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Low coral mortality during the most intense bleaching event ever recorded in subtropical Southwestern Atlantic reefs

Authors:
Thomás Banha at University of São Paulo
Thomás Banha
Kátia Capel at Federal University of São Carlos
Kátia Capel
Marcelo Visentini Kitahara at University of São Paulo
Marcelo Visentini Kitahara
Ronaldo Bastos Francini-Filho at University of São Paulo
Ronaldo Bastos Francini-Filho
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Abstract and Figures

Coral reefs globally are threatened by climate change, but reef assemblages at high latitudes may serve as refugia. Marginal coral communities located in the subtropical Southwestern Atlantic are poorly studied, but were subject to an unprecedented heatwave and associated coral bleaching in 2019. Record values of 18.5 and 20.5 °C-weeks were registered for coastal and insular sites, which are the highest ever documented for a reef in the South Atlantic. As a consequence, approximately 80% and 20% of the population of the reef-building coral Mussismilia hispida (1116 colonies surveyed) underwent bleaching in coastal and insular sites, respectively. However, mortality (2%) was far lower than for episodes of similar magnitude in other regions, particularly in the Indo-Pacific. Therefore, the subtropical Southwestern Atlantic MCC displayed low mortality and remarkable tolerance when exposed to the most intense bleaching episode ever recorded for the region, reinforcing its potential as a refugium.
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NOTE
Low coral mortality during the most intense bleaching event ever
recorded in subtropical Southwestern Atlantic reefs
T. N. S. Banha
1
•K. C. C. Capel
2
•M. V. Kitahara
2,3
•R. B. Francini-Filho
4
•
C. L. B. Francini
5
•P. Y. G. Sumida
1,6
•M. Mies
1,6
Received: 28 May 2019 / Accepted: 29 August 2019 / Published online: 6 September 2019
ÓSpringer-Verlag GmbH Germany, part of Springer Nature 2019
Abstract Coral reefs globally are threatened by climate
change, but reef assemblages at high latitudes may serve as
refugia. Marginal coral communities located in the sub-
tropical Southwestern Atlantic are poorly studied, but were
subject to an unprecedented heatwave and associated coral
bleaching in 2019. Record values of 18.5 and 20.5 °C-
weeks were registered for coastal and insular sites, which
are the highest ever documented for a reef in the South
Atlantic. As a consequence, approximately 80% and 20%
of the population of the reef-building coral Mussismilia
hispida (1116 colonies surveyed) underwent bleaching in
coastal and insular sites, respectively. However, mortality
(2%) was far lower than for episodes of similar magnitude
in other regions, particularly in the Indo-Pacific. Therefore,
the subtropical Southwestern Atlantic MCC displayed low
mortality and remarkable tolerance when exposed to the
most intense bleaching episode ever recorded for the
region, reinforcing its potential as a refugium.
Keywords Climate change Degree heating weeks
Marginal Mussismilia Scleractinia Brazil
Introduction
Earth’s climate has been unequivocally warming, produc-
ing unprecedented changes in the atmosphere and the
ocean (IPCC 2013). Much of that energy is stored in the
upper ocean layers, which has led to an increase of 0.1 °C
in sea surface temperature per decade in the last century
(Levitus et al. 2005; IPCC 2013). Some marine ecosys-
tems, such as shallow-water coral reefs, are particularly
vulnerable and have been severely impacted by global
warming (Hughes et al. 2018). Its primary effect on coral
reefs is the disruption of the symbiotic relationships
between corals and dinoflagellates (zooxanthellae), in a
phenomenon known as coral bleaching (Glynn 1993).
Increased temperatures lead symbiotic dinoflagellates to
produce excessive reactive oxygen species, which prompts
the coral host to expel them (Lesser 2006). Because the
dinoflagellates are highly pigmented, their expulsion leaves
the white coral skeleton visible underneath the transparent
tissue (Glynn 1993). Due to the obligate nature of the
symbiotic relationship for the host, bleaching often leads to
coral death and, consequently, loss of habitat structural
complexity and biodiversity (Eakin et al. 2010; De’ath
et al. 2012; Hughes et al. 2018).
Although global warming is intensifying, marginal coral
communities (MCC) thrive under oceanographic
Topic Editor John A. Burt
&M. Mies
miguel.mies@usp.br
1
Instituto Oceanogra
´fico, Universidade de Sa
˜o Paulo, Prac¸a
Do Oceanogra
´fico, 191, Cidade Universita
´ria, Sa
˜o Paulo,
SP 05508-120, Brazil
2
Centro de Biologia Marinha, Universidade de Sa
˜o Paulo,
Rodovia Manuel Hypo
´lito Do Rego, km 131, 5,
Sa
˜o Sebastia
˜o, SP 11612-109, Brazil
3
Departamento de Cie
ˆncias Do Mar, Universidade Federal de
Sa
˜o Paulo, Rua Dr. Carvalho de Mendonc¸a, Santos,
SP 11070-100, Brazil
4
Departamento de Engenharia E Meio Ambiente,
Universidade Federal da Paraı
´ba, Rua da Mangueira, s/n,
Rio Tinto, PB 58297-000, Brazil
5
Instituto Laje Viva, Rua Joaquim Floriano, 466, Conj. 2207,
Sa
˜o Paulo, SP 04534-002, Brazil
6
Instituto Coral Vivo, Rua Dos Coqueiros, 87,
Santa Cruz Cabra
´lia, BA 45807-000, Brazil
123
Coral Reefs (2020) 39:515–521
https://doi.org/10.1007/s00338-019-01856-y
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Until then, most bleaching reports were limited to snapshot assessments in Bahia State and the Abrolhos Bank Ferreira et al. 2013;Kelmo and Attrill 2013;Steiner et al. 2015), with a complete absence of data for the western coast of Africa. During the regional-scale bleaching event of 2019-20, there was a significant increase in the volume of information and reports for the South Atlantic (Banha et al. 2020;Duarte et al. 2020;Ferreira et al. 2021;Gaspar et al. 2021;Godoy et al. 2021;Braz et al. 2022;Corazza et al. 2024). Nonetheless, due to insufficient and inconsistent monitoring on both spatial and temporal scales, the thermal stress and potential bleaching experienced in the South Atlantic before 2015 remain largely unknown. ...
... Nonetheless, in general, coral mortality in the South Atlantic is expected to be lower than in other regions. Although highly context-dependent, while 3.8°C-weeks caused 26% mortality in the Caribbean (Belize) and 13°C-weeks led to 80% mortality in the Indo-Pacific (Scott Reef, Australia), a stress level of 20°C-weeks resulted in < 2% mortality in Ubatuba reefs in the South Atlantic (Eakin et al. 2010;Gilmour et al. 2013;Banha et al. 2020). Therefore, bleaching in the South Atlantic may have caused lower mortality than anticipated, but this remains unassessed. ...
... The Northeast, found at lower latitudes, has experienced unprecedented thermal stress and bleaching over the past 10 years, possibly facing the highest levels of coral mortality across the South Atlantic (Pereira et al. 2022). The South has endured some of the most intense heatwaves in recent years; however, despite elevated documented bleaching, little mortality has been detected at sites dominated by Mussismilia hispida, an endemic and thermallytolerant coral species (Mies et al. 2018;Banha et al. 2020). Additionally, these are higher-latitude reefs, which may benefit from increased resilience provided by high-frequency thermal variability (Oliver and Palumbi 2011;Grottoli et al. 2014 The duration of thermal stress episodes is also increasing in the South Atlantic. ...
The Thermal Stress History of South Atlantic Reefs Reveals Increasing Intensity, Duration, Frequency, and Likely Undocumented Bleaching Episodes
Article
  • Apr 2025
  • GLOBAL CHANGE BIOL
The primary consequence of global warming for reefs is coral bleaching, often leading to extensive coral mortality. Although bleaching is well‐documented globally, the thermal stress and bleaching experienced by the unique South Atlantic reefs remain largely unknown due to insufficient monitoring on both spatial and temporal scales. Therefore, this work aimed to reconstruct past thermal stress episodes across South Atlantic reefs, and assessed whether episodes are becoming more intense, longer‐lasting, and more frequent. We retrieved daily 5 km‐resolution Degree Heating Week (DHW) data from the U.S. National Oceanic and Atmospheric Administration Coral Reef Watch server for 33 reef sites spanning the last 40 years. For each thermal stress episode, we assessed the intensity (maximum DHW value), duration (number of continuous days under stress), and frequency (number of days between episodes). Generalized linear models were fitted to intensity, duration, and frequency data to evaluate the influence of latitude and the time x region interaction as predictors. We recorded multiple thermal stress episodes, increasing from 2010 onwards, ranging from 10 episodes between 1985–89 and 75 between 2020–24. Intensity and duration increased over time across the entire South Atlantic. Frequency also increased across the Southwestern Atlantic coast and oceanic islands, but not for Africa. Episodes at higher latitudes were more intense, prolonged, and frequent. The validity of the thermal stress history reconstruction was groundtruthed using information from the Abrolhos Bank, the only consistently monitored reef site in the South Atlantic—DHW data accurately matched the observed bleaching episodes at this site. With this, our dataset shows that multiple bleaching episodes likely occurred in the South Atlantic, but went undocumented in the field. Therefore, the information currently available for the South Atlantic likely underestimates the extent of bleaching occurring in the area, which is experiencing increases in intensity, duration, and frequency of thermal stress.
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... Due to the successive marine heat waves (MHW) recorded in the last decade, severe global-scale bleaching events have been documented, particularly affecting reefs in the Caribbean and Pacific (Muñiz-Castillo et al. 2019;Bove, Mudge, and Bruno 2022;Eakin et al. 2022;Smith et al. 2024). Although Brazilian scleractinian corals have historically exhibited lower mortality of dominant species after bleaching events compared to corals from other regions (Mies et al. 2020;Banha et al. 2020), emerging scientific evidences show that these marginal reefs have also been experiencing severe impacts as MHWs become more frequent and intense (Teixeira et al. 2019;Duarte et al. 2020;Ferreira et al. 2021;Soares et al. 2021;Braz et al. 2022;Pereira et al. 2022;Corazza et al. 2024). ...
... In 2019, an unprecedented MHW was recorded in the subtropical southwestern Atlantic (SWA), with degree heating weeks (DHW) reaching up to 20.5°C-weeks, resulting in the most severe coral bleaching event ever reported in this region (Banha et al. 2020). Among the affected areas was the Alcatrazes Archipelago Wildlife Refuge (IUCN Category III), located at the 24° S latitude. ...
... Among the affected areas was the Alcatrazes Archipelago Wildlife Refuge (IUCN Category III), located at the 24° S latitude. Despite the severity of the thermal anomaly, there was an overall low mortality and relatively low proportion of bleached colonies of Mussismilia hispida in the Alcatrazes Archipelago compared to other adjacent coastal areas (Banha et al. 2020). In their study, Banha et al. (2020) concluded that, despite their susceptibility to bleaching, corals from the SWA exhibit remarkable tolerance to heat stress, reinforcing the potential of SWA reefs as a long-term climate refugia, a concept proposed by Mies et al. (2020). ...
Scleractinian Corals at Their Subtropical SouthwesternAtlantic Limit: Post-2019 Mass Bleaching Event Analysis
Article
  • Dec 2024
  • AQUAT CONSERV
Thermal anomalies caused by climate change have emerged as a major threat to reef ecosystems globally. While the effects ofwarming oceans have been extensively investigated in tropical reefs, its effects on subtropical reefs, where coral diversity islower, remain largely unstudied. We analysed the spatial distribution, mean cover and health status of scleractinian corals in thesubtropical rocky reefs of the Alcatrazes Archipelago, a no-take marine protected area located 30 km off the coast of São Paulostate, Brazil (24° S). Data were collected before (2018) and after (2022) the most intense marine heatwave ever recorded in the re-gion, in 2019, using either fixed or random photoquadrats. Five scleractinian corals were recorded as follows: The zooxanthellatemassive species Mussismilia hispida and Madracis decactis, the azooxanthellate solitary corals Astrangia spp. and Coenocyathussebroecki and the invasive sun coral Tubastraea spp. M. hispida and M. decactis were the most abundant species, particularly inthe sheltered sites, while Astrangia spp. and C. sebroecki were less abundant and only recorded in the exposed side of the island.In the single site where Tubastraea spp. colonies prevailed, other coral species were nearly absent. Both M. hispida and M. decac-tis exhibited resilience to the 2019's bleaching event, with their abundance remaining almost the same in 2022. Our findings addevidences to the emerging idea that subtropical reefs in the southwestern Atlantic may serve as refuges during future thermalanomalies, highlighting the importance of monitoring these reefs in the context of changing habitats driven by warming oceans.
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... In contrast to other parts of the global ocean, no episode of mass mortality was ever spotted for SW Atlantic corals until a major heatwave event in 2019 (Duarte 2020). Previous studies have addressed how historical records in heat stress levels (e.g., DHW ≥ 20 • C week) were followed by surprisingly no coral mortality in major coral populations (Banha et al. 2020). Extensive coral monitoring during 1998-2005 showed that SST anomalies were responsible for only 30% of bleaching events on eastern Brazilian coral reefs (Leão et al. 2010). ...
... It seems that coral bleaching in the region has historically been driven by a much more complex process, involving a wider range of variables than just SST-induced bleaching. Previous studies have already addressed the historical resilience of these reefs to heat-induced mortality (Mies et al. 2020;Banha et al. 2020). It is possible that the majority of reported bleaching events, that were not anticipated by an increase in local SST conditions, may have been caused by a combination of factors such as: (i) delayed effects of previous heat stress events (Walker et al. 2023), (ii) other environmental factors and diseases (Anthony et al. 2007), (iii) low temperatureinduced bleaching (Hoegh-Guldberg and Fine 2004). ...
Thirty years of coral bleaching in the Southwestern Atlantic Ocean: a historical assessment based on degree heating week indices
Article
Full-text available
  • Apr 2025
  • CORAL REEFS
Three decades have passed since the first documented coral bleaching event in the Southwestern Atlantic Ocean. Rising sea surface temperatures continue to threaten coral conservation. Due to particular characteristics of Southwestern Atlantic coral communities, the influence of heat stress on bleaching events remains a challenge. Here, we review reports of coral bleaching over the past 30 yrs and their relationship to sea surface temperature anomalies. Coral bleaching reports were compiled from 1992 to 2022 and compared with bleaching predictions based on degree heating week (DHW) indices. Our results indicate that about 15% of the analyzed bleaching events were reported during periods of high DHW conditions. In contrast, 80% of these events occurred after 2010, coinciding with an average increase of 3 ∘^{\circ } ∘ C week in DHW values. These results support the expected increase in the influence of heat stress as one of the main causes of coral bleaching in recent years. In addition to a potential bias in bleaching reporting, corals near the coast between 3 ∘^{\circ } ∘ S–9 ∘^{\circ } ∘ S and 15 ∘^{\circ } ∘ S–18 ∘^{\circ } ∘ S appear to be historically most affected by heat stress events. Although no clear improvement in bleaching prediction performance was found by incorporating local SST variability into the DHW calculation, we suggest that extensive monitoring efforts could lead to a better understanding of this relationship under future climate change scenarios.
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... Corals in the western tropical and South Atlantic, for instance, tend to be less susceptible to bleaching with low mortality and have suffered from 50% to 60% fewer mass bleaching events in comparison to the Indo-Pacific and the Caribbean 18 . Even though coral bleaching has been recorded recently in the tropical and subtropical South Atlantic [19][20][21][22][23] , there is relatively low mortality of dominant species when compared to bleaching events in the Indo-Pacific and the Caribbean 24 , with only more significant mortality occurring in branching hydrocorals (Millepora alcicornis) and the endemic coral (Mussismilia hartti) in the tropical Atlantic 19,22,23 . Projections indicate that the western side of the tropical Atlantic will be the most vulnerable area for bleaching 25 , threatening the most diverse reefs in the tropical Atlantic, such as the Abrolhos Bank reefs at 17°S 25 . ...
The severe 2020 coral bleaching event in the tropical Atlantic linked to marine heatwaves
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Full-text available
  • Mar 2025
Marine heatwaves can amplify the vulnerabilities of regional marine ecosystems and jeopardise local economies and food resources. Here, we show that marine heatwaves in the tropical Atlantic have increased in frequency, intensity, duration, and spatial extent. Marine heatwaves are 5.1 times more frequent and 4.7 times more intense since the records started in 1982, with the 10 most extreme summers/falls in terms of marine heatwave cumulative intensity and spatial extension occurring in the last two decades. The extreme warming during the summer/fall of 2020 led to the largest bleaching event recorded along the Brazilian coast, with 85% of stony corals and 70% of zoanthids areas bleached in Rio do Fogo. The increase in the severity of the marine heatwaves in the western tropical Atlantic is not accompanied by trends in the strength of the local drivers. This suggests that weaker forcing can lead to more devastating marine heatwaves as the global ocean temperature rises due to climate change.
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... Up until the 2019 heatwave, bleaching-related coral mortality had been relatively low in the region and was largely associated with fast-growing hydrocorals (Millepora spp.) and the scleractinian coral Mussismilia harttii, the region's only branching forms (Teixeira et al. 2021;Duarte et al. 2020;Soares et al. 2021). However, the physiological stress and tissue mortality recorded herein spans the two most abundant massive corals and challenges the idea that SWA turbid-zone reefs are climate change refugia Banha et al. 2020). Besides exploring potential relationships between morphology and health, and how site and habitat influenced ...
Nowhere to hide: massive corals’ mortality after cumulative heat stress in a putative climate change refugium
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Full-text available
  • Dec 2024
  • CORAL REEFS
Coral reefs worldwide are under severe threat due to a combination of local stressors and escalating intensity and frequency of heatwaves, which lead to mass coral bleaching. Although turbid-zone reefs have been considered climate change refugia, their long-term responses to heatwaves remain poorly assessed. Additionally, the relationship between morphological variation and bleaching resistance within massive corals that often dominate turbid zones remains unclear. To address these two gaps, we conducted line-transect surveys during the 2016 and 2019 mass bleaching events (peak DHW 10.9 and 19.7 °C-weeks, respectively), estimated Symbiodiniaceae densities, and fate-tracked 79 colonies of the two massive coral species in Southwestern Atlantic’s largest turbid-zone reefs using 3D photogrammetry and pulse-amplified modulated fluorometry. Fate-track sampling was performed 5 months before, during, and 5 and 24 months after the 2019 event. We found no association between morphology (colony sphericity and polyp area) and tissue mortality, either between or within species. Coral tissue area continued to decline for up to two years after the heatwave, challenging the Brazilian climate change refugia hypothesis and emphasizing the need for long-term monitoring to fully understand the consequences of bleaching events. Notably, tissue mortality was unrelated to bleaching prevalence, suggesting that the phased recovery of photophysiological parameters may be decoupled from longer-term coral health and survival. Recommendations to policy-makers and managers include prioritizing climate change mitigation and improving monitoring programs.
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The Southwestern Atlantic coral Mussismilia hispida exhibit remarkable tolerance to nitrate enrichment
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Spatial and temporal patterns of mass bleaching of corals in the Anthropocene
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  • Jan 2018
  • SCIENCE
Tropical reef systems are transitioning to a new era in which the interval between recurrent bouts of coral bleaching is too short for a full recovery of mature assemblages. We analyzed bleaching records at 100 globally distributed reef locations from 1980 to 2016. The median return time between pairs of severe bleaching events has diminished steadily since 1980 and is now only 6 years. As global warming has progressed, tropical sea surface temperatures are warmer now during current La Niña conditions than they were during El Niño events three decades ago. Consequently, as we transition to the Anthropocene, coral bleaching is occurring more frequently in all El Niño–Southern Oscillation phases, increasing the likelihood of annual bleaching in the coming decades.
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Environmental forcing on phytoplankton biomass and primary productivity of the coastal ecosystem in Ubatuba region, southern Brazil
Article
Full-text available
  • Jan 1999
A time series of chlorophyll a and in situ primary production sampled over a period of 33 days during summer in Ubatuba region, southeastem Brazil, was subjected to multivariate and harmonic analysis. Principal Component Analysis has revealed four factors interpreted as (i) South Atlantic Central Water forcing; (ii) Transient ftontal systems and rain fali forcings; (iii) Wind forcing normal to the coast; (iv) Wind forcing parallel to the coast, as main factors in the variability of the phytoplankton biomass and primary productivity. Splitting of the time series according to four main events which had profound effects on the physicochemical characteristics of the region showed the following variations in the primary productivity integrated over the photic layer (g C m-2 day-1): mixing→stratification period, 0.40 ± 0.11; heavy rainfall, 1.24± 0.28; stratification after rainfall, 0.74± 0.10; stratification→mixing period, 0.90± 0.27; stratification after deep mixing, 0.63 ± 0.28. Harmonic analysis revealed two indistinguishable significant peaks of the phytoplankton biomass - one at a period of 8.25 days and one at a period of 6.6 days, contributing, respectively, about 17 and 32% ofthe total variance. Atmospheric forcing showed a characteristic period,of 200-264 hours while phytoplankton biomass response ranged over the 144-192 hours time scales and primary productivity was best related to the environment 360 hours before. Relative to total nitrogen' and ' biomass primary productivity oscillations were lagged about 96-144 hours. The interruption of steady-state conditions by transient atmospheric ev~nts and wind field intensification are the determining factors driving phytoplankton changes in this coastal environment.
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Validation of degree heating weeks as a coral bleaching index in the northwestern Pacific
Article
  • Nov 2016
Mass bleaching is the most significant threat to coral reefs. The United States National Oceanic and Atmospheric Administration monitors world sea surface temperature (SST) and releases warnings for bleaching based on degree heating weeks (DHW), which is the accumulation of temperature anomalies exceeding the monthly maximum mean SST for a given region. DHW values >4.0 °C-weeks are thought to induce bleaching, and those >8.0 °C-weeks are thought to result in widespread bleaching and some mortality. This study validates the effectiveness of DHW as a mass bleaching index by on-site historical observation at eight sites in the northwestern Pacific Ocean. The mass bleaching events occurred during different years at different sites. The recorded years of the bleaching events matched well with DHW values >8 °C-weeks, and the logistically projected probability of bleaching against DHW showed a positive relationship. DHW provides a reasonable threshold for bleaching.
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