Severe marine heatwaves have recently become a common feature of global ocean conditions due to a rapidly changing climate []. These increasingly severe thermal conditions are causing an unprecedented increase in the frequency and severity of mortality events in marine ecosystems, including on coral reefs []. The degradation of coral reefs will result in the collapse of ecosystem services that sustain over half a billion people globally []. Here, we show that marine heatwave events on coral reefs are biologically distinct to how coral bleaching has been understood to date, in that heatwave conditions result in an immediate heat-induced mortality of the coral colony, rapid coral skeletal dissolution, and the loss of the three-dimensional reef structure. During heatwave-induced mortality, the coral skeletons exposed by tissue loss are, within days, encased by a complex biofilm of phototrophic microbes, whose metabolic activity accelerates calcium carbonate dissolution to rates exceeding accretion by healthy corals and far greater than has been documented on reefs under normal seawater conditions. This dissolution reduces the skeletal density and hardness and increases porosity. These results demonstrate that severe-heatwave-induced mortality events should be considered as a distinct biological phenomenon from bleaching events on coral reefs. We also suggest that such heatwave mortality events, and rapid reef decay, will become more frequent as the intensity of marine heatwaves increases and provides further compelling evidence for the need to mitigate climate change and instigate actions to reduce marine heatwaves.

Results and Discussion

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Leggat W. Climate change disables coral bleaching protection on the Great Barrier Reef. 1 Di Lorenzo E.

Mantua N. Multi-year persistence of the 2014/15 North Pacific marine heatwave. Figure 1 Responses of Northern GBR Corals to the Severe Marine Heatwave in 2016 Show full caption (A–D) Time series of microbial colonization and succession following coral mortality over a 7 week period from March 27th (A) through April 5th (B), and April 9th (C) to May 15th (images from Chasing Coral [Netflix] courtesy of Exposure Labs). (E) Worldwide distribution of bleaching level (DHW ≥ 4°C-weeks) and severe heat stress (DHW ≥ 8°C-weeks) during the period January 2014–May 2017, the latter threshold (dark red) indicating locations that have experienced marine heatwave conditions similar to those seen in the northern GBR in 2016. (F) SST (blue) and DHW (red) experienced by northern GBR corals at Lizard Island. (G) Microprobes were used to monitor microbial metabolism changes by measuring oxygen bubbles trapped within the biofilm during the light that rapidly developed on the coral skeleton post mortem. See Figure S1 The benefits that are derived from coral reefs span from coastal protection to subsistence and industrial fisheries, and these benefits are indisputably contingent upon the integrity of the complex three-dimensional reef framework []. In 2016, the Great Barrier Reef (GBR) experienced the most severe marine heatwave that has ever been recorded in the region []. Reefs of the northern GBR were exposed to severe sea surface temperatures (SSTs), in that 31% of GBR reefs experienced in excess of 8°C weeks (also referred to as 8-degree heating weeks [DHWs]) the established threshold for coral mortality []. Associated with this event, we observed a conspicuous weakening and erosion of the coral skeleton in corals exposed to the severe event on the northern GBR ( Figures 1 A–1D). We also found that the severe heat stress event in the northern GBR was exacerbated by the temporal development of the heating event, in that the sea surface temperature changes were characterized as a rapid and direct SST trajectory that has previously shown to result in high coral mortality [] ( Figures 1 F and S1 ). A rapid degradation of the coral three-dimensional structure was observed in situ on the GBR ( Figure 1 D), and this occurred in the absence of any major storm or wave events ( Figure S1 ). The loss of structure was also not consistent with mechanical damage (e.g., the breakage or tipping of colonies) but was apparent as an erosion of surface area and complexity of the coral colonies exposed to the rapid and severe heat stress. Further observations indicated a rapid colonization of exposed calcium carbonate skeleton by a microbial biofilm associated with the rapid coral mortality ( Figures 1 A–1D). Accompanying the formation of this biofilm was an apparent concurrent decay of the corals’ calcium carbonate corallite structure ( Figure 1 D). Interestingly, severe heat stress events, wherein DHW exceeded 8°C weeks, are not only evident in temperature records of the northern GBR from 2016 but in fact occurred on 37% of reef locations worldwide during the 2014–2017 widespread global coral-bleaching event ( Figure 1 E) [], suggesting that these types of bleaching events are in fact a global phenomenon.

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Data S1. Daily Records of P. damicornis Coral Fragments within Experimental Simulation of Extreme Heatwave Conditions and Control Ambient Conditions, Related to Figures 2 and 3

Data S2. Daily Records of A. aspera Coral Fragments within the Experimental Simulation of Extreme Heatwave Conditions and Control Ambient Conditions, Related to Figures 2 and 3

2+/cm−2/h−1 (mean ± SE), respectively (utilizing quantification of CaCO 3 accretion-dissolution through changes of free Ca2+ in surrounding seawater measured by microwave plasma-atomic emission spectrometry under ambient light intensity). Interestingly, CaCO 3 accretion-dissolution in darkness demonstrated the same trend as in the light, independent of species (2+.cm−2.h−1 ( 2 with elevated temperatures; Figure 3 Skeletal Changes in Pocillopora damicornis and Acropora aspera Show full caption (A–D) Light and dark calcification rates for P. damicornis (A) and A. aspera (B) for healthy (black), algal overgrown (red), and algal overgrown with exterior biofilm removed (red hatched) corals 5 weeks after bleaching. Skeletal density and porosity of P. damicornis (C) and A. aspera (D), values represent average ± SE; n = 4; black, control; red, treatment. Bars cluster p > 0.05. (E–L) Representative SEM images of P. damicornis (E–H) and A. aspera (I–L) corallites for healthy (E, F, I, and J) and biofilm-encased (G, H, K, and L) corals at the end of the simulation period. Scale bars for (E)–(I) and (K) represent 500 μm, for (J) represent 100 μm, and for (L) represent 50 μm. See also Figures S2–S4 Data S1 and S2 , and Video S1 Concerningly, we further show that P. damicornis and A. aspera skeletons encased by this microbial biofilm decalcified at rates of 1.9 ± 0.6 and 2.2 ± 0.7 μmol Ca/cm/h(mean ± SE), respectively (utilizing quantification of CaCOaccretion-dissolution through changes of free Cain surrounding seawater measured by microwave plasma-atomic emission spectrometry under ambient light intensity). Interestingly, CaCOaccretion-dissolution in darkness demonstrated the same trend as in the light, independent of species ( Figures 3 A and 3B ). Importantly, the removal of the external biofilm did not significantly alter the decalcification rates, indicating internal microbial populations were contributing to the majority of decalcification (P. damicornis, p = 0.177; A. aspera, p = 0.668; Figures 3 A and 3B). Corals of both species held within the replicate ambient (control) conditions remained healthy throughout the simulation period and exhibited significant growth within the experimental systems (post hoc sequential Bonferroni; p < 0.001), calcifying at respective rates of 1.7 ± 0.2 and 1.7 ± 0.3 μmol Ca.cm.h Figures 3 A and 3B). When converted to monthly rates, the dissolution values recorded here were more than 10 times found in a normal reef environment and more than 5 times higher than coral skeletal dissolution rates seen in extreme conditions (1,010 μatm pCOwith elevated temperatures; Table S1 ). The effect of this rapid dissolution can be seen in the field images from the 2016 bleaching event at Lizard Island ( Figure 1 ) and further highlight the unique biological phenomena, caused by severe temperature and light conditions of marine heatwave events, on coral reefs, which we investigate in the current study ( Figures 1 A–1D).

20 Varslot T.

Kingston A.

Myers G.

Sheppard A. High-resolution helical cone-beam micro-CT with theoretically-exact reconstruction from experimental data. 2 environment [ 21 Enochs I.C.

Manzello D.P.

Kolodziej G.

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Fabricius K.E. Enhanced macroboring and depressed calcification drive net dissolution at high-CO2 coral reefs. 2 : mol O 2 ), driven by increased respiration over photosynthesis rates, inside the biofilm (P. damicornis = 1.35 ± 0.16; A. aspera = 0.56 ± 0.09) compared with healthy corals (P. damicornis = 1.76 ± 0.25; A. aspera = 1.02 ± 0.13). Increased respiration rates, and the associated increased CO 2 release, further accelerate chemical dissolution of the skeletal substrate, as reported in the current study. Although the exact mechanism by which microbial biofilm enhances dissolution could not be pinpointed, these responses are entirely consistent with metabolic acceleration of coral skeleton dissolution by Ostreobium spp. and cyanobacterial communities, as well as with heterotrophic bacterial breakdown of dissolved organic carbon from dead coral tissue [ 17 Reyes-Nivia C.

Diaz-Pulido G.

Kline D.

Guldberg O.H.

Dove S. Ocean acidification and warming scenarios increase microbioerosion of coral skeletons. 22 Ramírez-Reinat E.L.

Garcia-Pichel F. Characterization of a marine cyanobacterium that bores into carbonates and the redescription of the genus mastigocoleus(1). 23 Garcia-Pichel F.

Ramírez-Reinat E.

Gao Q. Microbial excavation of solid carbonates powered by P-type ATPase-mediated transcellular Ca2+ transport. 24 Kline D.I.

Kuntz N.M.

Breitbart M.

Knowlton N.

Rohwer F. Role of elevated organic carbon levels and microbial activity in coral mortality. Interestingly when exposed to heatwave conditions, microbial dissolution significantly altered the physical properties of the corals’ calcium carbonate skeleton. Computer tomography (CT) scans [] showed significant increases in total porosity (130%; p = 0.038) and micro-porosity (860%; p = 0.006) of biofilm-encased P. damicornis ( Figure 3 C) and total (53%; p = 0.027) and macro-porosity (107%; p = 0.046) in A. aspera ( Figure 3 D) over the 5-week simulation period. This increase in porosity also resulted in a significant loss (12% ± 1%; p = 0.022) of skeleton strength (hardness) for P. damicornis ( Figure 3 C). Consistent with increased porosity, skeletons of both P. damicornis and A. aspera also exhibited alterations to the ultrastructure and a loss of the characteristic calcium carbonate skeleton structure within 2 weeks of biofilm development ( Figures 3 E–3L and S4 ). Corals exhibited a widening of corallites and thinning of septa ( Figures 3 G, 3H, 3K, and 3L) when compared to healthy corals ( Figures 3 E, 3F, 3I, 3J, and S4 ). Similar microscale characteristic alterations have been reported as a result of decalcification in corals exposed to a high COenvironment []. Finally, we also find that oxygen bubbles trapped within the microbial biofilm immediately following coral mortality further signified a localized internal enhancement of microbial metabolism ( Figure 1 G). Microprobes confirmed a lower photosynthesis-to-respiration ratio (P:R) (mol O: mol O), driven by increased respiration over photosynthesis rates, inside the biofilm (P. damicornis = 1.35 ± 0.16; A. aspera = 0.56 ± 0.09) compared with healthy corals (P. damicornis = 1.76 ± 0.25; A. aspera = 1.02 ± 0.13). Increased respiration rates, and the associated increased COrelease, further accelerate chemical dissolution of the skeletal substrate, as reported in the current study. Although the exact mechanism by which microbial biofilm enhances dissolution could not be pinpointed, these responses are entirely consistent with metabolic acceleration of coral skeleton dissolution by Ostreobium spp. and cyanobacterial communities, as well as with heterotrophic bacterial breakdown of dissolved organic carbon from dead coral tissue [].

25 McDonald J.

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Bay R.A. Mechanisms of reef coral resistance to future climate change. Figure 4 Schematic Representation of the Succession of Coral Dissolution following Marine Heatwaves Show full caption Coral fragments transition from healthy (left) to becoming encased by microbial biofilm (right) under severe heat stress, resulting in coral mortality, microbial colonization, and skeletal decay. In conclusion, we propose that the rapid transition to microbial biofilm formation and skeletal decay that is associated with marine-heatwave-induced coral mortality, as reported here, is likely to become more common on coral reefs under future climate change ( Figure 4 ). We suggest that further research into the frequency and severity of heatwave conditions on coral reefs is urgently needed; in particular, it is imperative to determine what conditions on reefs, such as mixing, water flow, and SST trajectory, have the potential to mitigate the speed of heat-induced mortality events. Information such as this may be critical in determining the effectivity of any local-scale interventions aiming to minimize coral mortality and retain reef-wide ecosystem function []. This research also highlights the need to re-think our understanding of coral bleaching and the immediate impact of climate change on coral reefs. Coral bleaching has been widely described, and modeled, as a process of symbiosis breakdown from which corals have the capacity to recover, via a re-uptake of endosymbionts, if elevated temperatures abate. Under these conditions, corals surviving the thermal stress event and subsequent bleaching process have the potential to acclimatize and adapt to thermal stress and predicted future SST increases []. However, here, we show that marine heatwave events on coral reefs are biologically distinct to how coral bleaching has been understood to date, in that heatwave conditions result in an immediate heat-induced mortality of the coral colony, rapid coral skeletal dissolution, and the loss of the three-dimensional reef structure.

9 Ainsworth T.D.

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Maynard J.A.

Planes S. Temporary refugia for coral reefs in a warming world. 17 Reyes-Nivia C.

Diaz-Pulido G.

Kline D.

Guldberg O.H.

Dove S. Ocean acidification and warming scenarios increase microbioerosion of coral skeletons. 17 Reyes-Nivia C.

Diaz-Pulido G.

Kline D.

Guldberg O.H.

Dove S. Ocean acidification and warming scenarios increase microbioerosion of coral skeletons. 28 Tribollet A.

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Atkinson M.

Langdon C. Effects of elevated pCO 2 on dissolution of coral carbonates by microbial euendoliths. 29 Couch C.S.

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Kosaki R.K. Mass coral bleaching due to unprecedented marine heatwave in Papahānaumokuākea Marine National Monument (Northwestern Hawaiian Islands). 30 Frieler K.

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Hoegh-Guldberg O. Limiting global warming to 2°C is unlikely to save most coral reefs. 29 Couch C.S.

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Kosaki R.K. Mass coral bleaching due to unprecedented marine heatwave in Papahānaumokuākea Marine National Monument (Northwestern Hawaiian Islands). 31 Alvarez-Filip L.

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Watkinson A.R. Flattening of Caribbean coral reefs: region-wide declines in architectural complexity. 32 Eakin C.M. Where have all the carbonates gone? A model comparison of calcium carbonate budgets before and after the 1982–1983 El Nino at Uva Island in the eastern Pacific. 33 Eakin C.M. A tale of two ENSO events: carbonate budgets and the influence of two warming disturbances and intervening variability, Uva Island, Panama. 34 Logan C.A.

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Donner S.D. Incorporating adaptive responses into future projections of coral bleaching. Our results here, taken in context of underlying sea surface temperature conditions becoming more physiologically damaging within the coming decade [] and climate models projections of severe coral bleaching exceeding 8°C-weeks DHW annually by 2030 [], highlights the potential for bleaching events to have far more severe implications to the entire reef structure in the immediate future. Taken together, these results suggest far greater coral mortality associated with coral-bleaching events in the future. Our results also demonstrate that projected increases in SST have the potential to fuel the growth [] and metabolic rates of microalgae and cyanobacteria during summer heatwaves, further enhancing the rate of microbial-driven coral dissolution []. In fact, the reduction in structural complexity as documented here has already been observed as a result of the recent 2014–2017 global coral-bleaching event, where an approximately 30% reduction in topographic complexity was found in less than 1 year of the severe bleaching on two surveyed reefs []. Our evidence suggests erosion of coral skeletons is likely to occur far quicker than has so far been anticipated for coral reefs worldwide []. Such rapid decay starkly contrasts with previous estimates of erosion to the reef structural framework following bleaching, which is assumed to occur over timescales of months to years []. Reef degradation is therefore likely to be an immediate consequence of severe marine heatwave events on coral reefs, and concerningly, the implications of marine heatwaves on coral reefs globally have not yet been fully realized in predictions of future coral reef function [].