a state of dissolution may have already driven global temperatures beyond the level coral can survive . Atmospheric CO2 concentrations of 560 ppm have been proposed as the level at which the coral reefs will enter a state of dissolution . Fig. 5 demonstrates that an atmospheric CO2 concentration of 450 ppm has a 34% chance of driving a global temperature increase of ~1.5°C . Warming surpassing 1.5°C could result in the death of 90% or more of the worlds coral reefs irrespective of dissolution .
In terms of potential adaptive responses of coral to OA, the topic is largely unknown . This is in part due to experimental difficulties in isolating the effects of OA from temperature stress . OA is a significant stressor on coral reef ecosystems  and given the GBR’s southerly range, is potentially an even more prominent stressor than on other coral reef ecosystems [7, 58, 64, 66].
3) Increasing intensity of tropical cyclones
A number of studies have predicted that the overall frequency of tropical cyclones will not increase in conjunction with climate change, and may even decrease [33, 68, 69]. This said it is thought that the average intensity of cyclone events is set to increase in response to climate warming [33, 69-72]. Intense tropical cyclones are a prominent cause of coral cover decline on the GBR. De’ath et al.  estimated that 48% of the total coral lost on the GBR between 1985 and 2012 was due to cyclone damage. The ecological costs of severe cyclone damage on a reef is high [73, 74]. Following a bleaching event, until the intact dead coral skeleton degrades there is still potential for it to be utilised for shelter by reef fauna . Cyclones, however, have the potential to destroy and remove coral structures altogether, rendering entire areas uninhabitable .
The recovery time for an area of the GBR affected by an intense cyclone (category 5) has been estimated at approximately 15 years, however, some higher estimates have been as high as >36 years . Projections indicate the frequency of Category 5 cyclones on the GBR will increase from current figures of approximately one every 15 years (excluding the anomalous clustered events between 2009-2014), to one every 6-13 years before 2100 . Intense cyclone events of this frequency would not allow adequate time for the coral in the area to recover before being degraded again .
4) Synergistic effect of multiple stressors
As previously mentioned, the GBR faces a multitude of anthropogenic stressors [10, 20-26, 73]. The negative effects of these stressors do not work in isolation but compound together synergistically, exacerbating each factor [22, 27, 75].
The crown of thorns starfish (COTS; Acanthaster spp.) is a natural predator of hard coral and is not detrimental to reef health when they are present in low abundance . A COTS outbreak is defined to be where the rate of hard coral consumption by them surpasses the rate of coral growth . Previous COTS outbreaks on the GBR have had disastrous consequences, causing considerable reductions in coral cover [42, 73, 79, 80]. It has recently been found that COTS have increased growth and feeding rates in both warmer and more acidic oceans . Therefore, as climate change exacerbates bleaching events and OA, the threat of, and damage from COTS outbreaks will also likely increase .
Although coral can recover from a bleaching event, species may experience long-term sublethal effects, including reduced reproductivity and greater susceptibility to other stressors . Previously bleached corals show greater vulnerability to disease, reduced tissue regeneration efficiency following lesions and a reduced growth rate . When combined with the reduced growth rate caused by OA, this potentially further increases the severity of the problem [38, 63]. Severe cases of bleaching can trigger the reef to enter an erosion state . With projections for future OA already threatening to force reefs into dissolution [58, 65], this only furthers the problem.
Coral reefs under extreme stress have the potential to undergo a phase shift away from a coral dominated ecosystem to a macroalgae dominated ecosystem [24, 27, 82, 83]. The risk of this phase shift occurring increases as the resilience of a reef decreases, and as its structural complexity is compromised [27, 82-84]. It is now widely recognised that the resilience of reef ecosystems are being reduced by anthropogenic activity, primarily the synergism of climate change, overfishing and nutrient pollution (Fig. 6) [22, 24, 27, 82]. Nutrient pollution causes eutrophication of GBR waters . This encourages macroalgal growth subsequently driving the loss of living coral . Nutrient pollution on the GBR from terrestrial runoff occurs in high volumes after periods of heavy rainfall [86, 87]. This further intensifies the strain on the reef caused by climate change .
Positive feedback loops between multiple stressors mean that the effect of any one stressor exacerbates the effect of all stressors present . This positive feedback contributes hugely towards the likelihood of ecosystem phase shifts occurring . It also means that a considerably lower effect of each stressor is required to harm reef health than if it were acting in isolation [27, 75]. This means ongoing monitoring of the effect of stressors on the health of the GBR must encompass all stressors simultaneously. Because the threshold for detrimental effects are reduced in synergism, monitoring a single stressor in isolation can produce a false positive response .
As highlighted above, the GBR is plagued by a multitude of stressors that work in synergism, making its preservation extremely challenging. Some studies have highlighted the need to shift the focus of coral reef conservation away from preserving or restoring their former glory, towards damage limitation, minimising the loss of ecosystem services they provide and accepting that reductions are inevitable [27, 88]. Those reports that still hold hope for the future of coral reefs emphasise the necessity for immediate global action to curb emissions and warming [16, 22, 43]. The detrimental effects of climate change on coral reefs have been known for over two decades , and a multitude of warning papers have been published continuously since then [7, 20, 25, 53, 59, 82]. Despite this, global emissions have persisted in a business as usual manner . Therefore, unless a rapid global change in emissions occurs, preserving the GBR in its natural glory is unrealistic. This said, and despite climate change being the factor causing most severe coral declines, a handful of other mitigation factors addressing other aspects causing declines might be explored moving forward.
A reef’s resilience to climate change-induced stressors can be increased by reducing the effect of other anthropogenic stressors [25, 27, 82, 83]. Reducing fisheries pressure and implementing Marine Protected Areas (MPAs) is a conservation practice that would benefit many coral reefs around the globe . This said, the GBR Marine Park authority now comprehensively manages the MPA and is already managing fisheries on the reef at a sustainable level [28, 29]. 33% of the GBR is a fisheries ‘no-take’ zone, and all commercial stocks are being fished below their maximum sustainable yield . Therefore, there would be little conservation benefit in further reducing fisheries on the reef. It would result in lower fisheries yields, and consequently, reduce the volume of provisioning services provided by the GBR.
Reducing the nutrient pollution from terrestrial runoff onto the GBR would reduce eutrophication levels and enhance reef resilience to climate change [27, 87, 89]. The potentially beneficial outcome on coral health of effective fisheries management have been largely undone by large floods polluting certain no-take areas of the GBR . A considerably more effective management plan for coastal water quality is required to prevent the already prominent degradation of the GBR that is exacerbated by terrestrial water pollution [87, 89].
Maintaining the structural complexity of a coral reef is of paramount importance in ensuring the potential for recovery and survival following disturbances . Reef structural complexity is also vital to the maintenance of the ecosystem services reefs provides [84, 88]. Where a loss of habitat structure follows coral mortality, regenerative measures can be implemented to restore structural complexity . Regeneration of structural complexity can be done through utilising artificial reefs, or natural regenerative measures [84, 91, 92].
Artificial reefs encompass a multitude of varying structures, from simple objects such as car tires to complexly designed engineered constructs . Traditionally, the GBR has not been such a degraded ecosystem and therefore the use of artificial reefs has been minimal . Though this has been the case in the past, due to the severity of current losses, this strategy may be used less sparingly moving forward . Where reef complexity declines with live coral cover it may be necessary to utilise artificial reefs to ensure the continuation of the ecosystem services provided by the GBR .
The recent development of 3D printing has facilitated the production of artificial reefs with comparable structural complexity to a highly diverse natural system . 3D printed reefs have shown to be highly utilised in habitat selection by reef fish, and do not affect the growth of any live coral nearby . Nanotechnologies could allow the incorporation of slow-release materials into 3D printed reefs . These materials could be utilised to maintain a desirable pH in the micro-environment surrounding the printed reefs . Maintenance of a desirable pH could reverse the impact of OA on coral growth and enable faster coral recovery . On a small spatial scale, 3D printing is cost-effective and could be utilised to ensure the continuation of complex structured reef ecosystems [94, 95]. This said 3D printing complex reefs and incorporating nanotechnologies on the vast spatial scale of the GBR would pose an enormous challenge, both economically and practically. Perhaps targeting key individual reefs for 3D restoration would be a more realistic option. The consideration of the introduction of artificial reefs on the GBR has been met with opposition in the past . An ecosystem-scale cost-benefit analysis must be performed before practical implementation .
Although natural restoration may seem difficult, the “gardening” technique of coral reef restoration has been utilised for over two decades . It begins with a mid-water nursery stage, where large stocks of coral colonies are raised from a coral nubbin . When the colonies have reached a suitable size, they are then transplanted onto degraded reefs . This technique can reshape degraded coral communities into novel reef ecosystems [96-101]. Additionally, many of the transplanted colonies demonstrate fast-growth rates . Unfortunately, selecting coral species suitable for this restoration technique requires fast-growing and readily fragmenting corals, which reduces the species diversity within an assemblage . Many of the coral species which possess these traits are linked to a high thermal stress susceptibility [102-105]. In the face of a continuously warming ocean, this is not a trait beneficial to coral reef survivorship, and therefore a significant drawback of this biological restoration technique.
The recent discovery in Florida of a technique called microfragmenting gives some hope to the natural regeneration of coral reefs in the face of climate change . The coral species’ utilised in this technique have previously been overlooked for use in restoration because of their slow growth rate . Nevertheless, they are more thermally tolerant than their faster-growing counterparts and offer a large contribution to the reef framework [102, 104-106]. The technique involves cutting micro fragments to ≤ 1 cm2 and growing them to ~6 cm2, before outplanting them in a similar manner to the “gardening” technique . Unfortunately, one major drawback to this technique is a high predation rate on the microfragments . If predation rates were reduced, this method may prove more viable moving forward . Nevertheless, this technique is in early stages of testing on Florida reefs and it is unknown if the same potential for success exists on the GBR.
The GBR faces an enormous survival challenge in the Anthropocene, primarily as a result of climate change [16, 27]. Warming oceans are driving unprecedented levels of coral bleaching , and increases in atmospheric CO2 concentrations are driving OA . When combined with the synergistic effect of multiple additional stressors the future looks bleak for the GBR. Natural preservation and restoration offer some hope via the reduction of additional anthropogenic stressors such as nutrient pollution [22, 24, 27, 89], and utilising recently developed reef restoration techniques [96, 106]. Nevertheless, if global CO2 emissions are not addressed in the very near future natural preservation will be a futile effort that only delays the GBR’s inevitable demise.
1. Stehli, F.G. and J.W. Wells, Diversity and Age Patterns in Hermatypic Corals. Systematic zoology., 1971. 20(2): p. 115.
2. Bellwood, D.R. and T.P. Hughes, Regional-scale assembly rules and biodiversity of coral reefs. Science (New York, N.Y.), 2001. 292(5521): p. 1532.
3. Hoegh-Guldberg, O. and S. Dove, Primary production, nutrient recycling, and energy flow through coral reef ecosystems, in The Great Barrier Reef: Biology, Environment and Management, P.A. Hutchings, M. Kingsford, and O. Hoegh-Guldberg, Editors. 2019, CRC Press.
4. Moberg, F. and C. Folke, Ecological goods and services of coral reef ecosystems. Ecological Economics, 1999. 29(2): p. 215-233.
5. Sheppard, C.R.C., et al., The main reef builders and space occupiers, in The Biology of Coral Reefs, C.R.C. Sheppard, et al., Editors. 2017, Oxford : Oxford University Press.
6. Yellowlees, D., T.A.V. Rees, and W. Leggat, Metabolic interactions between algal symbionts and invertebrate hosts. 2008: Oxford, UK. p. 679-694.
7. Hoegh-Guldberg, O., et al., Coral reefs under rapid climate change and ocean acidification. Science, 2007. 318(5857): p. 1737-1742.
8. Sheppard, C.R.C., et al., Symbiotic Interactions, in The Biology of Coral Reefs, C.R.C. Sheppard, et al., Editors. 2017, Oxford : Oxford University Press.
9. Stoeckl, N., et al., The economic value of ecosystem services in the Great Barrier Reef: our state of knowledge. Annals of the New York Academy of Sciences, 2011. 1219(1): p. 113.
10. Johnson, J.E. and P.A. Marshall, Climate Change and the Great Barrier Reef: A Vulnerability Assessment. 2007, Townsville, Australia: Great Barrier Reef Marine Park Authority.
11. Ortiz, D.M. and B.N. Tissot, Evaluating ontogenetic patterns of habitat use by reef fish in relation to the effectiveness of marine protected areas in West Hawaii. Journal of Experimental Marine Biology and Ecology, 2012. 432-433(C): p. 83-93.
12. Fletcher, W.J., et al., Large-scale expansion of no-take closures within the Great Barrier Reef has not enhanced fishery production. Ecological Applications, 2015. 25(5): p. 1187-1196.
13. Ferrario, F., et al., The effectiveness of coral reefs for coastal hazard risk reduction and adaptation. Nature Communications, 2014. 5(1): p. 1-9.
14. Sheppard, C., et al., Coral mortality increases wave energy reaching shores protected by reef flats: Examples from the Seychelles. Estuarine, Coastal and Shelf Science, 2005. 64(2-3): p. 223-234.
15. Campbell, J., et al., Carbon Storage in Seagrass Beds of Abu Dhabi, United Arab Emirates. Journal of the Coastal and Estuarine Research Federation, 2015. 38(1): p. 242-251.
16. Hughes, T.P., et al., Global warming transforms coral reef assemblages. Nature, 2018. 556(7702): p. 492.
17. Richards, Z.T. and J.C. Day, Biodiversity of the Great Barrier Reef—how adequately is it protected? PeerJ, 2018. 6(5): p. e4747.
18. Cressey, D., Coral crisis: Great Barrier Reef bleaching is “the worst we’ve ever seen”. Nature, 2016.
19. Stuart-Smith, R.D., et al., Ecosystem restructuring along the Great Barrier Reef following mass coral bleaching. Nature, 2018. 560(7716): p. 92-+.
20. Veron, J.E.N., et al., The coral reef crisis: The critical importance of<350ppm CO2. Marine Pollution Bulletin, 2009. 58(10): p. 1428-1436.
21. Jackson, J., et al., Status and Trends of Caribbean Coral Reefs: 1970-2012. 2014: Global Coral Reef Monitoring Network, IUCN, Gland, Switzerland.
22. Harborne, A.R., et al., Multiple Stressors and the Functioning of Coral Reefs, in Annu. Rev. Mar. Sci. 2017. p. 445-468.
23. Bellwood, D.R., A.S. Hoey, and T.P. Hughes, Human activity selectively impacts the ecosystem roles of parrotfishes on coral reefs. Proceedings of the Royal Society B, 2012. 279(1733): p. 1621-1629.
24. Graham, N.A., et al., Managing resilience to reverse phase shifts in coral reefs. Frontiers in Ecology and the Environment, 2013. 11(10): p. 541-548.
25. Hughes, T.P., et al., Climate change, human impacts, and the resilience of coral reefs. Science, 2003. 301(5635): p. 929-933.
26. Chan, A. and P.A. Hodgson, A systematic analysis of blast fishing in South-East Asia and possible solutions. 2017. p. 1-6.
27. Hughes, T.P., et al., Coral reefs in the Anthropocene. Nature, 2017. 546(7656): p. 82.
28. Day, J.C., Planning and managing the Great Barrier Reef Marine Park, in The Great Barrier Reef: Biology, Environment and Management, P. Hutchings, M. Kingsford, and O. Hoegh-Guldberg, Editors. 2019, CRC Press.
29. Chin, A., D. Cameron, and R. Saunders, Fisheries of the Great Barrier Reef, in The Great Barrier Reef: Biology, Environment and Management, P. Hutchings, M. Kingsford, and O. Hoegh-Guldberg, Editors. 2019, CRC Press.
30. Von Schuckmann, K., et al., An imperative to monitor Earth's energy imbalance. Nature Climate Change, 2016. 6(2): p. 138.
31. Inter Governmenatal Panel on Climate Change (IPCC), Summary for policymakers. In: Global Warming of 1.5°C. A IPCC Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty. 2018, Geneva: World Meteorological Organization.
32. Cheng, L., et al., 2018 Continues Record Global Ocean Warming. Advances in Atmospheric Sciences, 2019. 36(3): p. 249-252.
33. Inter Governmental Panel on Climate Change (IPCC), Climate Change. Climate Change 2013: the physical science basis. IPCC Working Group I Fifth Assessment Report: Summary for Policymakers. 2013, Cambridge University Press: Cambridge and New York.
34. Cheng, L., et al., How fast are the oceans warming? Science (New York, N.Y.), 2019. 363(6423): p. 128.
35. Lesser, M.P., Oxidative stress in marine environments: biochemistry and physiological ecology. Annual review of physiology, 2006. 68: p. 253.
36. Weis, V.M., Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. The Journal of experimental biology, 2008. 211(Pt 19): p. 3059.
37. Berkelmans, R., et al., A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions. Journal of the International Society for Reef Studies, 2004. 23(1): p. 74-83.
38. Baker, A.C., P.W. Glynn, and B. Riegl, Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook. Estuarine, Coastal and Shelf Science, 2008. 80(4): p. 435-471.
39. Hoegh-Guldberg, O., Climate change, coral bleaching and the future of the worldís coral reefs. Marine and Freshwater Research, 1999. 50.
40. Franklin, D., et al., Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching. Mar. Ecol.-Prog. Ser., 2004. 272: p. 117-130.
41. Bruno, J., et al., Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS. Biol., 2007. 5(6): p. 1220-1227.
42. Wakeford, M., T. Done, and C. Johnson, Decadal trends in a coral community and evidence of changed disturbance regime. Journal of the International Society for Reef Studies, 2008. 27(1): p. 1-13.
43. Hughes, T.P., et al., Global warming and recurrent mass bleaching of corals. Nature, 2017. 543(7645): p. 373.
44. Baird, A. and P.A. Marshall, Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar. Ecol.-Prog. Ser., 2002. 237: p. 133-141.
45. Van Hooidonk, R., et al., Local-scale projections of coral reef futures and implications of the Paris Agreement. Scientific Reports, 2016. 6(6).
46. Liu, G., A. Strong, and W. Skirving, Remote sensing of sea surface temperatures during 2002 Barrier Reef coral bleaching. Eos, Transactions American Geophysical Union, 2003. 84(15): p. 137-141.
47. Gang, L., et al., Reef-Scale Thermal Stress Monitoring of Coral Ecosystems: New 5-km Global Products from NOAA Coral Reef Watch. Remote Sensing, 2014. 6(11): p. 11579-11606.
48. Palumbi, S.R., et al., Mechanisms of Reef Coral Resistance to Future Climate Change. Science, 2014. 344(6186).
49. Pandolfi, J., et al., Projecting Coral Reef Futures Under Global Warming and Ocean Acidification. Science, 2011. 333(6041): p. 418-422.
50. Ainsworth, T.D., et al., Climate change disables coral bleaching protection on the Great Barrier Reef. Science (New York, N.Y.), 2016. 352(6283): p. 338.
51. Logan, C.A., et al., Incorporating adaptive responses into future projections of coral bleaching. Global Change Biology, 2014. 20(1): p. 125-139.
52. Thornhill, D., et al., Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. International Journal on Life in Oceans and Coastal Waters, 2006. 148(4): p. 711-722.
53. Frieler, K., et al., Limiting global warming to 2 °C is unlikely to save most coral reefs. Nature Climate Change, 2012. 3(2): p. 165.
54. NOAA/ESRL. Trends in Atmospheric Carbon Dioxide. 2019 [cited 2019 8th December]; Available from: https://www.esrl.noaa.gov/gmd/ccgg/trends/mlo.html.
55. Khatiwala, S., et al., Global ocean storage of anthropogenic carbon. Biogeosciences, 2013. 10(4): p. 2169-2191.
56. DeVries, T., The oceanic anthropogenic CO 2 sink: Storage, air‐sea fluxes, and transports over the industrial era. Global Biogeochemical Cycles, 2014. 28(7): p. 631-647.
57. DeVries, T., M. Holzer, and F. Primeau, Recent increase in oceanic carbon uptake driven by weaker upper-ocean overturning. Nature, 2017. 542(7640): p. 215.
58. Orr, J., C., et al., Anthropogenic ocean acidification over the twenty- first century and its impact on calcifying organisms. Nature, 2005. 437(7059): p. 681.
59. Feely, R.A., et al., Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science (New York, N.Y.), 2004. 305(5682): p. 362.
60. Feely, R.A., S.C. Doney, and S.R. Cooley, Ocean acidification: Present conditions and future changes in a high-CO 2 world. Oceanography, 2009. 22(4): p. 36-47.
61. Gattuso, J.-P. and L. Hansson, Ocean Acidification. 2011: Oxford University Press.
62. Falini, G., et al., Control of aragonite or calcite polymorphism by mollusk shell macromolecules. Science, 1996. 271(5245): p. 67-69.
63. De'ath, G., J.M. Lough, and K.E. Fabricius, Declining coral calcification on the Great Barrier Reef. Science (New York, N.Y.), 2009. 323(5910): p. 116.
64. Albright, R., et al., Reversal of ocean acidification enhances net coral reef calcification. Nature, 2016. 531(7594): p. 362.
65. Silverman, J., et al., Coral reefs may start dissolving when atmospheric CO 2 doubles. Geophysical Research Letters, 2009. 36(5): p. n/a-n/a.
66. Dove, S.G., et al., Future reef decalcification under a business-as-usual CO2 emission scenario. Proceedings of the National Academy of Sciences, 2013. 110(38): p. 15342.
67. Anthony, K.R.N., et al., Ocean acidification causes bleaching and productivity loss in coral reef builders. Proceedings of the National Academy of Sciences, 2008. 105(45): p. 17442.
68. Walsh, K.J.E., et al., Tropical cyclones and climate change. 2016: Hoboken, USA. p. 65-89.
69. Knutson, T.R., et al., Tropical cyclones and climate change. Nature Geoscience, 2010. 3(3): p. 157-163.
70. Emanuel, K.A., Downscaling CMIP5 climate models shows increased tropical cyclone activity over the 21st century. Proceedings of the National Academy of Sciences, 2013. 110(30): p. 12219.
71. Emanuel, K., R. Sundararajan, and J. Williams, Hurricanes and Global Warming: Results from Downscaling IPCC AR4 Simulations. BAMS, 2008. 89(3).
72. Wolff, N., et al., Temporal clustering of tropical cyclones on the Great Barrier Reef and its ecological importance. Journal of the International Society for Reef Studies, 2016. 35(2): p. 613-623.
73. De’ath, G., et al., The 27–year decline of coral cover on the Great Barrier Reef and its causes. Proceedings of the National Academy of Sciences, 2012. 109(44): p. 17995.
74. Cheal, A.J., et al., The threat to coral reefs from more intense cyclones under climate change. Global Change Biology, 2017. 23(4): p. 1511-1524.
75. Leemput, I., et al., Multiple feedbacks and the prevalence of alternate stable states on coral reefs. Journal of the International Society for Reef Studies, 2016. 35(3): p. 857-865.
76. Madin, J.S., T.P. Hughes, and S.R. Connolly, Calcification, Storm Damage and Population Resilience of Tabular Corals under Climate Change (Erosion of Population Resilience). 2012. 7(10): p. e46637.
77. Madin, J.S., M.O. Hoogenboom, and S.R. Connolly, Integrating physiological and biomechanical drivers of population growth over environmental gradients on coral reefs. The Journal of experimental biology, 2012. 215(6): p. 968.
78. Lourey, M.J., D.A.J. Ryan, and I.R. Miller, Rates of decline and recovery of coral cover on reefs impacted by, recovering from and unaffected by crown-of-thorns starfish Acanthaster planci: A regional perspective of the Great Barrier Reef. Marine Ecology Progress Series, 2000. 196: p. 179-186.
79. Osborne, K., et al., Disturbance and the Dynamics of Coral Cover on the Great Barrier Reef (1995–2009) (Disturbance and Coral Cover on the GBR). PLoS ONE, 2011. 6(3): p. e17516.
80. Morello, E.B., et al., Model to manage and reduce crown-of-thorns starfish outbreaks. Marine Ecology Progress Series, 2014. 512: p. 167-183.
81. Kamya, P., et al., Enhanced performance of juvenile crown of thorns starfish in a warm-high CO 2 ocean exacerbates poor growth and survival of their coral prey. Journal of the International Society for Reef Studies, 2018. 37(3): p. 751-762.
82. Bellwood, D.R., et al., Confronting the coral reef crisis. Nature, 2004. 429(6994): p. 827.
83. Hughes, T.P., et al., Rising to the challenge of sustaining coral reef resilience. Trends in Ecology & Evolution, 2010. 25(11): p. 633-642.
84. Graham, N. and K. Nash, The importance of structural complexity in coral reef ecosystems. Journal of the International Society for Reef Studies, 2012. 32(2): p. 315-326.
85. Brodie, J., et al., Assessment of the eutrophication status of the Great Barrier Reef lagoon (Australia). An International Journal, 2011. 106(2): p. 281-302.
86. Wallace, J., F. Karim, and S. Wilkinson, Assessing the potential underestimation of sediment and nutrient loads to the Great Barrier Reef lagoon during floods. Marine Pollution Bulletin, 2012. 65(4-9): p. 194-202.
87. Brodie, J. and K. Fabricius, Terrestrial runoff to the Great Barrier Reef and the implications for its long term ecological status, in The Great Barrier Reef: Biology, Environment and Management, P. Hutchings, M. Kingsford, and O. Hoegh-Guldberg, Editors. 2019, CRC Press.
88. Rogers, A., et al., Anticipative management for coral reef ecosystem services in the 21st century. Global Change Biology, 2015. 21(2): p. 504-514.
89. Brodie, J. and R.G. Pearson, Ecosystem health of the Great Barrier Reef: Time for effective management action based on evidence. Estuarine, Coastal and Shelf Science, 2016. 183: p. 438-451.
90. Wenger, A.S., et al., Effects of reduced water quality on coral reefs in and out of no‐take marine reserves. Conservation Biology, 2016. 30(1): p. 142-153.
91. Edwards, A.J., Reef Rehabilitation Manual. 2010, St Lucia, Australia: The Coral Reef Targeted Research & Capacity Building for Management Program.
92. Edwards, A.J. and E.D. Gomez, Reef Restoration Concepts and Guidelines: making sensible management choices in the face of uncertainty. 2007, St Lucia, Australia: The Coral Reef Targeted Research & Capacity Building for Management Program.
93. Sutton, S.G. and S.L. Bushnell, Socio-economic aspects of artificial reefs: Considerations for the Great Barrier Reef Marine Park. Ocean and Coastal Management, 2007. 50(10): p. 829-846.
94. Mohammed, J.S., Applications of 3D printing technologies in oceanography. Methods in Oceanography, 2016. 17: p. 97-117.
95. Ruhl, E.J. and D.L. Dixson, 3D printed objects do not impact the behavior of a coral-associated damselfish or survival of a settling stony coral. PloS one, 2019. 14(8): p. e0221157.
96. Rinkevich, B., Climate Change and Active Reef Restoration—Ways of Constructing the “Reefs of Tomorrow”. Journal of Marine Science and Engineering, 2015. 3(1): p. 111-127.
97. Shaish, L., et al., Coral Reef Restoration (Bolinao, Philippines) in the Face of Frequent Natural Catastrophes. Restoration Ecology, 2010. 18(3): p. 285-299.
98. Linden, B. and B. Rinkevich, Creating stocks of young colonies from brooding coral larvae, amenable to active reef restoration. Journal of Experimental Marine Biology and Ecology, 2011. 398(1-2): p. 40-46.
99. Shaish, L., et al., Employing a highly fragmented, weedy coral species in reef restoration. Ecological Engineering, 2010. 36(10): p. 1424-1432.
100. Horoszowski-Fridman, Y.B., I. Izhaki, and B. Rinkevich, Engineering of coral reef larval supply through transplantation of nursery-farmed gravid colonies. Journal of Experimental Marine Biology and Ecology, 2011. 399(2): p. 162-166.
101. Rinkevich, B., Rebuilding coral reefs: does active reef restoration lead to sustainable reefs? Current Opinion in Environmental Sustainability, 2014. 7: p. 28-36.
102. Loya, Y., et al., Coral bleaching: the winners and the losers. Ecology Letters, 2001. 4(2): p. 122-131.
103. van Woesik, R., et al., Revisiting the winners and the losers a decade after coral bleaching. Mar. Ecol.-Prog. Ser., 2011. 434: p. 67-76.
104. McClanahan, T., The relationship between bleaching and mortality of common corals. International Journal on Life in Oceans and Coastal Waters, 2004. 144(6): p. 1239-1245.
105. Lirman, D., et al., Severe 2010 Cold-Water Event Caused Unprecedented Mortality to Corals of the Florida Reef Tract and Reversed Previous Survivorship Patterns (Cold-Water Anomaly Kills Corals in Florida). PLoS ONE, 2011. 6(8): p. e23047.
106. Page, C.A., E.M. Muller, and D.E. Vaughan, Microfragmenting for the successful restoration of slow growing massive corals. Ecological Engineering, 2018. 123: p. 86-94.