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The island continent of Madagascar spans nearly 13.5o of latitude in the SW Indian Ocean. Its coastline includes a number of well developed coral reefs, ranging from tropical Nosy Bé (NW Madagascar, 12oS) and Vohemar (Volhmarina, NE Madagascar, 13oS) to subtropical Tuléar (Toliara , SW Madagascar, 23.5oS), as well as temperate coral communities at Fort Dauphin (Tolagnaro, SE Madagascar, 25oS). Given the range of environmental conditions experienced by reef corals at these different sites, Madagascar represents an ideal location to study the distribution of algal symbionts (Symbiodinium spp.) in these coral hosts. To investigate the effect of latitudinal gradients in temperature on Symbiodinium distributions, 220 samples from 27 coral genera in 12 families were collected from these 4 sites in September 2001. To test the stability of these distributions over time, a further 337 samples were collected from the Nosy Bé and Tuléar regions in March 2007 and November 2009. Symbiodinium communities were screened using Denaturing Gradient Gel Electrophoresis (DGGE) to analyze the internal transcribed spacer-2 (ITS-2) region of Symbiodinium ribosomal DNA, with individual symbiont taxa identified by sequencing individual DGGE bands. Significant differences were found in the Symbiodinium cladal composition of reef corals at different sites, with corals at northern sites containing a higher relative frequency of Symbiodinium in clade D (occurring as mixed clade C+D communities) than southern sampling sites. Nominal logistic analysis of the distribution of symbionts found a significant effect of coral taxa and site, but not of sea surface temperature metrics (environmental data obtained from NOAA’s Coral Reef Watch satellite-derived data) in determining the distribution of different symbionts. Rarefaction analysis indicated there were no differences in Symbiodinium richness (at either the clade or the subtype level) between different sites, or between different sampling intervals. Differences existed in the subcladal composition of dominant ITS-2 types found in congeners at different latitudes, with corals in the genus Acropora being dominated by Symbiodinium C3 (specifically subtype C3z) in northern sites, and C1 in southern sites. Symbiont communities changed between 2001 and 2007/2009, with increases in mixed Symbiodinium C+D assemblages occurring at southern sites that had experienced temperature stress during the intervening period. Decreases in mixed Symbiodinium communities occurred at northern sites, which were not as severely affected by thermal stress. It is suggested that the latitudinal gradients in Symbiodinium found in Madagascar, and the environmental controls on community structure described here, provide important insight into how coral species in this understudied area can adapt or acclimatize to changing environmental conditions through shifts in the composition of their symbiont communities. This will help improve our understanding of how projected climate change in the SW Indian Ocean will affect survival trajectories for coral reefs in the region.

Zooxanthellae are very important for the coral reef ecosystem. The diversity of coral hosts is high in the Indo-Pacific, but the diversity of zooxanthellae has not been broadly investigated. Southern Taiwan and Penghu Islands are coral reef and non-reefal communities, respectively. These localities were chosen as the sampling sites for this study to maximize the opportunity of surveying this region in the Indo-Pacific. Zooxanthellae diversity was investigated in 40 host species including 32 species of Scleractinia, 4 species of Actiniaria, 3 species of Milleporina and 1 species of Helioporacea using polymerase chain reaction (PCR) of the ssrRNA gene and restriction fragment length polymorphism (RFLP) patterns. The phylogenetic relationship of partial and complete sequences of the ssrRNA gene were also analysed. Aiptasia puchella harbors clade B; Oulastrea crispata only harbors clade E; while Acropora palifera and Montipora cactus harbor both clades C and E. Zooxanthellae isolated from all except the above 4 host species are identified as "clade C" sensu Rowan and Powers (1991a). Therefore, the clade C is the dominant type in the Indo-Pacific. Phylogenetic analyses based on partial and complete sequences obtained in this study and also from the GenBank data base demonstrate 4 clades (A, B, C and E) in the genus Symbiodinium. Clade E, classed as D3 RFLP type in previous studies, is a distinct clade differing from A, B and C by RFLP and sequencing data. Clade E has only been found in Scleractinia host species collected in shallow-water habitats in the Pacific. The composition of zooxanthellae clades and ecological pattern of polymorphic symbiosis is not consistent with the irradiance adaptation hypothesis in the Caribbean. A literature survey of zooxanthellae in Scleractinian hosts indicates a significant difference between the Caribbean and the Pacific. The documented biogeography of zooxanthellae clades and the ecological pattern of polymorphic symbiosis are also differ between the Caribbean and the Indo-Pacific.

Corals reefs worldwide are facing many challenges due to global warming. Of these challenges, increasing sea temperatures represent a major threat. An increase of 1 °C above summer mean levels is greatly associated with coral bleaching, and massive coral bleaching is observed when accumulation of thermal-stress reaches 4 °C-weeks according to Degree Heating Weeks (DHW) measurements. The coral holobiont is an assemblage of many organisms including Symbiodiniaceae; a family of photosynthetic microalgae that form an endosymbiotic relationship with corals. Studies suggest that Symbiodiniaceae may drive the performance of the host, therefore, resilience of the coral host against thermal stress may be largely influenced by Symbiodiniaceae. The aim of this study was to compare the physiological performance under acute heat and light-stress conditions of several Symbiodiniaceae strains (clade A and B) isolated from different geographical locations with distinct thermal profiles (Red Sea, Hawaii, and North Carolina). Oxygen production, respiration rate, photosynthetic efficiency, and production of ROS were measured under conditions of acute heat and light-stress. The Red Sea strains (RS-B*, RS-B, and RS-A) exhibited a higher photosynthetic efficiency with increasing temperatures than the Hawaii and North Carolina strains (SSBO1, SSAO1, respectively). After heat-stress of 34 °C, RS-A was found to have the best thermotolerance with regard to ROS production. Oxygen production and respiration rate data showed high biological variation between culture replicates which prevented inter-strain comparisons and limited observation of consistent trends. The observed variability was largely due to the differential age of the cultures used, and the inability of the cell counting method to differentiate between live and dead cells. The results of this study indicate that Symbiodiniaceae strains originating from warmer geographic locations exhibit an overall better performance under acute heat-stress conditions. Variability in the physiological response of three samples from the same species (Breviolum minutum) exemplifies the large diversity in the family Symbiodiniaceae, and indicates the need to support genomic identification of Symbiodiniaceae isolates with physiological studies. Efforts to predict the future of coral reefs under current threats of climate change will only be productive if we have a comprehensive understanding of the complex interactions between corals and Symbiodiniaceae.

Os recifes de coral estão entre os ambientes marinhos mais produtivos e ricos em biodiversidade. Esta biodiversidade está em parte associada a complexas estruturas formadas por corais escleractíneos. Apesar da importância ecológica, social e econômica dos recifes de corais, eles são expostos a várias ameaças relacionadas às atividades humanas. Dentre os impactos antrópicos em recifes, o branqueamento, ou perda de zooxantelas, é o mais notável e é diretamente relacionado à mortalidade dos corais. Por possuírem uma associação simbiótica com essas zooxantelas, alguns corais escleractíneos são considerados mixotróficos, caracterizados por modos de alimentação autotrófico (através de simbiose com o dinoflagelado Symbiodinium) e heterotrófico (predação sobre zooplâncton). Alguns estudos comprovam que corais com maior capacidade de alimentação heterotrófica são mais resistentes ao branqueamento e, consequentemente, às alterações climáticas. A fim de analisar se o coral escleractíneo Mussismilia hispida, é capaz de alternar seu modo nutricional entre predominante autotrófico e predominante heterotróficos, dezoito colônias foram amostradas ao longo de um ano. Marcadores Tróficos de Ácidos Graxos (FATM, na sigla em inglês) foram utilizados para determinar a fonte nutricional de carbono em tecido de corais. A concentração de células de Symbiodinium e a temperatura local também foram avaliadas. Branqueamento foi observado nos meses mais quentes do ano, quando a concentração de Symbiodinium diminuiu, voltando a aumentar nos meses mais frios. O marcador para dieta heterotrófica CGA (C20: 1ω9) foi encontrado em amostras de zooplâncton de toda a área de estudo. Em laboratório, colônias sem acesso a zooplâncton apresentaram perda significativa deste marcador após 10 dias. Amostras de colônias naturalmente branqueadas não apresentaram nenhum vestígio dos marcadores de autotrofia SDA (18: 4ω3) e DPA (22: 5ω3), mas continham tanto CGA e DHA (22: 6ω3). Isso confirmou que SDA e DPA são marcadores autotróficos viáveis e CGA é um marcador de heterotrofia. FATM relacionados com autotrofia apresentaram padrão semelhante ao observado para as concentrações de Symbiodinium e foram positivamente correlacionados com a densidade numérica de simbiontes e negativamente com a temperatura. Para explorar os dados de concentração dos FATM, o Índice Trófico de Corais foi desenvolvido para exibir as alternâncias entre modos nutricionais. Mussismilia hispida de fato alterna entre predominância de modo nutritivo ao longo do ano, sendo mais heterotrófica em períodos mais quentes e em condições climáticas adversas, porem na maior parte do ano é predominantemente autotrófica. A validação dos ácidos graxos marcadores tróficos específicos como referência para autotrofia e heterotrofia em corais abre perspectivas para novos estudos em ecologia trófica bêntica em recifes de coral. Este trabalho também inclui o primeiro monitoramento de um ano do comportamento alimentar em um coral hermatípico no Atlântico Sul e o acompanhamento de um evento de branqueamento. / Coral reefs are among the most productive and biodiverse marine environments. This remarkable biodiversity is partly associated to the complex structures formed by scleractinian corals. Despite the ecological, social and economic importance of coral reefs, they are constantly exposed to several threats mainly related to human activities. Climate changes are one of the most notable impacts of human activity related to coral mortality, mainly due to coral bleaching. Some scleractinian corals are proved to be mixotrophs, displaying both autotrophic (through Symbiodinium) and heterotrophic (predation on zooplankton) nutrition modes. Many studies emphasize that corals with greater capability of heterotrophic feeding are more resilient to bleaching and consequently to climate change. In order to analyze whether the endemic scleractinian coral Mussismilia hispida is capable of shifting from predominant autotrophic and predominant heterotrophic in Ubatuba-SP, 18 colonies were sampled monthly for 12 months. The Fatty Acid Trophic Markers (FATM) approach was used to determine the source of carbon on coral tissues. Symbiodinium cell density and local seawater temperature were also assessed. A mild bleaching was observed showing a decrease in Symbiodinium numerical density during warmer months, but increasing in colder months. Reference samples validated the relation between all selected FATM and its corresponding nutritional mode. The heterotrophic feeding marker CGA (C20:1ω9) was found in zooplankton samples collected throughout the study area. Laboratory starved colonies (no access to zooplankton) lost any trace of this marker after 10. Samples from naturally bleached colonies presented no traces of the autotrophic feeding markers SDA (18:4ω3) and DPA (22:5ω3), but contained both CGA (C20:1ω9) and DHA (22:6ω3). These results confirmed that the FATM analyzed where reliable trophic markers. Autotrophic FATM presented a pattern similar to that observed for Symbiodinium concentration in M. hispida tissues and were positively correlated with the symbiont and negatively with temperature. The Coral Trophic Index showed that M. hispida undergoes shifts in nutritional modes along the year, being more heterotrophic in adverse conditions. The validation of specific FATM as proxies for autotrophic and heterotrophic feeding in corals opens new perspectives for further studies in benthic trophic ecology in coral reefs. This work also presents the first yearlong monitoring of the feeding behavior in a hermatypic coral in the South Atlantic and the monitoring of a mild bleaching event.

Os recifes de coral estão entre os ambientes marinhos mais produtivos e ricos em biodiversidade. Esta biodiversidade está em parte associada a complexas estruturas formadas por corais escleractíneos. Apesar da importância ecológica, social e econômica dos recifes de corais, eles são expostos a várias ameaças relacionadas às atividades humanas. Dentre os impactos antrópicos em recifes, o branqueamento, ou perda de zooxantelas, é o mais notável e é diretamente relacionado à mortalidade dos corais. Por possuírem uma associação simbiótica com essas zooxantelas, alguns corais escleractíneos são considerados mixotróficos, caracterizados por modos de alimentação autotrófico (através de simbiose com o dinoflagelado Symbiodinium) e heterotrófico (predação sobre zooplâncton). Alguns estudos comprovam que corais com maior capacidade de alimentação heterotrófica são mais resistentes ao branqueamento e, consequentemente, às alterações climáticas. A fim de analisar se o coral escleractíneo Mussismilia hispida, é capaz de alternar seu modo nutricional entre predominante autotrófico e predominante heterotróficos, dezoito colônias foram amostradas ao longo de um ano. Marcadores Tróficos de Ácidos Graxos (FATM, na sigla em inglês) foram utilizados para determinar a fonte nutricional de carbono em tecido de corais. A concentração de células de Symbiodinium e a temperatura local também foram avaliadas. Branqueamento foi observado nos meses mais quentes do ano, quando a concentração de Symbiodinium diminuiu, voltando a aumentar nos meses mais frios. O marcador para dieta heterotrófica CGA (C20: 1ω9) foi encontrado em amostras de zooplâncton de toda a área de estudo. Em laboratório, colônias sem acesso a zooplâncton apresentaram perda significativa deste marcador após 10 dias. Amostras de colônias naturalmente branqueadas não apresentaram nenhum vestígio dos marcadores de autotrofia SDA (18: 4ω3) e DPA (22: 5ω3), mas continham tanto CGA e DHA (22: 6ω3). Isso confirmou que SDA e DPA são marcadores autotróficos viáveis e CGA é um marcador de heterotrofia. FATM relacionados com autotrofia apresentaram padrão semelhante ao observado para as concentrações de Symbiodinium e foram positivamente correlacionados com a densidade numérica de simbiontes e negativamente com a temperatura. Para explorar os dados de concentração dos FATM, o Índice Trófico de Corais foi desenvolvido para exibir as alternâncias entre modos nutricionais. Mussismilia hispida de fato alterna entre predominância de modo nutritivo ao longo do ano, sendo mais heterotrófica em períodos mais quentes e em condições climáticas adversas, porem na maior parte do ano é predominantemente autotrófica. A validação dos ácidos graxos marcadores tróficos específicos como referência para autotrofia e heterotrofia em corais abre perspectivas para novos estudos em ecologia trófica bêntica em recifes de coral. Este trabalho também inclui o primeiro monitoramento de um ano do comportamento alimentar em um coral hermatípico no Atlântico Sul e o acompanhamento de um evento de branqueamento. / Coral reefs are among the most productive and biodiverse marine environments. This remarkable biodiversity is partly associated to the complex structures formed by scleractinian corals. Despite the ecological, social and economic importance of coral reefs, they are constantly exposed to several threats mainly related to human activities. Climate changes are one of the most notable impacts of human activity related to coral mortality, mainly due to coral bleaching. Some scleractinian corals are proved to be mixotrophs, displaying both autotrophic (through Symbiodinium) and heterotrophic (predation on zooplankton) nutrition modes. Many studies emphasize that corals with greater capability of heterotrophic feeding are more resilient to bleaching and consequently to climate change. In order to analyze whether the endemic scleractinian coral Mussismilia hispida is capable of shifting from predominant autotrophic and predominant heterotrophic in Ubatuba-SP, 18 colonies were sampled monthly for 12 months. The Fatty Acid Trophic Markers (FATM) approach was used to determine the source of carbon on coral tissues. Symbiodinium cell density and local seawater temperature were also assessed. A mild bleaching was observed showing a decrease in Symbiodinium numerical density during warmer months, but increasing in colder months. Reference samples validated the relation between all selected FATM and its corresponding nutritional mode. The heterotrophic feeding marker CGA (C20:1ω9) was found in zooplankton samples collected throughout the study area. Laboratory starved colonies (no access to zooplankton) lost any trace of this marker after 10. Samples from naturally bleached colonies presented no traces of the autotrophic feeding markers SDA (18:4ω3) and DPA (22:5ω3), but contained both CGA (C20:1ω9) and DHA (22:6ω3). These results confirmed that the FATM analyzed where reliable trophic markers. Autotrophic FATM presented a pattern similar to that observed for Symbiodinium concentration in M. hispida tissues and were positively correlated with the symbiont and negatively with temperature. The Coral Trophic Index showed that M. hispida undergoes shifts in nutritional modes along the year, being more heterotrophic in adverse conditions. The validation of specific FATM as proxies for autotrophic and heterotrophic feeding in corals opens new perspectives for further studies in benthic trophic ecology in coral reefs. This work also presents the first yearlong monitoring of the feeding behavior in a hermatypic coral in the South Atlantic and the monitoring of a mild bleaching event.

Coral reef environments have been degrading steadily over the last few decades. It is generally accepted now that coral reefs are one of the first marine ecosystems to show measurable perturbations driven by global warming. Some of theses perturbations are consequence of extreme stochastic disturbances like hurricanes or extreme thermal anomalies and therefore, can be easily identified using broad indicators like coral cover. These indicators are easy to measure and provide a general description of the system in question. The detection and interpretation of more subtle perturbation in coral communities is more complicated, both logistically and conceptually. However, detecting chronic perturbations at an early stage can increase significantly the success of early mitigating management strategies. This thesis focuses on the development and application of highly sensitive indicators that can detect subtle perturbations in coral communities. It also studies the ecological interpretation of mild perturbations and their effect on the future structure of coral reef environments. The mild thermal disturbance experienced by the Heron Island reef in the south of the Great Barrier Reef during the 2005-2006 summer, and an environmental gradient along the central coast of Venezuela (south Caribbean Sea), were used as models to test the sensitivity of coral reefs to mild disturbances at different organisation levels (organism, population, and community). At the organismal level my results showed that the intensity of bleaching that a colony shows during a mild thermal disturbance is affected by the morphology of the colony as well as the substrates surrounding the colony. Colonies surrounded by sand bleached more than colonies surrounded by dead coral or rubble. I propose that reef specific information on the relative cover of sand, rubble, and dead coral can improve the fine scale accuracy of bleaching predicting models. Studying the same mild thermal disturbance at Heron Island, I showed how demographic parameters of some populations are more sensitive to mild thermal disturbances than coral cover (the most widely used response variable in coral monitoring programs around the world). Furthermore, my results suggest that the response of coral populations to mild thermal disturbance is different in nature and intensity to the respond observed during extreme thermal disturbances. Some taxa like Stylophora pistillata, are highly sensitive to extreme thermal disturbances, and tend to be the first to die under these conditions. In contrast, this taxon was extremely tolerant to the mild thermal disturbance of early 2006 in comparison to other taxa identified previously as more tolerant than S. pistillata. This difference in the response of coral environments to milder more common disturbances can have great influence in the trajectory that coral reefs follow in a rapidly changing world. Finally at a community level, I demonstrated how the power to detect the effect of environmental conditions on coral environments is drastically increased when the coral host-endosymbiotic algae relationship is interpreted holistically. The percentage of the variability of the community structure that can be explained by environmental variables in the central coast of Venezuela is doubled when the unit of selection considered is the holobiont instead of the coral host or the endosymbiont independently. This approach can be crucial for the detection of subtle changes in coral communities as the frequency and intensity of disturbances increase rapidly. The increase in detection power provided by the different approaches developed in this project can both improve our understanding of the structuring role of mild disturbances in coral communities as well as help identify the effect of disturbances in an early stage before the perturbation reaches catastrophic proportions. This early identification of perturbations can be used for the development of adaptive management strategies that can increase the resistance and resilience of coral reefs in the future.

Coral reefs, the planet’s most diverse marine ecosystems, are threatened globally by climate change and locally by overfishing and pollution. The dynamic partnership between coral and their endosymbiotic algae (Symbiodinium) is the foundation of all tropical reef ecosystems. Symbiodinium provide coral with nutrients for growth, but stress can break down this symbiosis, causing coral bleaching. There are also life-history trade-offs amongst Symbiodinium types - some provide coral with more nutrition, while others are better able to cope with environmental stressors. Although these symbioses are believed to be a critical element of reef resilience, little is known about how local and global stressors alter these partnerships. In this thesis, I combine synthetic literature reviews and a meta-analysis, with field research, molecular analyses, bioinformatics, and statistical analyses to investigate environmentally-driven mechanisms of change in coral-symbiont interactions with the aim of advancing understanding of how corals will adapt to the stressors they now face. First, I conducted a review of coral-Symbiodinium interactions, from molecules to ecosystems and summarized the current state of the field and knowledge gaps. Next, I conducted a meta-analysis of coral bleaching and mortality during El Niño events and created an open-source coral heat stress data product. I found that the 2015-2016 El Niño instigated unprecedented thermal stress on reefs globally, and that, across all El Niño events, coral bleaching and mortality were greater at locations with higher long-term mean temperatures. I provided recommendations for future bleaching surveys, and in a related perspectives piece, highlighted the importance of survey timing during prolonged coral bleaching events. The latter three empirical chapters are based on my six field expeditions to Kiritimati (Christmas Island). Taking advantage of the atoll’s natural ecosystem-scale experiment, I tagged, sampled and tracked over 1,000 corals across its chronic human disturbance gradient. Since corals can uptake Symbiodinium from the surrounding environment, I first investigated the effect of local disturbance and winter storm waves on Symbiodinium communities in coral, sediment, and seawater. Greater variability in Symbiodinium communities at highly disturbed sites suggests that local disturbance destabilizes symbiont community structure. Since local disturbance influences Symbiodinium community structure and coral-associated microbial communities, I next examined the covariance of coral-associated Symbiodinium and microbial communities for six coral species across Kiritimati’s disturbance gradient. Most strikingly, I found corals on Kiritimati that recovered from globally unprecedented thermal stress, experienced during the 2015-2016 El Niño, while they were still at elevated temperatures. This is notable, because no coral has previously been documented to recover from bleaching while still under heat stress. Only corals protected from local stressors exhibited this capacity. Protected corals had distinct pre-bleaching algal symbiont communities and recovered with different algal symbionts, suggesting that Symbiodinium are the mechanism of resilience and that protection governs their communities. Together, this research provides novel evidence that local protection may be more important for coral resilience than previously thought, and that variability in symbiotic and microbial communities provides a potentially flexible mechanism for corals to respond to both local and global stressors. / Graduate / 2019-11-26

Corals form a symbiotic relationship with photosynthetic zooxanthellae from the genus Symbiodinium; the breakdown of this symbiosis results in the phenomenon known as coral bleaching. This relationship is especially vulnerable to high temperature stress, although corals may survive if they have resistant types of symbionts, or switch their community composition towards them. To assess the variation of the symbiont community in different environmental conditions, I recorded the temperature and collected samples from six scleractinian coral species and one calcifying hydrozoan, in two inshore, two mid-shelf, and two offshore reefs at 1, 15, and 30m depth, analyzing Symbiodinium diversity using Next Generation Sequencing with the SymPortal profile typing approach. The temperature was very similar for all points in winter, when coral samples were collected, but variation between points increased until a maximum at summer, with the shallower parts of the inshore reefs showing higher temperatures and the points at 30m depth showing the lowest. The Symbiodinium composition was more similar between samples of the same host species than among samples of the same reefs or depths. Coral species from the Pocilloporidae family and Millepora dichotoma showed specific association with different profile types, specifically, intragenomic variants of Symbiodinium type A1, which appears to be dominant in the Red Sea although it has not been reported for these species in other regions. The other species showed specific associations with types previously reported in other regions, mostly from clade C and D, although also having different types and intragenomic variants. For most cases, certain profile types, which can reflect different species or populations, appeared to be dominant in particular environmental conditions, following a distribution related with depth, reef type, or both. In conclusion, this study showed that the Symbiodinium composition depends more on the host species than on the environmental conditions, and within each species the adaptation to environmental gradients can rely on tolerant symbiont species or populations characteristic of the Red Sea, or association with different types and clades that are common also in other regions.

The stability of marine photosymbiotic holobionts has major implications for the future of coral reef communities. This study aims to describe the stability of the Red Sea giant clam holobiont over the duration of one year and during induced bleaching stress under laboratory thermal manipulations. Tridacnid clams of the species Tridacna maxima were sampled at three reef locations near the central Saudi coast of the Red Sea. Associated Symbiodinium of Red Sea giant clams have previously been described to be part of only Clade A, which suggests a strong specificity in the clam-algal partnership, but specific types and potential shifting of types within this clade have not been examined for giant clams. The results from this study confirm that tridacnid symbiont types shift over time and the change between three A1 types suggests a biological and functional significance of two undescribed A1 Symbiodinium types. Experimental bleaching shows that Red Sea giant clams, although exposed to rather hot temperatures naturally, will bleach at 34°C after two weeks, and severely bleached clams likely will not recover. During bleaching, Symbiodinium types shift as well, and shift more drastically than seasonal shifts during the year. This shifting may be an evolved characteristic of the giant clam to aid in surviving major changes in the environment. However, more research is needed to determine if these holobionts are capable of keeping up with the global forecast of warming in reef environments.