Rodrigo L. Moura

Rhodolith Beds Are Major CaCO3 Bio-Factories in the Tropical South West Atlantic

Rhodoliths are nodules of non-geniculate coralline algae that occur in shallow waters (<150 m depth) subjected to episodic disturbance. Rhodolith beds stand with kelp beds, seagrass meadows, and coralline algal reefs as one of the worlds four largest macrophyte-dominated benthic communities. Geographic distribution of rhodolith beds is discontinuous, with large concentrations off Japan, Australia and the Gulf of California, as well as in the Mediterranean, North Atlantic, eastern Caribbean and Brazil. Although there are major gaps in terms of seabed habitat mapping, the largest rhodolith beds are purported to occur off Brazil, where these communities are recorded across a wide latitudinal range (2°N - 27°S). To quantify their extent, we carried out an inter-reefal seabed habitat survey on the Abrolhos Shelf (16°50′ - 19°45′S) off eastern Brazil, and confirmed the most expansive and contiguous rhodolith bed in the world, covering about 20,900 km2. Distribution, extent, composition and structure of this bed were assessed with side scan sonar, remotely operated vehicles, and SCUBA. The mean rate of CaCO3 production was estimated from in situ growth assays at 1.07 kg m−2 yr−1, with a total production rate of 0.025 Gt yr−1, comparable to those of the worlds largest biogenic CaCO3 deposits. These gigantic rhodolith beds, of areal extent equivalent to the Great Barrier Reef, Australia, are a critical, yet poorly understood component of the tropical South Atlantic Ocean. Based on the relatively high vulnerability of coralline algae to ocean acidification, these beds are likely to experience a profound restructuring in the coming decades.

Diseases leading to accelerated decline of reef corals in the largest South Atlantic reef complex (Abrolhos Bank, eastern Brazil)

Although reef corals worldwide have sustained epizootics in recent years, no coral diseases have been observed in the southwestern Atlantic Ocean until now. Here we present an overview of the main types of diseases and their incidence in the largest and richest coral reefs in the South Atlantic (Abrolhos Bank, eastern Brazil). Qualitative observations since the 1980s and regular monitoring since 2001 indicate that coral diseases intensified only recently (2005-2007). Based on estimates of disease prevalence and progression rate, as well as on the growth rate of a major reef-building coral species (the Brazilian-endemic Mussismilia braziliensis), we predict that eastern Brazilian reefs will suffer a massive coral cover decline in the next 50 years, and that M. braziliensis will be nearly extinct in less than a century if the current rate of mortality due to disease is not reversed.

Abrolhos Bank Reef Health Evaluated by Means of Water Quality, Microbial Diversity, Benthic Cover, and Fish Biomass Data

The health of the coral reefs of the Abrolhos Bank (southwestern Atlantic) was characterized with a holistic approach using measurements of four ecosystem components: (i) inorganic and organic nutrient concentrations, [1] fish biomass, [1] macroalgal and coral cover and (iv) microbial community composition and abundance. The possible benefits of protection from fishing were particularly evaluated by comparing sites with varying levels of protection. Two reefs within the well-enforced no-take area of the National Marine Park of Abrolhos (Parcel dos Abrolhos and California) were compared with two unprotected coastal reefs (Sebastião Gomes and Pedra de Leste) and one legally protected but poorly enforced coastal reef (the “paper park” of Timbebas Reef). The fish biomass was lower and the fleshy macroalgal cover was higher in the unprotected reefs compared with the protected areas. The unprotected and protected reefs had similar seawater chemistry. Lower vibrio CFU counts were observed in the fully protected area of California Reef. Metagenome analysis showed that the unprotected reefs had a higher abundance of archaeal and viral sequences and more bacterial pathogens, while the protected reefs had a higher abundance of genes related to photosynthesis. Similar to other reef systems in the world, there was evidence that reductions in the biomass of herbivorous fishes and the consequent increase in macroalgal cover in the Abrolhos Bank may be affecting microbial diversity and abundance. Through the integration of different types of ecological data, the present study showed that protection from fishing may lead to greater reef health. The data presented herein suggest that protected coral reefs have higher microbial diversity, with the most degraded reef (Sebastião Gomes) showing a marked reduction in microbial species richness. It is concluded that ecological conditions in unprotected reefs may promote the growth and rapid evolution of opportunistic microbial pathogens.

Metagenomic Analysis of Healthy and White Plague-Affected Mussismilia braziliensis Corals

Coral health is under threat throughout the world due to regional and global stressors. White plague disease (WP) is one of the most important threats affecting the major reef builder of the Abrolhos Bank in Brazil, the endemic coral Mussismilia braziliensis. We performed a metagenomic analysis of healthy and WP-affected M. braziliensis in order to determine the types of microbes associated with this coral species. We also optimized a protocol for DNA extraction from coral tissues. Our taxonomic analysis revealed Proteobacteria, Bacteroidetes, Firmicutes, Cyanobacteria, and Actinomycetes as the main groups in all healthy and WP-affected corals. Vibrionales, members of the Cytophaga–Flavobacterium–Bacteroides complex, Rickettsiales, and Neisseriales were more abundant in the WP-affected corals. Diseased corals also had more eukaryotic metagenomic sequences identified as Alveolata and Apicomplexa. Our results suggest that WP disease in M. braziliensis is caused by a polymicrobial consortium.

Bacterial Community Associated with Healthy and Diseased Reef Coral Mussismilia hispida from Eastern Brazil

In order to characterize the bacterial community diversity associated to mucus of the coral Mussismilia hispida, four 16S rDNA libraries were constructed and 400 clones from each library were analyzed from two healthy colonies, one diseased colony and the surrounding water. Nine bacterial phyla were identified in healthy M. hispida, with a dominance of Proteobacteria, Actinobacteria, Acidobacteria, Lentisphaerae, and Nitrospira. The most commonly found species were related to the genera Azospirillum, Hirschia, Fabibacter, Blastochloris, Stella, Vibrio, Flavobacterium, Ochrobactrum, Terasakiella, Alkalibacter, Staphylococcus, Azospirillum, Propionibacterium, Arcobacter, and Paenibacillus. In contrast, diseased M. hispida had a predominance of one single species of Bacteroidetes, corresponding to more than 70% of the sequences. Rarefaction curves using evolutionary distance of 1% showed a greater decrease in bacterial diversity in the diseased M. hispida, with a reduction of almost 85% in OTUs in comparison to healthy colonies. ∫-Libshuff analyses show that significant p values obtained were <0.0001, demonstrating that the four libraries are significantly different. Furthermore, the sympatric corals M. hispida and Mussismilia braziliensis appear to have different bacterial community compositions according to Principal Component Analysis and Lineage-specific Analysis. Moreover, lineages that contribute to those differences were identified as α-Proteobacteria, Bacteroidetes, and Firmicutes. The results obtained in this study suggest host–microbe co-evolution in Mussismilia, and it was the first study on the diversity of the microbiota of the endemic and endangered of extinction Brazilian coral M. hispida from Abrolhos bank.

Bacterial diversity associated with the Brazilian endemic reef coral Mussismilia braziliensis

Aims:  We performed the first characterization of the microbiota associated with the reef coral Mussismilia braziliensis by means of a culture‐independent approach.

An extensive reef system at the Amazon River mouth

A novel Amazonian reef biome was discovered, encompassing large rhodolith and sponge beds under low light, low oxygen, and high POC. Large rivers create major gaps in reef distribution along tropical shelves. The Amazon River represents 20% of the global riverine discharge to the ocean, generating up to a 1.3 × 106–km2 plume, and extensive muddy bottoms in the equatorial margin of South America. As a result, a wide area of the tropical North Atlantic is heavily affected in terms of salinity, pH, light penetration, and sedimentation. Such unfavorable conditions were thought to imprint a major gap in Western Atlantic reefs. We present an extensive carbonate system off the Amazon mouth, underneath the river plume. Significant carbonate sedimentation occurred during lowstand sea level, and still occurs in the outer shelf, resulting in complex hard-bottom topography. A permanent near-bottom wedge of ocean water, together with the seasonal nature of the plume’s eastward retroflection, conditions the existence of this extensive (~9500 km2) hard-bottom mosaic. The Amazon reefs transition from accretive to erosional structures and encompass extensive rhodolith beds. Carbonate structures function as a connectivity corridor for wide depth–ranging reef-associated species, being heavily colonized by large sponges and other structure-forming filter feeders that dwell under low light and high levels of particulates. The oxycline between the plume and subplume is associated with chemoautotrophic and anaerobic microbial metabolisms. The system described here provides several insights about the responses of tropical reefs to suboptimal and marginal reef-building conditions, which are accelerating worldwide due to global changes.

Diversity and pathogenic potential of vibrios isolated from Abrolhos Bank corals.

We performed the first taxonomic characterization of vibrios and other culturable microbiota from apparently healthy and diseased Brazilian-endemic corals at the Abrolhos reef bank. The diseases affecting corals were tissue necrosis in Phyllogorgia dillatata, white plague and bleaching in Mussismilia braziliensis and bleaching in Mussismilia hispida. Bacterial isolates were obtained from mucus of 22 coral specimens originated from the Abrolhos Bank (i.e. Itacolomis reef, Recife de Fora reef and Santa Barbara Island) in 2007. Vibrios counts in the water and coral mucus were approximately 104 cfu ml(-1) and 106 cfu ml(-1) respectively. One hundred and thirty-one representative vibrio isolates were identified. Most vibrio isolates (n = 79) fell into the core group using the pyrH identification marker. According to our analysis, diseased corals did not possess a unique vibrio microbiota. Vibrio species encompassed strains originated from both apparently healthy and diseased corals. The pathogenic potential of representative vibrio isolates (V. alginolyticus 40B, V. harveyi-like 1DA3 and V. coralliilyticus 2DA3) were evaluated in a standardized bioassay using the animal model Drosophila melanogaster and caused 25-88% mortality. This is the first taxonomic characterization of the culturable microbiota from the Brazilian-endemic corals. Endemic Brazilian corals are a reservoir of the vibrio core group. Vibrio alginolyticus, V. harveyi and V. coralliilyticus are dominant in the mucus of these corals and may be a normal component of the holobiont.

Extensive Rhodolith Beds Cover the Summits of Southwestern Atlantic Ocean Seamounts

Abstract PEREIRA-FILHO, G.H.; AMADO-FILHO, G.M.; MOURA, R.L.; BASTOS, A.C.; GUIMARÃES, S.M.P.B.; SALGADO, L.T.; FRANCINI-FILHO, R.B.; BAHIA, R.G.; ABRANTES, D.P.; GUTH, A.Z., and BRASILEIRO, P.S., 2012. Extensive rhodolith beds cover the summits of southwestern Atlantic Ocean seamounts. Calcium carbonate production by marine organisms is an essential process in the global budget of , and coralline reefs are the most important benthic carbonate producers. Crustose coralline algae (CCA) are well recognized as the most important carbonate builders in the tropical Brazilian continental shelf, forming structural reefs and extensive rhodolith beds. However, the distribution of CCA beds, as well as their role in mineralization in mesophotic communities and isolated carbonate banks, is still poorly known. To characterize the bottom features of several seamount summits in the Southwestern Atlantic (SWA), side-scan sonar records, remotely operated vehicle imagery, and benthic samples with mixed-gas scuba diving were acquired during two recent research cruises (March 2009 and February 2011). The tops of several seamounts within this region are relatively shallow (∼60 m), flat, and dominated by rhodolith beds (Vitória, Almirante Saldanha, Davis, and Jaseur seamounts, as well as the Trindade Island shelf). On the basis of abundance, dimensions, vitality, and growth rates of CCA nodules, a mean CaCO3 production was estimated, ranging from 0.4 to 1.8 kg m−2 y−1, with a total production reaching 1.5 × 10−3 Gt y−1. Our results indicate that these SWA seamount summits provide extensive areas of shallow reef area and represent 0.3% of the worlds carbonate banks. The importance of this habitat has been highly neglected, and immediate management needs must be fulfilled in the short term to ensure long-term persistence of the ecosystem services provided by these offshore carbonate realms.

Live coral predation by parrotfishes (Perciformes: Scaridae) in the Abrolhos Bank, eastern Brazil, with comments on the classification of species into functional groups

Parrotfishes (Perciformes: Scaridae) represent a critical functional group on coral reefs because their intense herbivory activity helps in avoiding coral overgrowth by algae. Although feeding preferentially on algae and detritus, some parrotfish species also consume live corals, leading to detrimental effects that may offset the benefits of removing competitive seaweeds. Parrotfish species differ markedly in terms of jaw morphology, foraging activity and extent of substratum excavation, and are typically divided into three functional groups: browsers, scrapers and excavators. The recognition of species within each functional group helps to understand their relative effects in terms of bioerosion, coral fitness and survival, habitat alteration and ecosystem dynamics. Here we report on live coral predation by the Brazilian endemic parrotfishes Scarus trispinosus and Sparisoma amplum in the largest coral reefs of the South Atlantic (Abrolhos Bank, eastern Brazil) and comment on their classification into functional groups based on direct behavioral observations. Scarus trispinosus and Sp. amplum allocated 0.8% and 8.1% of their bites to live corals respectively. Sparisoma amplum fed at lower rates, took shorter feeding forays and larger bites than Sc. trispinosus. Bite rates and foray size were negatively correlated to body size for Sc. trispinosus, but not for Sp. amplum. Our results indicate that Sp. amplum may be primarily recognized as an excavating species, as well as the most specialized parrotfish coral predator in Brazil, while Sc. trispinosus may be recognized as a scraper or excavator depending on its body size. This functional classification corresponds to the classification used for the putative sister taxa of Sc. trispinosus (Sc. coeruleus) and the sister taxa of Sp. amplum (Sp. viride) in the Caribbean, indicating that these two congeneric species pairs play similar ecological roles in different geographic regions.