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Widespread Coral Bleaching and Mass Mortality of Reef-Building Corals in Southern Mexican Pacific Reefs Due to 2023 El Niño Warming [1]

['López-Pérez', 'Granja-Fernández', 'Ramírez-Chávez', 'Valencia-Méndez', 'Rodríguez-Zaragoza', 'Fabián A.', 'González-Mendoza', 'Martínez-Castro', 'Andrés López-Pérez', 'Rebeca Granja-Fernández']

Date: 1924-05-02

The Climate Prediction Center of the National Oceanic and Atmospheric Administration: https://www.cpc.ncep.noaa.gov/products/CDB/CDB_Archive_html/CDB_archive.shtml (accessed on 20 September 2023) reported that during early 2023, there was a transition from negative to positive anomalies in the Pacific. However, it was not until May that the oceanic and atmospheric anomalies were consistent with El Niño conditions: https://www.cpc.ncep.noaa.gov/products/CDB/CDB_Archive_html/bulletin_052023/ (accessed on 20 September 2023). Since mid–June 2023, multiple reports on social media emerged regarding disturbances in coral communities and reefs in the southern Mexican Pacific and other areas of Central America, indicating mild to severe coral bleaching associated with El Niño conditions. In this study, we document the impact of the current 2023 El Niño bleaching event on coral communities and reefs located on the central coast of Oaxaca in the Southern Mexican Pacific. The data indicate that bleaching caused significant mortality on Huatulco reefs by early-to-mid August. Concurrently, bleaching and mortality also occurred in the Central Mexican Pacific, the Gulf of Mexico, and the Mexican Caribbean [ 22 ].

On the Pacific coast of Mexico, coral bleaching events were associated with the ENSO event in 1982–1983 [ 20 ], as well as during subsequent ENSO events in 1987 [ 10 ], 1997–1998 [ 11 14 ], 2009–2010 [ 16 ], and 2015–2016 [ 15 17 ]. Contrary to Central America, where ENSO has had catastrophic effects from Costa Rica to Ecuador [ 8 ], coral mortality in Mexico has ranged from 15 to 60% of coral colonies [ 10 12 ] in the Baja Peninsula area. In other areas, the impact has been different. In the central area [ 14 ] and in some parts of the southern Mexican Pacific reef track (specifically, the westernmost Puerto Ángel reefs), 96% of corals died during the 1997–1998 ENSO event [ 21 ]; however, during the 2009–2010 ENSO event, mortality remained modest [ 16 ].

Depending on various factors—such as their relative strengths, onset seasons, maturity, overall duration, and the spatial extent of maximum SST anomalies—in synergy with local and regional stressors [ 3 4 ], ENSO events may lead to coral bleaching. Under adequate environmental conditions, reef-building corals fix calcium and carbonate ions in seawater to secrete a white calcium carbonate skeleton [ 5 ]. As coral tissue is translucent, coral bleaching occurs when there is a partial to complete loss of dinoflagellate algae population within the coral host (70 to >90% reduction in algal density) or a degradation of algal pigments [ 6 ]. Under mild thermal stress, the coral host can survive and recover the algal symbionts when seawater temperatures decrease over several weeks to months; however, acute and prolonged thermal stress can lead to severe coral bleaching, regardless of whether it is associated with warm or cold phases, causing extensive coral mortality and concomitant degradation of coral reef ecosystems [ 7 8 ]. The first extensive coral bleaching and mortality in the eastern Pacific associated with an ENSO event was reported by Glynn [ 9 ], who observed bleaching and mortality in the Gulf of Chiriquí and the Galapagos Islands during early 1983 but also signaled widespread bleaching and mortality in several other localities in the Pacific and Caribbean [ 9 ]. Numerous studies have addressed coral bleaching and mortality linked to both positive and negative moderate-to-strong ENSO anomalies in the eastern Pacific, extending from the Gulf of California [ 10 13 ] to the central Mexican Pacific [ 14 15 ], the southern Mexican Pacific [ 16 17 ], and Central America from Costa Rica to Ecuador (see [ 8 19 ] and the references therein).

The El Niño Southern Oscillation (ENSO) is a global-scale climatic event, with consistent records dating back to the early Holocene period in the eastern Pacific [ 1 ]. ENSO is an interannual and irregular event that alternates between two phases, El Niño and La Niña, leading to changes in sea surface temperature (SST) in extensive ocean areas compared to average conditions. While El Niño results in positive anomalies (warming), La Niña causes negative anomalies (cooling) in the ocean [ 2 ]. Both climatic anomalies can significantly stress terrestrial and aquatic ecosystems, including coral reefs [ 1 ].

The trophic level for each fish species was retrieved from FishBase [ 27 ]. The trophic level index categorizes adult fish species based on their position within the food web. Herbivores and detritivores have a trophic level below 2.20. Omnivores (low-trophic-level omnivores) who consume plant matter and other prey (e.g., sponges, isopods, and amphipods) have a level ranging from 2.20 to 2.80, while omnivores (high-trophic-level omnivores) with a preference for animals but feed on diverse prey (e.g., algae, bivalves, isopods, and fish larvae) have a value of 2.81–3.70. Piscivores and carnivores, with a preference for large decapods, cephalopods, and fish (carnivores), have a value above 3.70 [ 27 28 ].

Belt transects were used to record the echinoderm (echinoids) density (20 × 2 m, 40 m) and fish abundance and size (20 × 4 m, 80 m) three times before the 2023 El Niño bleaching event (February 2020, September–October 2021, and February 2023) and during the event (August 2023); see Table 1 . All sampling transects were haphazardly placed on each locality, running parallel to the coastline in shallow (0–5 m) and deep waters (>5 m) within the bathymetric range where reefs occur (2–18 m) [ 20 ].

The substrate was characterized via the use of a lightweight uncrewed aerial vehicle (UAV) that conducted flights over the studied area before (June–July 2017) and twice during the current 2023 El Niño bleaching event (27 June–2 July and 14–18 August 2023). The UAV flights followed a reticular pattern over the San Agustín, Riscalillo, Cacaluta, Maguey, and La Entrega reefs ( Figure 1 Table 1 ). Structure-from-motion (SfM) algorithms were implemented to recreate the substrate [ 26 ]. The substrate was identified—using a support vector machine (SVM) algorithm for each time frame, with a segmentation scale of 50—as live coral, bleached coral, dead coral, sand, and rocks. Substrate characteristics represent the percentage change in live, bleached, and dead corals before and during the heat stress event. However, only the first three substrates were visually depicted.

Monthly historic sea surface temperature (SST) records of the study area were gathered from the Hadley Centre Sea Ice and Sea Surface Temperature data set: https://www.metoffice.gov.uk/hadobs/hadisst/ (accessed on 28 July 2023). Satellite images were also gathered; daily SST records for each surveyed reef locality were obtained from January to September 2023: Aqua/MODIS, level 3 processing, 4 × 4 km resolution, http://oceancolor.gsfc.nasa.gov (accessed on 1 October 2023). Monthly pooled satellite-derived temperature data from January to September 2023 were calculated and plotted alongside historical data from 1870 to 2023. Concurrently, we obtained the daily 5 km satellite coral bleaching heat stress Degree Heating Weeks (DHW) for 1 January to 31 December 2023 from the NOAA Coral Reef Watch: https://coralreefwatch.noaa.gov/product/5km/index_5km_dhw.php (accessed on 12 January 2024). We employed the DHW product as it is directly related to the timing and intensity of coral bleaching, given that it accumulates instantaneous bleaching heat stress during the most recent 12-week period [ 25 ].

The Huatulco reef area is located on the western margin of the Gulf of Tehuantepec in the southern Mexican Pacific ( Figure 1 ). The Eastern Pacific warm pool (SST > 28 °C) influences these coastal waters; this oceanographic feature is centered off Guatemala and the southwestern coast of Mexico and is characterized by high temperatures, small annual thermal oscillations (<2 °C), an average surface salinity of 34, and the presence of a shallow (20–40 m) and relatively stable thermocline [ 23 ]. Seasonally (November through March), the area is under the influence of intense wind bursts called Tehuanos, which produce substantial changes in the structure of the water column and complex coastal circulation [ 24 ]. ENSO events, which have a frequency of 4–5 years between phases, are the predominant cause of interannual oceanographic fluctuations within the southern Mexican Pacific [ 23 ].

During La Niña and ENSO-neutral periods, we recorded 80 fish species, whereas this richness decreased significantly to 36 species during the 2023 El Niño. The majority of the decreased biomass belonged to corallivorous species (non-bleaching biomass:, 79.25 g·m67.42 g·m, 64.60 g·m) and carnivorous species (non-bleaching biomass: e.g.,, 139.22 g·m, 49.08 g·m, 41.50 g·m). The omnivorous species (19 species) with a trophic range of 2.8–3.7 and super-carnivorous species (20 species) with a trophic level greater than 3.8 exhibited the most significant declines. Prior to the El Niño event, the average trophic level was 3.43 while, during El Niño, it dropped slightly (3.28), indicating a shift toward fish with omnivorous feeding habits in the systems ( Figure 9 ).

Corals experienced no heat stress in the Huatulco area from 1 January to 16 May 2023 ( Figure 6 ). Reef surveys conducted during February 2023 resulted in non-bleached corals; however, from 17 May 2023 (day 137), the coral bleaching heat stress increased rapidly. By 21 June 2023 (day 172), DHW showed values over 5 in concordance, with a video being posted on social networks showing the coral bleaching. From 2 to 6 July 2023 (days 183–187), reef surveys presented massive coral bleaching and modest coral mortality associated with heat stress. Between 17 and 21 August 2023 (days 229–233), DHW reached values around 15–16, and reef surveys revealed massive coral mortality ( Figure 6 ). Echinoderm abundance and fish biomass also experienced significant declines. Declines in abundance were observed in both of the sea urchins(Student-t = 2.24,= 147,= 0.0001; Figure 7 a) and(Student-t = 2.01,= 147,= 0.0001; Figure 7 b) in August 2023, when compared to the previous non-bleaching sampling periods. There was also a significant decrease in fish biomass during the 2023 bleaching event (Mann–Whitney U-test = −6.9,= 147,= 0.0005; Figure 8 ) in the Huatulco area reefs.

Data analysis revealed significant changes in substrate characteristics over time in the study area. Bleaching was not observed during the non-bleaching periods (February 2020 and September 2021) but increased rapidly and significantly in the summer of 2023 (29.9%, Mann–Whitney U-test = −7.28,= 132,= 0.0001). Additionally, dead coral coverage remained relatively invariable during non-bleaching periods (19.7–24.7%) but peaked sharply during 2023 El Niño bleaching (70 ± 23.5%, Mann–Whitney U-test = −6.81,= 132,= 0.0001). Non-bleached live coral coverage remained relatively stable during non-bleaching periods (75.3–80.2%) but dropped to zero by July 2023 (Mann–Whitney U-test = 8.58,= 132,= 0.0001). In summary, the live coral coverage in the Huatulco area was approximately 75–80% during non-bleaching periods, with dead coral coverage ranging within 20–25% with no signs of bleaching. However, by July 2023, all corals at all sites had bleached entirely, and by August, 50–93% of the total coral cover had died ( Figure 4 and Figure 5 ).

Following the initial rapid survey, UAV flights rendered striking images of the area’s extent and severity of coral bleaching. During El Niño conditions, extremely clear waters allowed the UAVs to obtain imagery down to the reef base (12–17 m). The results from orthomosaic classification analysis revealed that, by late June to early July, the average coral bleaching of the entire coral area of Huatulco reached 76.85% (±12.27%). We observed moderate mortality in La Entrega (~12.31%; dead/bleached ratio [d/b] = 0.18) and San Agustín (~8.29%, d/b = 0.26), whereas it was low in Riscalillo (0.06%, d/b = 0.08), resulting in average mortality of 6.59% (±12.27%, d/b = 0.3) for the whole coral area associated with the ENSO.

Bleaching started in the Huatulco vicinity by mid–June 2023. According to a rapid survey, bleaching was widespread by late June–early July from San Agustín (15.686320°, −96.230536°) to Chahué reef (15.751882°, −96.119355°). The coral speciesandwere the most affected by bleaching, as they were entirely white across all depths (0–17 m) at all reef sites.spp. bleaching was particularly severe in shallow water (<5 m depth), with >95% ofcover bleached; however, there was a slight reduction, to 75–80% ofcover bleached, at mid-depths (5–7 m). As the depth increased (>7 m), bleaching decreased to 50–60% of the totalcover. Even though the percentage and bleaching severity decreased with depth, all of thespp. colonies were pale in color, including at the base of the coral branches. In some cases, corals presented yellow, pink, or blue fluorescence. By July 2023, we had already observed the start of coral mortality and some algal overgrowth inspp. colonies, independent of their depth ( Figure 3 ).

Positive SST anomalies occurred in Huatulco from January of 2023. Notably, anomalies were relatively higher in January (1.4 °C) but were more modest from February to April 2023 (0.2–0.48 °C). SST anomalies increased in May (0.76 °C) and, starting in June 2023, the area experienced abnormally high temperatures (>31 °C since early June; approximately 2 °C above historical records) along with calm and clear waters ( Figure 2 ). Consequently, this situation led to severe bleaching in the coral communities and reefs located in the Huatulco area.

4. Discussion

16,20, In Huatulco, the 2023 El Niño event led to a positive thermal anomaly of +1.6 °C above the historical average from June to September. Furthermore, it was 0.5 to 0.7 °C warmer than the previous (2009–2010) El Niño in the area. Consequently, the 2023 El Niño event is presently the warmest event documented in the Huatulco area. The initial observations of coral bleaching in Huatulco occurred during mid-to-late June, approximately four to six weeks after the announcement of the El Niño condition in the eastern Pacific: https://www.cpc.ncep.noaa.gov/products/CDB/CDB_Archive_html/bulletin_052023/ (accessed on 20 September 2023), and also when DHW index reached values around 3.7 to 5.6. The 2023 El Niño event is part of a sequence of strong El Niño anomalies affecting coral systems in the Mexican Pacific ( Figure 2 ) [ 14 21 ]. In 2023, coral bleaching was also reported in the central Mexican Pacific (pers. comm. Rodríguez-Troncoso, Cupul-Magaña, and Rodríguez-Zaragoza) and Baja California Sur entrance (pers. comm. Reyes-Bonilla), illustrating that bleaching is widespread in the Mexican Pacific. Concurrently, there are also reports of coral bleaching from the Gulf of Mexico [ 22 ] and the Mexican Caribbean (pers. comm. Álvarez-Filip). These reports indicate that the current El Niño event may correspond with the most devastating bleaching event ever striking coral systems in Mexico.

Pavona gigantea [ The Oaxaca reef track has experienced three bleaching events associated with ENSO events, one in 1997–1998 during La Niña [ 21 ] and the other two in 1982–1983 and 2009–2010 during El Niño conditions [ 16 20 ]. Indirect evidence suggests that the 1982–1983 ENSO event resulted in unquantifiable mortality at La Entrega reef, as indicated by the colony-size patterns of 20 ]. In the 1997–1998 cooling event, only the westernmost sites of the Puerto Ángel reef area experienced high (>90%) coral mortality [ 21 ]. Meanwhile, the 2009–2010 El Niño event caused only moderate (18%) mortality in the Huatulco reef area [ 13 ]. Conversely, the current overall mortality in Huatulco is above 50%, with numerous cases reaching values exceeding 73.8% and La Entrega experiencing unprecedented mass mortality (>92%) as heat stress values (according to DHW) reached 15.5–16.5. However, the current mortality percentages may be understated, as positive SST anomalies and El Niño conditions are predicted to persist through the first several months of 2024: https://www.cpc.ncep.noaa.gov/products/analysis_monitoring/enso_advisory/ensodisc.html (accessed on 12 January 2024). In the southern Mexican Pacific, the first news of massive coral bleaching (21 June 2023) occurred when the product reached an average of 5.4 (±0.24). However, incipient mortality occurred when the value rose to an average of 7.8 (±0.31). Nevertheless, massive coral mortality (>50%) occurred by earlier to mid–August, when DHW values reached average values of 13.2 to 15.7.

Pocillopora due to its shallower distribution compared to Pavona and Porites , making it more vulnerable to the synergy between heat shock and increasing solar radiation [32, Pocillopora spp. varies as a function of the dinoflagellate species, with Pocillopora —which hosts Durusdinium glynnii —exhibiting the highest heat tolerance in the eastern Pacific [ D. glynnii , as corals are dying regardless of species identity and depth. Nevertheless, future research on holobionts surviving the 2023 El Niño event may elucidate whether organism survival in the area relates to symbiont recombination or natural selection (sensu [ The coral genus most impacted by rising temperature in Huatulco is unquestionablydue to its shallower distribution compared toand, making it more vulnerable to the synergy between heat shock and increasing solar radiation [ 7 ]. Due to elevated temperature and irradiance, the primary disruptive mechanism causing bleaching is suggested to be damage to and reduction in the D1 protein in the photosystem II reaction center of dinoflagellate cells, as well as disruption of the Calvin cycle (which mediates photosynthetic carbon dioxide fixation) [ 31 33 ]. The bleaching sensitivity ofspp. varies as a function of the dinoflagellate species, with—which hosts—exhibiting the highest heat tolerance in the eastern Pacific [ 34 ]. We suggest that the intensity of the current El Niño could surpass the thermal tolerance of those corals hosting, as corals are dying regardless of species identity and depth. Nevertheless, future research on holobionts surviving the 2023 El Niño event may elucidate whether organism survival in the area relates to symbiont recombination or natural selection (sensu [ 35 ]).

D. mexicanum and E. thouarsii decreased by around 50%, while fish biomass decreased by 45.7%. The 2023 El Niño event has resulted in changes to holobiont physiology and affected several biological organization levels. Reductions in density and biomass were observed in echinoderms ( Figure 6 ) and fish ( Figure 7 ), respectively, alongside mass coral bleaching and mortality ( Figure 4 and Figure 5 ) when compared with non-bleaching periods. For instance, in early to mid–August 2023, the density of the sea urchinsanddecreased by around 50%, while fish biomass decreased by 45.7%.

D. mexicanum and E. thouarsii [ D. mexicanum in the tropical Eastern Pacific is relatively low (0.008–14.04 ind·m2; [ Diadema species from different regions [2 [ D. mexicanum populations tend to increase due to low predation and the availability of algal turf as a food source [2 vs. bleaching = 0.01 ind·m2) [ E. thouarsii in Huatulco have been reported to be as high as 1.14 ind·m2, exceeding those observed in the present study. It is worth noting that a population increase in E. thouarsii was recorded during the El Niño 2009–2010 event [2 compared to the 2023 El Niño density of 0.03 ind·m2. No skeletons or spines of either sea urchin species were observed on the reefs during the survey, which suggests the possibility that the organisms moved to deeper or adjacent areas rather than perishing. Both species feed primarily on algal turf and macroalgae, but they may also consume scleractinian corals [ Previous heatwave events in Huatulco have significantly impacted the echinoderm population, particularlyand 16 ]. The density ofin the tropical Eastern Pacific is relatively low (0.008–14.04 ind·m; [ 36 37 ]) compared to that of otherspecies from different regions [ 38 ]. Huatulco’s densities range from 0.26 to 6.8 ind·m 39 ]. Generally, during El Niño events,populations tend to increase due to low predation and the availability of algal turf as a food source [ 36 40 ]. Nonetheless, Huatulco populations were reduced during the 2009–2010 and 2023 El Niño events (average density: non-bleaching = 0.03 ind·mvs. bleaching = 0.01 ind·m) [ 16 ]. The population reduction during the 2009–2010 El Niño was likely due to the combination of warming events and the previous mass mortality caused by a pathogen [ 16 41 ]. This mass mortality event resulted in many loose spines and hundreds of bare tests scattered throughout the Huatulco reefs [ 41 ]. In contrast, only a few were observed during the 2023 El Niño. On the other hand, densities ofin Huatulco have been reported to be as high as 1.14 ind·m, exceeding those observed in the present study. It is worth noting that a population increase inwas recorded during the El Niño 2009–2010 event [ 16 ]. However, the opposite was observed during the 2023 El Niño, with an average non-bleaching density of 0.07 ind·mcompared to the 2023 El Niño density of 0.03 ind·m. No skeletons or spines of either sea urchin species were observed on the reefs during the survey, which suggests the possibility that the organisms moved to deeper or adjacent areas rather than perishing. Both species feed primarily on algal turf and macroalgae, but they may also consume scleractinian corals [ 42 43 ]. The observed displacement in a vertical direction could be attributed to the rise in herbivorous fish, with which the sea urchins may be competing for food (algal turf), as well as coral reduction and mortality. Further surveys and analyses are necessary to address this hypothesis.

Over the past four decades, coral bleaching events have significantly reduced live coral cover in concert with local chronic stressors, resulting in a regime shift from coral to macroalgal dominance on coral reefs worldwide [ 44 ]. According to our data, the 2023 El Niño bleaching event severely reduced the live coral cover in Huatulco and proportionally increased the coverage of turf and fleshy macroalgae. This regime shift has impacted the communities that rely on the reef for food and shelter to the point of reducing the trophic level of the fish-associated community. According to data, two elements may have contributed to the observed pattern: the dramatic reduction in fish richness and abundance—particularly of super-carnivorous taxa and corallivores—and the increases in biomass at the base trophic level. Recent studies have indicated that the reef fish community becomes increasingly dissimilar between alternative reef ecosystem states. For instance, following the 1998 El Niño disturbance in Seychelles, mid-trophic level species—including specialists such as corallivores—declined with the loss of coral habitat. However, there was an increase in biomass at base trophic levels, as herbivorous species benefitted from increased algal resources [ 45 ]. Notably, following the reef fish community and their associated changes in trophic level in Huatulco reef systems may render information for understanding the link between habitat structure, fish communities, and the concomitant trophic level changes during ecosystem recovery in impoverished eastern Pacific coral reef systems.

Pavona varians populations in Huatulco reefs may face local extinction, as these are the only populations in the southern Mexican Pacific [ Leptoseris papyracea , Psammocora stellata , and Cycloseris distorta ) [49, Stenorhynchus debilis and Trapezia spp., which are typically associated with Pocillopora spp. corals. In addition, sponges ( Amphimedon texotli ), ascidians, and gorgonians ( Leptogorgia spp.) experienced tissue and associated fauna (e.g., brittle star Ophiothela mirabilis and microcrustaceans) loss, implying that ENSO has had physiological impacts on different species, highlighting the need for future work to investigate this point further. In summary, the ENSO disturbances in the eastern Pacific have resulted in species elimination, displacement, or recruitment beyond the coral [ 46 47 ]. For instance, if the 2023 El Niño-related mortality persists,populations in Huatulco reefs may face local extinction, as these are the only populations in the southern Mexican Pacific [ 20 ]. Their loss would join the documented cases of species elimination in the Huatulco area (, and) [ 48 ], resulting in an overall decrement in range distribution throughout the eastern Pacific and, consequently, in the regional richness of coral species. On the other hand, echinoderms and fish experienced horizontal or vertical displacements in response to seasonal and interannual warming and cooling in the area, resulting in decreases or increases in the abundance and density of these species [ 16 50 ]. At present, the observed decrease in abundance is altering both density (sea urchins) and biomass (fish) metrics in the area, possibly due to the vertical displacement of individuals to deeper areas, as observed in the Central Mexican Pacific (pers. comm. Galván-Villa). Other researchers have reported that ENSO events can impact the abundance and distribution of invertebrates, primarily corallivores (e.g., mollusks and macrocrustaceans) [ 8 51 ]. Our rapid survey revealed the absence of macrocrustacean species, includingandspp., which are typically associated withspp. corals. In addition, sponges (), ascidians, and gorgonians (spp.) experienced tissue and associated fauna (e.g., brittle starand microcrustaceans) loss, implying that ENSO has had physiological impacts on different species, highlighting the need for future work to investigate this point further.

The rapid decline in stony coral coverage in the Huatulco area will likely impact the ecosystem’s carbonate budgets and reef architecture. Carbonates fixed in coral skeletons could also be lost, which has been observed in Caribbean reef-building corals affected by stony coral tissue loss disease [ 52 53 ]. Coral mortality can have far-reaching effects on reef biodiversity and socio-ecosystem functioning [ 54 55 ]. Therefore, future area monitoring can provide valuable information for estimating the extent of carbonate and functional losses [ 56 ] in southern Mexican Pacific reefs. Additionally, it can provide a baseline for local and large-scale coral reef management procedures.

The documented mass mortality of corals off Huatulco may impede reef recovery in the short- and medium-term at the regional scale, as mass mortality may profoundly alter connectivity patterns across the tropical eastern Pacific, where Huatulco is a pivotal stepping stone for reef-associated fauna from El Salvador and Costa Rica toward northwestern Pacific reefs located in areas such as Ixtapa-Zihuatanejo and those located at the entrance of the Gulf of California [ 57 ]. In this context, it is necessary to implement regional initiatives for designing and managing a network of natural protected areas to address the increasingly severe and frequent future bleaching events predicted with simulation models utilizing the latest data on bleaching incidence and projected climate change [ 58 ].

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