RESUMO

Reef corals have been threatened by climate change, with more frequent and intense bleaching events leading to extensive coral mortality and loss of coral cover worldwide. In the face of this, the corals' photosymbiont assemblages have received special attention as a key to better understand the bleaching process and its recovery. To assess the effects of thermal anomalies, the coral Mussismilia harttii and the hydrocoral Millepora alcicornis were monitored through the El Niño 2015/2016 at a Southwestern Atlantic (SWA) coral reef. A severe bleaching event (57% of colonies bleached) was documented, triggered by a < 3 °C-week heatwave, but no mortality was detected. The hydrocoral was more susceptible than the scleractinian, displaying bleaching symptoms earlier and experiencing a longer and more intense bleaching event. The composition of photosymbionts in the M. alcicornis population was affected only at the rare biosphere level (< 5% relative abundance), with the emergence of new symbionts after bleaching. Conversely, a temporary dysbiosis was observed in the M. harttii population, with one of the dominant symbiodiniaceans decreasing in relative abundance at the peak of the bleaching, which negatively affected the total ß-diversity. After colonies' complete recovery, symbiodiniaceans' dominances returned to normal levels in both hosts. These results highlight critical differences in how the two coral species cope with bleaching and contribute to the understanding of the role of photosymbionts throughout the bleaching-recovery process.

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Abstract: 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.

Resumo: Ameaçados pelo aquecimento global e eventos climáticos extremos, como El Niño Oscilação Sul (ENSO) e Ondas de Calor Marinhas (MHW), os recifes de coral em todo o mundo enfrentaram o pior evento de branqueamento e mortalidade entre 2014 e 2017, induzido pelo ENSO 2015/2016. Nesse estudo, avaliamos os impactos dos episódios de ENSO e MHW nas frequências de branqueamento e mortalidade de Siderastrea stellata no Atol de Rocas, Atlântico Sudoeste, a partir de censos visuais realizados em 2016, 2017 e 2019. O branqueamento variou significativamente ao longo do período de amostragem (11,71% em 2016, 1,52% em 2017, e 88% em 2019), mas a mortalidade não, sendo sempre inferior a 4%. Eventos de branqueamento em recifes do Atlântico têm sido constantemente associados ao ENSO, até os eventos recentes dos últimos dois anos. Nós sugerimos que as MHW foram provavelmente o principal impulsionador do branqueamento observado, especialmente em 2019, quando as taxas de branqueamento observadas foram maiores do que nos períodos de ENSO. Embora os corais massivos do Atlântico Sudoeste sejam considerados mais resistentes ao estresse térmico quando comparados com corais recifais de outros oceanos, os fortes eventos registrados desde 2019 destacam a necessidade de monitoramento contínuo para entender melhor a dinâmica do branqueamento de corais e melhorar as previsões sobre os efeitos das mudanças globais na região.

RESUMO

Zooxanthellate corals live in symbiosis with phototrophic dinoflagellates of the family Symbiodiniaceae, enabling the host coral to dwell in shallow, nutrient-poor marine waters. The South Atlantic Ocean is characterized by low coral diversity with high levels of endemism. However, little is known about coral-dinoflagellate associations in the region. This study examined the diversity of Symbiodiniaceae associated with the scleractinian coral Favia gravida across its distributional range using the ITS-2 marker. This brooding coral endemic to the South Atlantic can be found across a wide range of latitudes and longitudes, including the Mid-Atlantic islands. Even though it occurs primarily in shallower environments, F. gravida is among the few coral species that live in habitats with extreme environmental conditions (high irradiance, temperature, and turbidity) such as very shallow tide pools. In the present study, we show that F. gravida exhibits some degree of flexibility in its symbiotic association with zooxanthellae across its range. F. gravida associates predominantly with Cladocopium C3 (ITS2 type Symbiodinium C3) but also with Symbiodinium A3, Symbiodinium linucheae (ITS2 type A4), Cladocopium C1, Cladocopium C130, and Fugacium F3. Symbiont diversity varied across biogeographic regions (Symbiodinium A3 and S. linucheae were found in the Tropical Eastern Atlantic, Cladocopium C1 in the Mid-Atlantic, and other subtypes in the Southwestern Atlantic) and was affected by local environmental conditions. In addition, Symbiodiniaceae diversity was highest in a southwestern Atlantic oceanic island (Rocas Atoll). Understanding the relationship between corals and their algal symbionts is critical in determining the factors that control the ecological niches of zooxanthellate corals and their symbionts, and identifying host-symbiont pairs that may be more resistant to environmental changes.

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The hologenome theory of evolution (HTE), which is under fierce debate, presupposes that parts of the microbiome are transmitted from one generation to the next [vertical transmission (VT)], which may also influence the evolution of the holobiont. Even though bacteria have previously been described in early life stages of corals, these early life stages (larvae) could have been inoculated in the water and not inside the parental colony (through gametes) carrying the parental microbiome. How Symbiodinium is transmitted to offspring is also not clear, as only one study has described this mechanism in spawners. All other studies refer to incubators. To explore the VT hypothesis and the key components being transferred, colonies of the broadcast spawner species Mussismilia hispida were kept in nurseries until spawning. Gamete bundles, larvae and adult corals were analyzed to identify their associated microbiota with respect to composition and location. Symbiodinium and bacteria were detected by sequencing in gametes and coral planula larvae. However, no cells were detected using microscopy at the gamete stage, which could be related to the absence of those cells inside the oocytes/dispersed in the mucus or to a low resolution of our approach. A preliminary survey of Symbiodinium diversity indicated that parental colonies harbored Symbiodinium clades B, C and G, whereas only clade B was found in oocytes and planula larvae [5 days after fertilization (a.f.)]. The core bacterial populations found in the bundles, planula larvae and parental colonies were identified as members of the genera Burkholderia, Pseudomonas, Acinetobacter, Ralstonia, Inquilinus and Bacillus, suggesting that these populations could be vertically transferred through the mucus. The collective data suggest that spawner corals, such as M. hispida, can transmit Symbiodinium cells and the bacterial core to their offspring by a coral gamete (and that this gamete, with its bacterial load, is released into the water), supporting the HTE. However, more data are required to indicate the stability of the transmitted populations to indicate whether the holobiont can be considered a unit of natural selection or a symbiotic assemblage of independently evolving organisms.