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![Studied areas at Rocas atoll, NE Brazil, indicating the different habitats.
The large scale map was plotted with the R software using the 'maptools' package [41] based on data provided by the GEOphysical DAta System—Next Generation (GEODAS-NG) of the NOAA (https://www.ngdc.noaa.gov/mgg/geodas/geodas.html). The illustration of the atoll was adapted from [39] but is not identical.](profile/Guilherme-Longo/publication/278160252/figure/fig9/AS:340496791687176@1458192169320/Studied-areas-at-Rocas-atoll-NE-Brazil-indicating-the-different-habitats-The-large.png)
Studied areas at Rocas atoll, NE Brazil, indicating the different habitats. The large scale map was plotted with the R software using the 'maptools' package [41] based on data provided by the GEOphysical DAta System—Next Generation (GEODAS-NG) of the NOAA (https://www.ngdc.noaa.gov/mgg/geodas/geodas.html). The illustration of the atoll was adapted from [39] but is not identical.
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The Southwestern Atlantic harbors unique and relatively understudied reef systems, including the only atoll in South Atlantic: Rocas atoll. Located 230 km off the NE Brazilian coast, Rocas is formed by coralline red algae and vermetid mollusks, and is potentially one of the most "pristine" areas in Southwestern Atlantic. We provide the first compre...
Citations
... Our study highlighted a combination of seven different physical/chemical environmental drivers that explain, at different scales, the distribution patterns of CRA. The study area stretches across 29 degrees of latitude (from 1°N to 27°S), which naturally implies a wide variety of ecological conditions resulting from differences in abiotic variables (Adey and Steneck 2001) and biological interactions, such as herbivory-the major biotic driver of macroalgal composition (Floeter et al. 2005;Bonaldo and Hay 2014;Longo et al. 2015). ...
Coralline red algae (CRA) are key players in the construction and maintenance of biogenic reefs, and they have important functional roles in ecological systems in the Southwestern Atlantic (SWA). Like many other marine organisms, CRA are currently affected by global and local stressors, but little is known about their biodiversity and the environmental drivers that influence their distribution patterns in the SWA. In the present study, we quantified the species richness of CRA in six ecoregions within the SWA using DNA-based species delimitation methods. We then verified their distribution and identified the main drivers shaping the macroecological patterns of richness and β-diversity. We found 79 phylogenetic species that belong to the three main CRA orders (Sporolithales, Corallinales, and Hapalidiales), in the tropical and warm temperate SWA. Temperature, nutrients, and water current velocity were the main environmental drivers of CRAs in the evaluated ecoregions. The Eastern Brazil ecoregion stands out due to its high richness, exclusive species, β-diversity between ecoregions, and as a transitional zone of the SWA. The results of our study have several important practical implications with repercussions for monitoring actions and conservation planning for the coastal region. These results show that each ecoregion has unique characteristics, and the mesophotic habitat is of primary importance because it harbors species that are not found in other habitats, and because it provides structural connectivity with shallower habitats.
... It is important to note, however, that the Atlantic sediment suckers appear to be more labile in this feeding behaviour than their Indo-Pacific counterparts, with several studies highlighting that they can also predominantly feed over turf on hard substrata (Robertson 1991;Francini-Filho et al. 2010;Duran et al. 2019). Nevertheless, given the feeding habits of most sediment suckers, their gut contents are generally dominated by inorganic sediments and organic particulate material (Dias et al. 2001;Debenay et al. 2011;Longo et al. 2015;Kelly et al. 2016). Notably, sediment suckers also often reach their highest abundances in low energy back reef and lagoon habitats (Fig. 8f) (Russ 1984b;Lewis and Wainwright 1985), where their preferred feeding substrata are relatively abundant. ...
... Therefore, when feeding over mixed substrata or hard substrata they are likely to remove algae as well as particulates. Consequently, substantial quantities of algal material have been found in the gut contents of sediment suckers (Clements 2015), especially in the Atlantic (although sediment and detritus are still often major components as well) (Randall 1967;Dias et al. 2001;Dromard et al. 2015;Longo et al. 2015;Mendes et al. 2018). Nevertheless, sediment suckers are generally united by the possession of a gizzard-like stomach, multidenticulate teeth and feeding over soft or mixed-substrata. ...
... However, it is highly likely that sediment suckers also play a major role in this function. This is because, like brushers, sediment suckers ingest and process substantial quantities of sediment when feeding (Jones 1968;Kopp et al. 2010;Longo et al. 2015). Furthermore, many species of sediment suckers are relatively large (e.g. ...
Surgeonfishes have had a long evolutionary history that has been closely linked with coral reef ecosystems. Today they are a key component of reef fish assemblages, playing a pivotal role in a variety of ecosystem functions. However, coral reefs are at the forefront of environmental change with a suite of stressors pushing these ecosystems towards alternative configurations. The role of surgeonfishes in these ecosystems may be changing and our understanding of these fishes must now be considered within a context of change. To explore these issues, we review the literature on surgeonfishes and examine (1) how their functional roles on coral reefs have evolved over the past 50 million years, (2) the key functions performed by surgeonfishes on present-day coral reefs, and (3) predict how the nature and importance of these roles may change in the near future (~ 30 years). Specifically, we draw on recently clarified functional frameworks to categorise surgeonfishes into six broad functional groups (browsers, brushers, croppers, concealed croppers, sediment-suckers, water-column feeders) using morphological and behavioural traits. Subsequently, we explore how these functional groups make critical contributions to the ecosystem processes of macroalgal removal, algal turf removal, detritus removal, sediment dynamics, plankton harvesting and cross-habitat trophic linkages. Furthermore, using this framework we consider how environmental factors, anthropogenic stressors, as well as other behavioural and morphological traits can shape the delivery of key functions by surgeonfishes. Finally, we highlight how surgeonfishes may play increasingly important roles in supporting key functions and services on current and future, highly-altered, coral reefs.
Graphical abstract
... Algae species were grouped in: articulated calcareous algae (ACA), corticated, crustose, filamentous, foliose and leathery, following Steneck and Dethier (1994) morphological groups classification. The epilithic algae matrix forming thick mats < 2 cm tall were classified as ''turf'' (Connell et al., 2014;Longo et al., 2015). Animal groups were classified according to phylum except for cnidarians that were separate in zoanthids and other cnidarian (anemone Bunodosoma sp.). ...
... To identify macroalgal components of the turf possibly found in the gut content, we scraped the substrate using quadrats (10 × 10 cm) haphazardly placed in the same sampling area with five replicates in each site (Longo et al., 2015). In the lab, the turf was sifted with a three-level sieve (710, 500, and 425 µm) and washed with distilled water to separate the sediment from the organic matter. ...
Sea urchins play a key role in shallow rocky shores, acting as modulators of abundance, density and species composition of macroalgae. In communities that host more than one species, understanding how trophic resources are used and partitioned is a key aspect of understanding the ecosystem’s dynamics in which they are inserted. In Southern Brazil, Echinometra lucunter and Paracentrotus gaimardi show a high spatial overlap, in the upper (1–3 m) subtidal zone. Because trophic niche differentiation largely contributes to the coexistence of species, we hypothesize that the evaluated species will have low overlap in diet since they share the same habitat and have access to similar resources. Therefore, this study aimed to investigate the stomach contents of twenty (20) individuals of each species, in two sites (Gravatá and Matadeiro rocky shores) to verify feeding patterns of the species. Using taxonomic and morphological levels in identifying stomach contents and Pianka’s index to assess the degree of trophic overlap between species in each site. It was found that despite the differences in benthic composition, the feeding patterns of both species were similar in both sites with the species being classified as generalist herbivores. The species showed a low degree of dissimilarity in the acquisition of trophic resources, and a high trophic overlap. The results indicate that the main influencing factor of the feeding patterns was the availability of resources. The high trophic overlap occurs due to the generalist behavior of the species, which use and share the resources available in the environment.
... Indeed, large kelp plants and coralline algae are only consumed by a few specialized organisms (Andrew & Jones, 1990;Nicholson & Clements, 2020; Table S5), their productivity being largely exported to other habitats as detritus (Krumhansl & Scheibling, 2012). For instance, the skeleton of coralline algae makes them relatively unpalatable and very well-defended, with few herbivore species being able to feed on them even in areas with diverse herbivore assemblages (Longo et al., 2015). ...
The structure of ecological communities is rapidly changing across the globe due to climate‐mediated shifts in species distributions, with novel ecosystem states emerging as new species become dominant. While it is clear that such changes restructure habitat properties and their associated assemblages, how new nutritional resources and consumers may affect the ecosystem trophic structure and energetic dynamics remains poorly resolved. Here, we investigate how the reconfiguration of tropicalized reefs—that is, temperate ecosystems receiving an influx of tropical species—affects the availability of nutritional resources and energy flow through herbivore‐based trophic pathways. To do so, we quantified changes in algal and detrital resources along a tropicalization gradient in eastern Australia. We also estimated energy flow towards herbivorous fishes by quantifying their standing biomass (kg/ha), productivity (kg ha−1 day−1), and biomass turnover (% day−1), using an individual‐level modelling approach that combines estimates of fish growth rates and mortality. Along the gradient, tropicalized reefs had relatively higher amounts of palatable algal turfs and detrital particulates compared to non‐tropicalized sites. Feeding intensity by herbivorous fishes was also c. 400 times higher on tropicalized reefs, with tropical turf‐cropping surgeon fishes being responsible for >98% of the feeding rates. Turf‐driven trophic pathways underpinned virtual all (>99%) of the biomass produced by tropical fishes, which contributed up to 63% of the total herbivorous fish standing biomass and 86% of the productivity despite only representing 35% of the abundance. Turfs also fuelled most of the secondary productivity of tropical fishes on tropicalized reefs across Australia's western tropical–temperate transition zone, although their overall productivity was ~5 times lower. This is possibly due to turfs there containing elevated sediment loads, which dilute the nutritional quality of turf‐based resources, as well as other differences in the biogeographical context. We propose that algal turfs are central drivers of ecosystem energetic shifts on temperate reefs as they become tropicalized because they support novel algal and detrital trophic pathways that enhance secondary productivity and biomass turnover. Our results also suggest that turf characteristics such as organic content or sediment load may emerge as increasingly important drivers of energy flow in temperate locations where turfs dominate benthic cover. A free Plain Language Summary can be found within the Supporting Information of this article. A free Plain Language Summary can be found within the Supporting Information of this article.
... In the Southwest Atlantic, however, reefs are naturally characterized by low coral cover (Leão et al., 2003;Aued et al., 2018), even those geographically isolated and with little human influence. In fact, turf algae and macroalgae are the major components of reef benthic communities across all of the Brazilian Province, including oceanic islands (Pereira-Filho et al., 2011;Fonseca et al., 2012;Longo et al., 2015;Magalhães et al., 2015;Meirelles et al., 2015;Aued et al., 2018;Matheus et al., 2019). This distinct structure is possibly related to the setting of environmental conditions under which these ecosystems have developed over time. ...
... Although there are some temporal studies on reef benthic communities along the Brazilian coast, to date, only spatial or short-term assessments of reef benthic communities in Brazilian oceanic islands are available (Laborel, 1970;de Eston et al., 1986;Pires et al., 1992;Maida et al., 1995;Ferreira et al., 2006Ferreira et al., , 2012Krajewski et al., 2010;Krajewski and Floeter, 2011;Pereira-Filho et al., 2011;Amado-Filho et al., 2012;Longo et al., 2015;Magalhães et al., 2015;Meirelles et al., 2015;Aued et al., 2018;Matheus et al., 2019) and the lack of methodological standardization jeopardizes temporal comparisons. Additionally, there is a gap in the understanding of environmental drivers that most influence communities' structure, which has already been raised by other studies (Francini-Filho et al., 2013). ...
... The overall community structure was consistent with the preexisting information for FNA's shallow reefs (de Eston et al., 1986;Krajewski and Floeter, 2011;Aued et al., 2018;Matheus et al., 2019). It was also comparable with reefs at similar depths from the other three Brazilian oceanic islands (Pereira-Filho et al., 2011;Fonseca et al., 2012;Longo et al., 2015;Magalhães et al., 2015;Meirelles et al., 2015), especially in terms of high abundance of turf algae (here referred to as EAM) and macroalgae. Indeed, the dominance of these two benthic groups was already described for reef benthic communities from all the Brazilian Province (Aued et al., 2018). ...
Reefs are the richest marine ecosystems. Their benthic communities generate structural complexity and participate in nutrient cycles, providing habitat and food for many marine species. These ecosystems have been threatened by local and global anthropogenic impacts and changes in community structure have led to loss of biodiversity, ecosystem function and services worldwide. Most studies about these structural changes have been conducted in Caribbean and Indo-Pacific coral reefs. In the Southwestern Atlantic, where reefs are naturally algae-dominated, these efforts are incipient, especially at oceanic islands where local anthropic impacts tend to be lower, and natural and climate-induced fluctuations might be easily detected. We conducted the first temporal assessment of benthic communities and the influence of oceanographic parameters between 2013 and 2019 in Fernando de Noronha (FNA), the largest Brazilian oceanic archipelago. We annually sampled benthic communities in FNA’s shallow reefs (2–21 m) using photoquadrats, quantified and gathered organisms in major groups according to their functional roles. We also characterized and tested “sea surface temperature,” “marine heatwaves,” “diffuse attenuation coefficient,” and “wave energy” influence for the same period. The most abundant groups were epilithic algal matrix (EAM; mean annual coverage: 23–60%), macroalgae (15–35%) and calcifiers (15–29%), followed by cyanobacteria (1–37%), suspension/filter-feeders (<2%), zoanthids (<1%) and other invertebrates (<0.1%). EAM was negatively correlated with “marine heatwaves” and positively correlated with “wave energy,” while macroalgae and calcifiers showed opposite responses to “marine heatwaves” and “wave energy,” respectively. Cyanobacteria was positively correlated with “marine heatwaves.” The dominance of EAM and macroalgae was already described for reefs along the Brazilian Province and we demonstrated the persistence of this structure over the years in FNA, with the exception of 2019 when there was a substantial increase of cyanobacteria after a strong marine heatwave. Our results suggest a flickering dynamic between EAM and macroalgae, which vary according to the oceanographic conditions, reinforcing its distinct dynamics from most tropical coral reefs. However, the increase of cyanobacteria added to projections of more frequent and stronger marine heatwaves worldwide indicate possible structural changes in this community. Continued monitoring of community and oceanographic drivers is key for better understanding and predicting changes in important marginal reefs.
... We measured the per capita consumption rate of the surgeonfish Acanthurus chirurgus feeding on the red seaweed D. simplex, its primary diet item (Longo et al. 2015), in a tide pool in the Rocas Atoll (32°00′W-34°00′W longitude and 03°30′S-04°30′S latitude, Fig. 1). The area of the pool where the study was conducted was about 595 m 2 (70 × 8.5 m). ...
... The area of the pool where the study was conducted was about 595 m 2 (70 × 8.5 m). In this pool, hardly any Digenea simplex was available for fish to eat, as it was mostly covered by sand (Longo et al. 2015). The surgeonfish A. chirurgus is a diurnal grazer that mostly feeds on algae and organic detritus found on compacted sand and rocky bottoms (Choat et al. 2002, Ferreira and Gonçalves 2006, Longo et al. 2015. ...
... In this pool, hardly any Digenea simplex was available for fish to eat, as it was mostly covered by sand (Longo et al. 2015). The surgeonfish A. chirurgus is a diurnal grazer that mostly feeds on algae and organic detritus found on compacted sand and rocky bottoms (Choat et al. 2002, Ferreira and Gonçalves 2006, Longo et al. 2015. Maximum movement distance of 215 m is reported for A. chirurgus (Chapman and Kramer 2000). ...
In theoretical ecology, the quantity of resource consumed by a consumer per unit of time, defined as functional response, is of paramount importance. To better understand species interactions over time it is necessary to analyze whether consumer's functional response depends on resource density alone (which is the reference assumption) or on both resource and consumer densities. There are few field studies that, by varying the resource and consumer densities, provide solid empirical evidence to indicate the most suitable model of functional response in complex systems, such as coral reefs. We performed a field experiment with an herbivorous surgeonfish and their resource, a red seaweed, in a near-pristine reef ecosystem. We measured algal consumption while varying densities of consumers and resources. We fit nine alternative functional response models, which either included or excluded consumer-dependence. The model selection and the parameter estimation indicated that the functional response of the her-bivorous surgeonfish depended on the ratio of seaweed to herbivorous fish densities. These results imply that, within a given density, surgeonfish can share resources but individual's consumption rate decrease with higher fish densities. These results also suggest that mutual intraspecific interference exists at herbivorous fish densities generally observed in the field and it should be considered in predicting consumption rates by herbivorous reef fishes. Finally, this study indicates that models incorporating consumer dependence must be considered for understanding herbivorous fish and algae population dynamics when placed in the context of the most biodiverse ecological communities, such as reef ecosystems.
... For instance facultative cleaners such as Thalassoma noronhanum, T. adscensionis, T. lucasanum, Johnrandallia nigrirostris and Stegastes santicpauli account for about 15% of the total abundance in several locations in the Atlantic and Eastern Pacific (Krajewski & Floeter, 2011;Longo et al., 2015;Luiz et al., 2015;Quimbayo et al., 2019). ...
Several drivers explain the global distribution of all reef fish. However, whether these drivers also explain the distribution and traits of a functional subgroup involving cleaner fishes remain unclear. Here we examine the variation in traits of cleaner fishes and test whether historical, environmental, ecological and geographical drivers are correlated with cleaner species richness and abundance at global reefs. Tropical and subtropical reefs. Actinopterygii. We tested whether species traits and trait space vary between facultative (i.e. species that clean only during the juvenile stages or sporadically) and dedicated (i.e. species that clean during their whole lives) cleaner types. We compiled data from local checklists (relative richness) and belt transects (standardized richness and abundance). We built four models to test whether past and current isolation (i.e. distance from Quaternary refugia and biodiversity centres), sea temperature, primary productivity, local species pool and abundance of potential clients influenced the relative richness and abundance of cleaners. Facultative cleaners had high trait variability that contributed disproportionally to the trait space, whereas dedicated cleaners exhibited low trait variability. Cleaner species richness was higher in the Indo‐Pacific and Caribbean provinces, but the relative richness and standardized abundance of cleaners were higher in the Atlantic (i.e. North Eastern and Southwestern) and Eastern Pacific. Isolation influenced the relative richness of facultative cleaners, whereas the distance to Quaternary refugia, sea temperature and isolation influenced the relative richness of dedicated cleaners. Local species richness and standardized abundance of cleaner fish exhibited a strong relationship with regional diversity. The standardized abundance of both facultative and dedicated cleaners was influenced by the abundance of potential clients and the local species pool. The small trait space occupied by cleaner fishes may reflect their restricted origin among lineages of reef fishes. Differences in the relative richness and standardized abundance of cleaner fishes across marine realms suggest a strong influence on biogeographical history. Our results also indicate that cleaner fishes originated mostly in peripheral areas in high latitudes due to the absence of dedicated cleaners. Our results imply that cleaner fishes do not follow the pattern of main centres of origin described for reef fishes due to opportunistic cleaning behaviour that originated with higher frequency at locations with low species richness.
... It has controlled anthropic impacts (e.g. very low pollution and shing) and it is probably the most similar to a pristine reef in Brazil, being a natural laboratory and an important study area (Longo et al. 2015). ...
... Wilderness areas as Rocas Atoll support unique ecological values, different from the ones near the coast, due to well-managed efforts and limited human pressure, being the only environment considered as near pristine in Brazil(Longo et al. 2015). In our research, due to the maintenance in number of functional entities, small oscillations in FRic and FEnt, ecosystem functions do not seem to vary substantially, indicating a stable state dominated by primary producers and tridimensional complexity functional entities over the years. ...
Reef benthic communities provide many important ecosystem functions such as nutrient cycling, carbonate accretion and tridimensional complexity. Yet, reefs worldwide face an uncertain future, being threatened by local and global impacts. As an alternative approach to evaluate communities’ changes, functional ecology aims to understand how species shape the environment and how functions conduct ecosystems’ dynamics. The aim of this study was to investigate the temporal dynamics (2013–2019) of the reef benthic community in the most pristine reef in Brazil, Rocas Atoll, using a functional diversity approach. We identified 48 organisms grouped into 17 functional entities (according to their traits’ combination), considering all sampling years. Benthic community was temporally dominated by functional entities responsible for providing low reef tridimensional complexity (represented mainly by turf algae). This dominance reflected in low values of functional entropy, due to uneven abundances distribution between unique functional entities, those that have unique trait combination. Functional richness oscillated over years, but did not show great changes in functional spaces, maintaining an equity in the number of functional entities and indicating stability of reef functions in Rocas Atoll, even with unequal abundances’ distribution. Our study is the first to use a functional approach in temporal scale and represents a baseline for South Atlantic, since it provides the actual state of reef benthic communities using a functional approach, in an environment with no direct anthropic impacts. This can help to predict the effects on some ecosystem functions caused by local and global changes and its consequence for ecosystem services.
... For instance, longer video assessments often occur in herbivory assessment, varying from one to several hours (Fox & Bellwood, 2008;Rasher et al., 2013), whereas baited approaches reached between 30 and 60 min of video analysis (Bosch et al., 2017;Ebner et al., 2015;Langlois et al., 2010;Post et al., 2011). Shorter videos (c. 10 min) have been used to assess fish feeding pressure on the benthos in reefs and freshwater ecosystems (Canterle et al., 2020;Longo et al., 2014Longo et al., , 2015Longo et al., , 2019Miranda et al., 2018;Nunes et al., 2020), enabling large-scale understanding of trophic interactions based on a large number of replicates per sampling site Longo et al., 2019). The large variability in published sampling times and number of replicates indicates a possible trade-off between sampling shorter videos in more sites or sampling longer videos in fewer sites. ...
Remote underwater videos are widely employed to assess the structure and composition of reef fish assemblages but the sampling effort employed on each survey differs considerably, indicating that both the number of assessments and video length could be optimized. We searched for this optimal sampling effort in remote video samples to conduct rapid assessments of community composition and discussed the relation between number of replicates and video length, and how it impacts the method's efficiency to characterize species assemblages. We used remote video recordings from tropical reefs in Northeastern Brazil to investigate how fish species richness and composition builds across time and number of assays. Videos as short as 5 min successfully recorded richness, requiring about 5 repetitions to record most species that compose 80% of the total biomass. Recording species composition required even less time in these reefs, setting a minimum of 3 min with the same 5 videos. By comparing the detected richness per analyzed time unit, we found several shorter videos recorded more species than a few longer videos, indicating that increasing the sampling coverage in the reef area might be better than just extending video length for rapid assessments.
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... Thus, we assessed the frequency of bleaching and mortality of the coral Siderastrea stellata Verrill, 1868 at the Rocas Atoll from 2016 to 2019, and evaluated its relation with the 2015/2016 ENSO and other climatic events, such as MHW. Rocas is potentially one of the most "pristine" areas of the Southwest Atlantic, and figures as a natural laboratory to understand the effect of thermal stress on corals, since it is not directly exposed to other anthropogenic impacts, such as pollution, urbanization and fishing (Longo et al. 2015). ...
... During the low tide, two main habitats can be distinguished, open pools that constantly communicate with the exterior of the atoll and are more exposed to wave action than closed pools, which remain completely isolated from the exterior area of the atoll during low tides ( Figure 1b). The benthic community in Rocas is dominated by the abundant reef-building coral Siderastrea stellata (Echeverria et al. 1997, Longo et al. 2015. This species is highly tolerant to thermal stress and widely distributed and common on Brazilian coastal reefs (Leão et al. 2016, Garcia et al. 2017). ...
... A) Geographic location of the Rocas Atoll and B) Position of study sites, at the tide pools: Falsa Barreta, Cemitério, Salão, Tartarugas, and Âncoras. Adapted fromLongo et al. (2015) ...
Threatened by global warming and extreme climatic events, such as El Niño Southern Oscillation (ENSO) and Marine Heatwaves (MHW), coral reefs worldwide faced the worst bleaching and mortality event between 2014 and 2017, induced by the 2015/2016 ENSO. We evaluated the impacts of ENSO and MHW episodes on bleaching and mortality frequencies of Siderastrea stellata at Rocas Atoll, Southwestern Atlantic, using visual censuses conducted in 2016, 2017 and 2019. Bleaching rate varied significantly along the sampling period (11.71% in 2016, 1.52% in 2017, and 88% in 2019), but mortality was always less than 4%. Bleaching events in Atlantic reefs have been constantly associated with ENSO, until these recent events of the last two years. We suggest that MHW were probably the primary driver of the observed bleaching, especially in 2019, when much higher bleaching rates were observed than in ENSO periods. Although Southwestern Atlantic massive corals are considered more resistant to thermal stress than reefs corals worldwide, the strong events registered since 2019 highlight the need for continuous monitoring to better understand coral bleaching dynamics and improve predictions on the effects of global change in the region.
