South Atlantic Coral Reefs Are Major Global Warming Refugia and Less Susceptible to Bleaching

Mass coral bleaching has increased in intensity and frequency and has severely impacted shallow tropical reefs worldwide. Although extensive investigation has been conducted on the resistance and resilience of coral reefs in the Indo-Pacific and Caribbean, the unique reefs of the South Atlantic remain largely unassessed. Here we compiled primary and literature data for reefs from three biogeographical regions: Indo-Pacific, Caribbean and South Atlantic and performed comparative analyses to investigate whether the latter may be more resistant to bleaching. Our findings show that South Atlantic corals display critical features that make them less susceptible to mass coral bleaching: (i) deeper bathymetric distribution, as species have a mean maximum depth of occurrence of 70 m; (ii) higher tolerance to turbidity, as nearly 60% of species are found in turbid conditions; (iii) higher tolerance to nutrient enrichment, as nitrate concentration in the South Atlantic is naturally elevated; (iv) higher morphological resistance, as massive growth forms are dominant and comprise two thirds of species; and (v) more flexible symbiotic associations, as 75% of corals and 60% of symbiont phylotypes are generalists. Such features were associated with occurrence of fewer bleaching episodes with coral mortality in the South Atlantic, approximately 60% less than the Indo-Pacific and 50% less than the Caribbean. In addition, no mass coral mortality episodes associated with the three global mass bleaching events have been reported for the South Atlantic, which suffered considerably less bleaching. These results show that South Atlantic reefs display several remarkable features for withstanding thermal stress. Together with a historic experience of lower heat stress, our findings may explain why climate change impacts in this region have been less intense. Given the large extension and latitudinal distribution of South Atlantic coral reefs and communities, the region may be recognized as a major refugium and likely to resist climate change impacts more effectively than Indo-Pacific and Caribbean reefs.


INTRODUCTION
Coral reefs are diverse marine ecosystems that harbor approximately 25% of marine eukaryotic and prokaryotic species in less than 1% of the ocean surface area (Spalding et al., 2001;Knowlton et al., 2010;Sheppard et al., 2018). However, coral reefs have suffered significantly from anthropogenic impacts such as global warming, ocean acidification, pollution and overfishing (Hoegh-Guldberg et al., 2007;Bellwood et al., 2012;Wenger et al., 2015;Hughes et al., 2018a). Marine heat waves in combination with background warming and consequential elevated sea surface temperatures are responsible for the bleaching phenomenon, in which the key symbiotic relationship between reef-building corals and photosynthetic Symbiodiniaceae dinoflagellates is disrupted (Glynn, 1993(Glynn, , 1996Fitt et al., 2001). Thermal stress induces the dinoflagellates to produce reactive oxygen species, which leads the coral host to expel them and leave its white calcareous skeleton visible under a thin and transparent tissue layer (Glynn, 1993;Lesser, 1996Lesser, , 2006. Because the symbiotic relationship is obligate for most shallow-water reef-building corals, bleaching frequently leads to coral mortality (Glynn, 1993;Brown, 1997;Hoegh-Guldberg, 1999).
Recurrent mass bleaching events have contributed to severe reduction in coral cover in both the Indo-Pacific and Caribbean regions (Sheppard, 2003;Eakin et al., 2010;De'ath et al., 2012;DeCarlo et al., 2017;Hughes et al., 2017Hughes et al., , 2018b. Loss of coral cover is often followed by decline in carbonate budgets and habitat complexity, which in turn compromises overall reef biodiversity (Pratchett et al., 2011;Descombes et al., 2015;Perry and Morgan, 2017). Mass bleaching also dramatically affects several economic activities and ecosystem services that are associated with coral reefs, such as fisheries and tourism, on which millions of people depend (Moberg and Folke, 1999;Cesar et al., 2003;Graham, 2014). Furthermore, the loss of structural complexity reduces the ability of shallow reefs to absorb wave energy and protect coastal communities from storms and erosion (Sheppard et al., 2005).
Although the impacts of mass bleaching and climate change on reef-building fauna have been well documented in several areas of the Indo-Pacific and Caribbean provinces, coral reefs in the South Atlantic remain little investigated on this regard. South Atlantic reefs are separated from the Caribbean by the Amazon-Orinoco plume and are mostly restricted to the Brazilian coast in the Western Atlantic due to upwelling preventing reef development on the African side (Le Laeuff and von Cosel, 1998;Leão et al., 2003Leão et al., , 2016. The consequence is a unique system (the "Brazilian Province, " sensu Castro and Pires, 2001;Floeter et al., 2008) with low diversity and high proportion of endemic reef-building corals distributed across approximately 3,000 km from equatorial to subtropical latitudes (Castro and Pires, 2001;Leão et al., 2003Leão et al., , 2016Pereira-Filho et al., 2019). South Atlantic reefs are also distinctive because they are mostly coastal as atolls and oceanic archipelagos are very few (Leão et al., 2016). In addition, they encompass extensive mesophotic reefs Francini-Filho et al., 2019;Soares et al., 2019) the largest rhodolith beds in the world (Pereira-Filho et al., 2011;Amado-Filho et al., 2012;Moura et al., 2016) and are significantly influenced by river discharge (Leão et al., 2003(Leão et al., , 2016Moura et al., 2016). Therefore, South Atlantic reefs display several features that are unique to them and not typically found in the more studied reef habitats of the Indo-Pacific and Caribbean.
To assess whether South Atlantic reefs are less susceptible to bleaching than those in the Indo-Pacific and Caribbean, we compiled data for the three regions and performed a comparative analysis to address six hypotheses: (i) South Atlantic coral species have a deeper bathymetric distribution; (ii) South Atlantic coral species occur more frequently in turbid waters; (iii) South Atlantic reefs occur in higher nutrient conditions; (iv) there is a greater proportion of coral species displaying resistant growth forms in the South Atlantic; (v) there is a greater proportion of generalist coral species and symbiont phylotypes in the South Atlantic; and (vi) South Atlantic reefs have fewer bleaching episodes with coral mortality. These hypotheses investigate if the following characteristics associated with thermal stress resistance are typical of South Atlantic coral populations: possibility of refuge in deeper and cooler conditions (Glynn, 1996); possibility of refuge in turbid areas that attenuate high irradiance and temperature (van Woesik et al., 2012); tolerance to local stressors that enhance bleaching effects, such as nutrient enrichment (Kuta and Richardson, 2002); robust morphology (Loya et al., 2001); and flexible symbiotic associations that may increase adaptability to environmental disturbances (Baker, 2003). Together, these topics allow for a comprehensive evaluation of whether South Atlantic corals are less susceptible to bleaching and if reefs in this area serve as climate change refugia. Addressing these topics for the South Atlantic may also bring awareness to one of the largest coral reef communities in the world, which is still relatively little investigated and neglected in most global studies.

MATERIALS AND METHODS
To address the six hypotheses, data were compiled for four specific coral traits (lower bathymetric distribution limit, occurrence in turbid waters, typical growth morphology and diversity of symbiont associations), as well as for reef nutrient concentration (inferred using nitrate) and the frequency of coral mortality associated with bleaching episodes. Data were compiled for all three regions, Indo-Pacific, Caribbean and South Atlantic, which were considered in their entirety and by including both coastal and oceanic reefs. Only zooxanthellate scleractinian and hydrocoral species were considered. The three regions (i.e., biogeographical provinces) were delimited based on their distinctive phylogeographic characteristics and following a widely used classification (LaJeunesse, 2005;Floeter et al., 2008;Roff and Mumby, 2012).

Nutrient Conditions
Nitrate (NO 3 − ) is widely used as a proxy for nutrient enrichment in marine environments (Kennedy et al., 2013). To assess whether South Atlantic reefs are found in higher nutrient conditions, we compiled nitrate (NO 3 − ) data available from scientific publications for 15 reefs in each region (References 1-37 in Supplementary Reference List S1). For three reef sites in the South Atlantic (Araripe, Porto Seguro, and Recife de Fora), data obtained in situ were provided by the Coral Vivo Institute. In cases where nitrate concentration was given as an interval, the median value between the minimum and maximum values was considered.

Symbiotic Associations
A symbiotic organism is considered as generalist when found in association with a high diversity of partner phylotypes, whereas specialists associate with a restrictive pool of partners (Baker, 2003). To investigate if corals and Symbiodiniaceae dinoflagellates in Indo-Pacific, Caribbean and South Atlantic reefs are either generalists or specialists, we compiled the symbiont diversity for 339 scleractinian and hydrocoral species that have undergone assessment (references 38-78 in Supplementary Reference List S1 for Indo-Pacific corals; 41,47,48,50,54,57,[79][80][81][82][83][84][85][86][87][88][89][90][91][92][93][94][95] for Caribbean; and 96-102 for South Atlantic). Additional primary data on South Atlantic coral symbiont diversity were provided by the Laboratório de Biodiversidade de Cnidaria at the Universidade Federal do Rio de Janeiro (authors CZ and AG). The diversity of Symbiodiniaceae dinoflagellates was considered at the Internal Transcribed Spacer 2 (ITS2) level, which is a non-coding region in the ribosomal operon that is widely used as a marker for identification and diversity assessments (LaJeunesse, 2001;Arif et al., 2014;Hume et al., 2018). For our analyses, symbiont phylotypes were considered generalists when associated with more than one coral genus. Coral species were considered generalists when associated with more than one symbiont clade, given that Symbiodiniaceae clades have recently been assigned generic status (LaJeunesse et al., 2018). Corals and symbionts associated with a single symbiont clade or host genus were considered specialists.

Mortality Associated With Bleaching Episodes
To evaluate if fewer bleaching episodes associated with coral mortality have been observed in the South Atlantic than in the Indo-Pacific and Caribbean, we compiled 775 independent bleaching records, spanning 1980 to 2018, from scientific articles available in PubMed, Scopus, Web of Knowledge and Google Scholar, and the Bleaching Database (Donner et al., 2017). Based on the information reported, bleaching records were divided into two groups, with or without associated mortality. The proportion of bleaching episodes associated with coral mortality was then calculated for each of the three regions.

Statistical Analyses
To investigate if South Atlantic species have a deeper bathymetric distribution limit, a Kruskal-Wallis test was performed followed by a Steel-Dwass post-hoc test. For differences in nitrate content, a one-way analysis of variance (ANOVA) was performed, followed by Tukey's HSD post-hoc test. One-tailed Fisher-Irwin tests were performed for proportion data (%) to assess if the South Atlantic has (a) more coral species found in turbid conditions, (b) more massive growth species, (c) proportionally fewer bleaching episodes with mortality, and a higher proportion of (d) generalist corals, and (e) generalist symbionts than the Indo-Pacific and Caribbean. Differences were considered significant at p < 0.05 for all tests.

RESULTS
The results for all statistical tests comparing differences in traits associated with resistance to bleaching between Indo-Pacific, Caribbean and South Atlantic coral reefs are summarized in Table 1.

Lower Bathymetric Limit
Analysis of the lower bathymetric limits shows that there are differences between Indo-Pacific, Caribbean and South Atlantic coral species (p < 0.001). Post-hoc tests demonstrate that corals in the South Atlantic and Caribbean have lower limits than in the Indo-Pacific (p < 0.001 for both cases). Depth limit for Indo-Pacific, Caribbean and South Atlantic species is 30.6 ± 0.7 (mean ± standard error), 59.5 ± 3.9 and 70.1 ± 9.0 m, respectively (Figure 1). Several species shared between the Caribbean and South Atlantic have been reported deeper than 100 m, such as Agaricia fragilis, Montastraea cavernosa, Madracis decactis, Meandrina brasiliensis, and Scolymia wellsii (Supplementary Table S1).

Turbidity Tolerance
South Atlantic reefs harbor a higher proportion of species that occur in turbid waters than both the Indo-Pacific (p < 0.01) and Caribbean (p < 0.01). The proportion of species that occur in turbid waters is 16, 21, and 57% for the Indo-Pacific, Caribbean and South Atlantic, respectively (Figure 1). Many South Atlantic species that are tolerant to high turbidity also display a deeper bathymetric limit, such as the cases of Mussismilia hispida, Scolymia wellsii, Siderastrea stellata, Montastraea cavernosa, and Stephanocoenia michelinii (Supplementary Table S1).

Nutrient Conditions
Nitrate content was different among Indo-Pacific, Caribbean and South Atlantic reefs (p = 0.017), with South Atlantic reefs presenting a higher nitrate content than both the Indo-Pacific (p = 0.03) and Caribbean (p = 0.04) (Figure 1). Several locations in the South Atlantic display remarkably high nitrate concentrations, occasionally above 5.0 µM (Supplementary Table S2).

Coral Growth Morphology
A higher proportion of species displaying massive growth forms are found in the South Atlantic than in both the Indo-Pacific (p < 0.01) and Caribbean (p = 0.023). Massive species comprise the majority of reef-building corals in the South Atlantic, but not in the Indo-Pacific and Caribbean (Figure 2). While South Atlantic reefs have the highest proportion of massive species, the Indo-Pacific has the lowest. For branching corals, the exact opposite pattern is observed, i.e., highest proportion in the Indo-Pacific and lowest proportion in the South Atlantic. Only three branching species occur in the South Atlantic, the milleporid hydrocorals Millepora alcicornis, M. braziliensis, and M. nitida (Supplementary Table S1).

Symbiotic Associations
South Atlantic reefs have a higher proportion of generalist coral species than the Indo-Pacific (p = 0.01 -see Table 1). However, no statistical differences were found between the South Atlantic and Caribbean. From the symbiont perspective, South Atlantic reefs have a higher proportion of generalist Symbiodiniaceae phylotypes than both the Indo-Pacific (p = 0.01) and Caribbean (p = 0.01). For species that have been evaluated for symbiont diversity, three quarters of coral species and approximately 60% of Symbiodiniaceae phylotypes in the South Atlantic are generalists (Figure 3a and Supplementary

Mortality Associated With Bleaching Episodes
South Atlantic reefs have experienced proportionally fewer bleaching episodes with coral mortality than both the Indo-Pacific (p < 0.01) and Caribbean (p = 0.01). Most South Atlantic bleaching episodes occurred in Northeastern Brazil, particularly in the coast of Bahia State (Figure 3b). No mortality was observed in 80% of bleaching episodes in the South Atlantic (Figure 3a). Additionally, no mass mortality episodes (>20% at the community level) were observed in the South Atlantic so far, including the three global mass bleaching events (Leão et al., 2016;Teixeira et al., 2019).

DISCUSSION
The analyses performed in this study confirmed six hypotheses that together argue that South Atlantic reefs are less susceptible to mass coral bleaching episodes. Below, we discuss in detail each of the six lines of investigation performed comparatively between Indo-Pacific, Caribbean and South Atlantic reefs.

Lower Bathymetric Limit
Deep and mesophotic reefs have been widely hypothesized as refugia for reef-building corals against elevated temperatures Frontiers in Marine Science | www.frontiersin.org FIGURE 2 | Composition of the main growth forms displayed by corals in Indo-Pacific, Caribbean and South Atlantic reefs. Primary growth morphology data were collected for 850 zooxanthellate scleractinian and hydrocoral species and were divided into four main categories: branching (branching, corymbose, digitate and tabular forms), massive (massive, submassive, hemispherical, dome-shaped and nodule), plate (plate, laminar and foliose) and others (encrusting, phacelloid, meandroid and solitary). (Glynn, 1996;Riegl and Piller, 2003;Bongaerts et al., 2010;Smith et al., 2014;Semmler et al., 2017;Baird et al., 2018). These reefs typically undergo less bleaching, although exceptions have been documented (Eakin et al., 2019). Deeper habitats are cooler and less susceptible to rapid temperature variations because of a lower incidence of solar radiation and light penetration (Glynn, 1996). As a consequence, most coral bleaching episodes worldwide occur in depths shallower than 20 m (Donner et al., 2017).
Our analysis on coral bathymetric distribution shows that South Atlantic and Caribbean coral species extend into deeper waters than those in the Indo-Pacific (Figure 1). This does not necessarily mean that South Atlantic reefs are deeper, but that most coral species are tolerant to the relatively low light and temperature conditions found at greater depths. The refugium potential for a geographic region may largely depend on species and context (Bongaerts et al., 2010;Smith et al., 2016) but populations of depth-generalist species tend to benefit more and become established more successfully in deeper areas (Holstein et al., 2016). In the South Atlantic, most dominant reef-building species (e.g. Mussismilia spp., Siderastrea spp., Montastraea cavernosa) are depth-generalists found in both shallow (<5 m) and deep (>30 m) environments (Leão et al., 2003(Leão et al., , 2010(Leão et al., , 2016Francini-Filho et al. (2019) Supplementary Table S1). In addition, many South Atlantic species thrive in conditions of significant light attenuation (Freitas et al., 2019). Therefore, many South Atlantic coral species are already adapted to and occur in depth zones that may shelter them from bleaching caused by global warming impacts.

Turbidity Tolerance
Corals adapted to lower light levels are also likely to tolerate turbid waters. Turbid reef environments may also serve as refugia from climate change impacts, as the suspended particles protect corals from high irradiance and reduce the intensity of thermal stress (Iglesias-Prieto and Trench, 1994;van Woesik et al., 2012;Cacciapaglia and van Woesik, 2016;Sully and van Woesik, 2020). During the third global mass bleaching event, turbid sections of the Great Barrier Reef showed remarkable tolerance and underwent little or no bleaching . South Atlantic reefs are naturally turbid and associated with high sediment loads, mostly because of resuspension of fine sediments and terrigenous discharges from large rivers such as the Amazon, São Francisco, Doce and their many affluent streams (Dutra et al., 2006;Castro et al., 2012;Silva et al., 2013;Omachi et al., 2019). For instance, the Abrolhos reefs, which are the largest coral reefs in the South Atlantic, are associated with a high content of siliciclastic sand and mud, which is atypical for Caribbean and Indo-Pacific reefs (Leão and Kikuchi, 2001).
Our analysis shows that more than half of South Atlantic coral species are tolerant to turbid environments, which is more than twice than the proportion recorded for the Caribbean and more than three times higher than that for the Indo-Pacific (Figure 1). An emblematic example is Mussismilia braziliensis, an endemic species which is one of the main South Atlantic reef-builders, that displays higher growth rate and reproduction effort when found in more turbid conditions (Pires et al., 2011;Ribeiro et al., 2018). In addition, turbid inshore reefs in the South Atlantic often display higher coral cover and abundance than less turbid offshore reefs, particularly Montastraea cavernosa (Francini-Filho et al., 2013;Loiola et al., 2019). Therefore, unlike for the Indo-Pacific and Caribbean, most South Atlantic coral species have already adapted for thriving in turbid environments that may prove critical for surviving the increasing impacts of climate change and mass bleaching episodes.

Nutrient Conditions
Along with sediment, river run-off also releases considerable nutrient quantities. Nutrification often works in tandem with climate change and typically triggers negative impacts on coral reefs such as reduction in bleaching temperature threshold and disease outbreaks (Kuta and Richardson, 2002;Schlöder and D'Croz, 2004;Wiedenmann et al., 2013). However, local environmental stressors such as high nutrient concentration may also favor and select coral species or genotypes that are stresstolerant, leading to more resistant species and populations over evolutionary time scales (Côté and Darling, 2010).
Our findings show that the mean nitrate concentration in South Atlantic reefs is approximately 2.5 times greater in comparison to those in the Indo-Pacific and Caribbean (Figure 1). South Atlantic coral reefs are typically found and develop under higher nitrogen, phosphorus and chlorophyll-a content (Leipe et al., 1999;Costa et al., 2002Costa et al., , 2006. In fact, in several South Atlantic reef areas, the soluble reactive phosphorus content is among the highest in all of the world's reefs (Costa et al., 2008). While urban pollution has been hypothesized as a driver for disease outbreaks in the South Atlantic (Francini-Filho et al., 2008) there have been no reports of disease or mortality associated with the naturally higher nutrient concentration. In addition, South Atlantic corals seem to benefit from high nutrient levels by increasing their abundance and reproductive output (Pires et al., 2011). Therefore, South Atlantic corals appear to be more tolerant to nutrification. Furthermore, South Atlantic reefs are also farther from nutrient depletion. The increase in sea surface temperature is likely to produce intense stratification in the next decades and limit nutrient availability in coral reefs (Moore et al., 2013). Because nutrient depletion (<0.05 µM of both nitrate and phosphate) is associated with decrease in photosynthetic activity and enhanced bleaching effects (Ezzat et al., 2019). South Atlantic reefs are also less vulnerable to impacts connected to nutrient starvation.

Coral Growth Morphology
Corals may also display morphological adaptations that reduce the impacts of high temperature and irradiance. Mostly because of their skeletal architecture, thicker tissues and high metabolic rates, massive corals are more resistant to thermal stress and other impacts than branching ones (Gates and Edmunds, 1999;Loya et al., 2001;Schlöder and D'Croz, 2004). Their higher content of soluble proteins and photosynthetically-fixed carbon inside tissues are also key factors in their adaptation to exacerbated environmental disturbances (Gates and Edmunds, 1999).
Our findings show that massive growth forms comprise the majority of reef-building species in the South Atlantic, unlike the Indo-Pacific and Caribbean (Figure 2). Almost two thirds of South Atlantic coral species are massive, with reefs largely formed by genera such as Siderastrea, Montastraea and Mussismilia. The latter is the most widespread in the South Atlantic, and an endemic relict genus dating back to the Tertiary (Leão et al., 2016). Mussismilia spp. have been widely reported as stresstolerant organisms (Leão et al., 2003;Loiola et al., 2013;Mies et al., 2018). Among branching corals, only three species occur in South Atlantic reefs, while several species within the Millepora, Acropora and Porites genera are found in the Caribbean. In the Indo-Pacific, branching acroporids and pocilloporids account for most of the coral cover (Clark et al., 2017) and less than one third of species in that region is massive. The higher proportion of massive and the lower number of branching species compared to other regions is another factor suggesting that South Atlantic reefs are relatively more tolerant to thermal stress.

Flexibility of Symbiotic Associations
Another critical component in the coral response to thermal stress is the photosynthetic symbiont community that resides within its tissue. Symbiont identity itself is a major predictor of thermal tolerance (Berkelmans and van Oppen, 2006;Hume et al., 2015;Swain et al., 2017) but the flexibility of the symbiotic relationship is also a key factor. The capacity of corals to establish a relationship with a wide symbiont diversity is an important mechanism for rapid acclimation and adaptation to environmental disturbances (Baker, 2003;Baker et al., 2004;Little et al., 2004;Baird et al., 2007).
Our analysis shows that South Atlantic and Caribbean reefs have proportionally more generalist coral species than the Indo-Pacific (Figure 3a). South Atlantic reefs also have more generalist symbiont phylotypes than both the Indo-Pacific and Caribbean. So far, only Symbiodiniaceae genera Symbiodinium, Breviolum, Cladocopium, Fugacium, and Gerakladium (formerly clades A, B, C, F, and G, respectively -see LaJeunesse et al., 2018) have been reported for the South Atlantic (Silva-Lima et al., 2015;Picciani et al., 2016;Teschima et al., 2019; Supplementary Table S4), but a remarkable 60% of local phylotypes are generalists. In addition, the most abundant phylotypes occur in a wide range of environmental conditions along the Southwestern Atlantic coast (Silva-Lima et al., 2015) reinforcing their physiological plasticity. Generalist phylotypes such as A4 (Symbiodinium linucheae), C1 (Cladocopium goreaui), and C3 are commonly found in South Atlantic locations that undergo drastic changes in temperature and other abiotic factors (Teschima et al., 2019). Generalist phylotypes also predominate in turbid Caribbean and Indo-Pacific reefs, especially Durusdinium trenchii (D1a) (LaJeunesse et al., 2014;Pettay et al., 2015). This species has recently invaded Caribbean reefs and are distributed in several reefs that underwent disturbances (Pettay et al., 2015;Chen et al., 2020). However, the Durusdinium genus has not yet been recorded for the South Atlantic and other generalist phylotypes within multiple genera dominate. Therefore, South Atlantic corals are thus not only typically generalists, but also tend to associate with generalist symbionts. This symbiotic flexibility allows for adaptive shifts in the symbiont community, which can be critical in increasing resistance and resilience to bleaching (Baker et al., 2004). Still, symbiont diversity data are missing for several species and this is imperative for further understanding the response of South Atlantic corals to climate change and other disturbances.

Mortality Associated With Bleaching Episodes
The five traits addressed above are likely major contributing factors for South Atlantic reef corals to suffer fewer bleaching episodes with associated mortality than those in the Indo-Pacific and Caribbean. Until 2018, there were only 44 independent bleaching records for the entire South Atlantic (Figures 3a,b), most of them from the 1990's onward, when more systematic monitoring programs began by dozens of independent Brazilian research groups. Only 20% of those records reported mortality, which is approximately 60 and 50% lower than the number of coral mortality reports due to bleaching for the Indo-Pacific and Caribbean, respectively (Figure 3a). Mortality reports in the SA are in most cases associated with hydrocoral species (Millepora spp.), which are typically branching and inhabit very shallow depths (Amaral et al., 2006;Santos et al., 2016;Teixeira et al., 2019). Only a single mass coral mortality EPISODE has been recorded for the South Atlantic reefs (also mostly associated with Millepora spp., despite occurring in turbid conditions Duarte et al., 2020) and none of the three major global mass bleaching events that affected the Indo-Pacific and Caribbean had comparable effects in the South Atlantic (Kelmo et al., 2003;Teixeira et al., 2019). Further evidence for the resilience of South Atlantic reefs is that a heat stress of 7.7 • C-weeks (degree heating weeks, which accounts for the accumulation of temperature anomalies exceeding the monthly maximum mean Liu et al., 2006;Kayanne, 2017) caused 20% coral mortality in the Caribbean (Florida Keys) and 13 • C-weeks caused 80% mortality in Indo-Pacific (Australia) reefs, however, a remarkable value of 20 • C-weeks, ranking among the highest ever recorded, resulted in less than 2% mortality in the marginal reefs of the Southwestern Atlantic (Gilmour et al., 2013;Gintert et al., 2018;Banha et al., 2019). And even more recently, in late 2019, 19.6 • C-weeks recorded for the diverse Abrolhos reefs caused no significant mortality for any reef-building species with the exception of the branching and fast-growing hydrocoral Millepora alcicornis and, to a lesser extent, the phacelloid Mussismilia harttii, further highlighting the resilience of South Atlantic reefs to heat stress (Duarte et al., 2020). Two additional advantages are that the South Atlantic is historically and currently less exposed to heat waves (Skirving et al., 2019) and that the largest reefs in the South Atlantic are found in the Abrolhos Bank, which is systematically influenced by cooler-water eddies that reduce thermal stress (Ghisolfi et al., 2015). Therefore, it is likely that the relatively smaller impacts of bleaching are a consequence of both the resistance and resilience of local coral species and the lower intensity and frequency of heat waves. In fact, specific physical oceanography studies on South Atlantic heat waves are warranted for further context.
The resistance of South Atlantic coral fauna to bleaching was first proposed by Leão et al. (2003Leão et al. ( , 2010 likely as a consequence of biogeographic and evolutionary processes. Caribbean and South Atlantic coral fauna were separated probably during the late Cretaceous, when continental elevation in western South America and changes in ocean circulation directed the flow of the Amazon River to the Atlantic Ocean (Frost, 1977;Leão, 1983;Leão et al., 2003). These events resulted in an adverse FIGURE 4 | General comparison of Indo-Pacific, Caribbean and South Atlantic reefs: (A) Depiction of main characteristics that make South Atlantic reefs more resistant: (i) deeper mean distribution limit for coral species, (ii) tolerance of coral species to turbid conditions, (iii) reefs found in higher nutrient conditions, (iv) predominance of massive coral species (with proportion of massive and branching forms displayed according to Figure 2), (v) prevalence of generalist corals and symbionts (not shown in figure), and (vi) lower incidence of severe bleaching episodes (with proportion of bleached colonies according to Figure 3). (B) In situ photographs of typical coral reef morphology in the Indo-Pacific (branching forms at Milln Reef, Great Barrier Reef), Caribbean (mixed branching and massive forms at Andros Island, Bahamas) and South Atlantic (massive forms at Fernando de Noronha Archipelago, Brazil). oceanographical environment for the development of coral reefs, thereby selecting resistant species (Leão et al., 2003(Leão et al., , 2008Vasconcelos et al., 2018). This kept acroporids entirely out of the South Atlantic and favored massive species with large corallites, which aid in sediment cleaning and heterotrophic feeding (Logan, 1988;Crabbe and Smith, 2002;Mies et al., 2018;Marangoni et al., 2019). Therefore, South Atlantic corals may represent something of a resistant subset of Caribbean coral diversity.

PERSPECTIVE AND CONCLUSION
Coral bleaching is intensifying in the Indo-Pacific and Caribbean as large-scale episodes are becoming more frequent and longerlasting (Hughes et al., 2019). However, this does not seem to be the case for the South Atlantic. Our results show that South Atlantic corals occupy greater depth zones, are tolerant to higher turbidity and nutrification, are morphologically resistant, engaged in flexible symbiotic associations, and most importantly, are less affected by bleaching (Figures 4A,B). In addition, they harbor numerous mesophotic reefs, possibly more than anywhere else in the world, that may serve as additional refugia (Soares et al., 2019). This qualifies South Atlantic reefs, especially its largest reefs in the Abrolhos Bank, as bioclimatic units (BCUs). BCUs are defined as large reef areas with lower vulnerability to climate disturbances and well-connected to surrounding marine ecosystems (Hoegh-Guldberg et al., 2018). However, it is important to note that although South Atlantic reefs have been historically less affected by bleaching, they are still vulnerable to increases in sea surface temperature (Kelmo et al., 2003).
The global disparity in coral reef resistance and resilience to climate change has already been demonstrated for the Indo-Pacific and Caribbean (Roff and Mumby, 2012;Cinner et al., 2016) but never assessed comprehensively for the South Atlantic. Besides the vertical (bathymetric) refugium that South Atlantic reefs may offer, their extended latitudinal distribution of approximately 3,000 km makes them one of the largest coral reef refugia in the world. However, it remains to be seen how these reefs will respond under continuing ocean warming. Unfortunately, South Atlantic reefs and its marine protected areas still lack adequate management programs and enforcement. In face of the increasing magnitude of climate change, local management is often ineffective for oligotrophic reefs dominated by bleaching-susceptible species (Bruno et al., 2019). However, this may not be the case for the South Atlantic, where climate change impacts on corals are less dramatic due to intrinsic characteristics. Therefore, enhancing local conservation policies is warranted. Climate refugia may offer habitat persistence and increase biodiversity over evolutionary time scales (Pellissier et al., 2014) highlighting the importance of considering South Atlantic reefs as priorities for conservation.

DATA AVAILABILITY STATEMENT
All datasets generated for this study are included in the article/Supplementary Material.

AUTHOR CONTRIBUTIONS
MM, RF-F, CZ, AGG, GL, PS, and TB designed the work. MM, RF-F, CZ, AGG, GL, EL, and TB collected data. MM, RF-F, AGG, AZG, and TB analyzed the data. All authors contributed to the manuscript.

ACKNOWLEDGMENTS
We thank Coral Vivo Institute, Petrobras (through the Petrobras Environmental Program) and Arraial d'Ajuda Eco Parque for data provided, Linda Waters and Christian Voolstra for reviewing the manuscript and Fernando Saraiva, Gayle Plaia, and Zaira Matheus for illustrations and pictures.