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.

[1]  B. Willis,et al.  Diversities of coral-associated bacteria differ with location, but not species, for three acroporid corals on the Great Barrier Reef. , 2009, FEMS microbiology ecology.

[2]  B. Lapointe,et al.  The relative importance of nutrient enrichment and herbivory on macroalgal communities near Norman's Pond Cay, Exumas Cays, Bahamas: a "natural" enrichment experiment , 2004 .

[3]  D. Bellwood,et al.  Quantifying herbivory across a coral reef depth gradient , 2007 .

[4]  Manfred Ehrhardt,et al.  Methods of seawater analysis , 1999 .

[5]  D. Bellwood,et al.  Phase Shifts, Herbivory, and the Resilience of Coral Reefs to Climate Change , 2007, Current Biology.

[6]  L. Martinelli,et al.  Lignin phenols used to infer organic matter sources to Sepetiba Bay – RJ, Brasil , 2010 .

[7]  R. Francini-Filho,et al.  Challenges and Prospects of Fisheries Co-Management under a Marine Extractive Reserve Framework in Northeastern Brazil , 2009 .

[8]  R. Francini-Filho,et al.  Evidence for spillover of reef fishes from a no-take marine reserve: An evaluation using the before-after control-impact (BACI) approach , 2008 .

[9]  D. Vaulot,et al.  Prochlorococcus, a Marine Photosynthetic Prokaryote of Global Significance , 1999, Microbiology and Molecular Biology Reviews.

[10]  John B. Lewis,et al.  Abundance, distribution and partial mortality of the massive coral Siderastrea siderea on degrading coral reefs at Barbados, West Indies , 1997 .

[11]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[12]  C. Rezende,et al.  Distribution of HNA and LNA bacterial groups in the Southwest Atlantic Ocean , 2007 .

[13]  L. Richardson,et al.  Microbial Communities in the Surface Mucopolysaccharide Layer and the Black Band Microbial Mat of Black Band-Diseased Siderastrea siderea , 2006, Applied and Environmental Microbiology.

[14]  J. Handelsman,et al.  Introducing DOTUR, a Computer Program for Defining Operational Taxonomic Units and Estimating Species Richness , 2005, Applied and Environmental Microbiology.

[15]  J. Cortés.  Latin American coral reefs , 2003 .

[16]  Florent E. Angly,et al.  Microbial Ecology of Four Coral Atolls in the Northern Line Islands , 2008, PloS one.

[17]  G. Russ.  Yet another review of marine reserves as reef fishery management tools , 2002 .

[18]  O. Hoegh‐Guldberg,et al.  Dynamics of a temperature-related coral disease outbreak , 2004 .

[19]  J. Bruno,et al.  Nutrient enrichment can increase the severity of coral diseases , 2003 .

[20]  M. Attrill,et al.  Seasonal and spatial controls on the delivery of excess nutrients to nearshore and offshore coral reefs of Brazil , 2006 .

[21]  Dennis Swanger,et al.  Advances in microbial ecology , 1979, Economic Botany.

[22]  A. Muirhead,et al.  Changes in sulfate-reducing bacterial populations during the onset of black band disease , 2011, The ISME Journal.

[23]  B. Halpern,et al.  Biological Effects Within No-Take Marine Reserves: A global Synthesis , 2009 .

[24]  S. R. Santos,et al.  The Adaptive Bleaching Hypothesis: Experimental Tests of Critical Assumptions , 2001, The Biological Bulletin.

[25]  M. Søndergaard,et al.  Net accumulation and flux of dissolved organic carbon and dissolved organic nitrogen in marine plankton communities , 2000 .

[26]  V. Ittekkot,et al.  Biogeochemical characteristics of coastal waters adjacent to small river–mangrove systems, East Brazil , 1999 .

[27]  J. Sieburth,et al.  Studies on algal substances in the sea. III. The production of extracellular organic matter by littoral marine algae , 1969 .

[28]  William J. Kimmerer,et al.  Kaneohe Bay Sewage Diversion Experiment: Perspectives on Ecosystem Responses to Nutritional Perturbation , 1981 .

[29]  R. Francini-Filho,et al.  Dynamics of fish assemblages on coral reefs subjected to different management regimes in the Abrolhos Bank, eastern Brazil , 2008 .

[30]  E. Sala,et al.  Large Recovery of Fish Biomass in a No-Take Marine Reserve , 2011, PloS one.

[31]  F. Thompson,et al.  Bacterial Community Associated with Healthy and Diseased Reef Coral Mussismilia hispida from Eastern Brazil , 2010, Microbial Ecology.

[32]  Forest Rohwer,et al.  Hyperspectral and Physiological Analyses of Coral-Algal Interactions , 2009, PloS one.

[33]  B. Willis,et al.  Metagenomic analysis of the coral holobiont during a natural bleaching event on the Great Barrier Reef. , 2011, Environmental microbiology reports.

[34]  Spatial dynamics of benthic competition on coral reefs , 2012, Oecologia.

[35]  P. Bell,et al.  Eutrophication and coral reefs—some examples in the Great Barrier Reef lagoon , 1992 .

[36]  M. Hay,et al.  Chemically rich seaweeds poison corals when not controlled by herbivores , 2010, Proceedings of the National Academy of Sciences.

[37]  Claude E. Shannon,et al.  The mathematical theory of communication , 1950 .

[38]  F. V. AraÚjo,et al.  Flow cytometry assessment of bacterioplankton in tropical marine environments. , 2003, Journal of microbiological methods.

[39]  W. Bossert,et al.  The Measurement of Diversity , 2001 .

[40]  O. Kinne,et al.  Marine ecology progress series , 1989 .

[41]  Elizabeth R. Selig,et al.  A Global Analysis of the Effectiveness of Marine Protected Areas in Preventing Coral Loss , 2010, PloS one.

[42]  C. Summerhayes,et al.  The influence of upwelling on suspended matter and shelf sediments off southeastern Brazil , 1976 .

[43]  T. Hughes.  Catastrophes, Phase Shifts, and Large-Scale Degradation of a Caribbean Coral Reef , 1994, Science.

[44]  N. Knowlton,et al.  Shifting Baselines, Local Impacts, and Global Change on Coral Reefs , 2008, PLoS biology.

[45]  Isabelle M. Côté,et al.  Effects of marine reserve age on fish populations: a global meta‐analysis , 2009 .

[46]  Dennis A. Hansell,et al.  Effect of nutrient amendments on bacterioplankton production, community structure, and DOC utilization in the northwestern Sargasso Sea , 2002, Aquatic Microbial Ecology.

[47]  Andreas Wilke,et al.  phylogenetic and functional analysis of metagenomes , 2022 .

[48]  Robert G. Beiko,et al.  Identifying biologically relevant differences between metagenomic communities , 2010, Bioinform..

[49]  C. Wild,et al.  Organic matter release by coral reef associated benthic algae in the Northern Red Sea , 2010 .

[50]  R. Neutze,et al.  Proteorhodopsin Phototrophy Promotes Survival of Marine Bacteria during Starvation , 2010, PLoS biology.

[51]  Z. M. Leão,et al.  Corals and coral reefs of Brazil , 2003 .

[52]  B. Lapointe,et al.  Reevaluation of ENCORE: Support for the Eutrophication Threshold Model for Coral Reefs , 2007, Ambio.

[53]  Natalia N. Ivanova,et al.  Genomic Potential of Marinobacter aquaeolei, a Biogeochemical “Opportunitroph” , 2011, Applied and Environmental Microbiology.

[54]  L. Kaufman,et al.  Foraging activity of roving herbivorous reef fish (Acanthuridae and Scaridae) in eastern Brazil: influence of resource availability and interference competition , 2009, Journal of the Marine Biological Association of the United Kingdom.

[55]  Z. M. Leão,et al.  Nutrification impacts on coral reefs from northern Bahia, Brazil , 2000, Hydrobiologia.

[56]  H. Ducklow,et al.  Oceanic Bacterial Production , 1992 .

[57]  J. G. Field,et al.  The Ecological Role of Water-Column Microbes in the Sea* , 1983 .

[58]  O. Pantos,et al.  The bacterial ecology of a plague-like disease affecting the Caribbean coral Montastrea annularis. , 2003, Environmental microbiology.

[59]  M. Attrill,et al.  Coastal nutrification in Brazil: A review of the role of nutrient excess on coral reef demise , 2008 .

[60]  Les Kaufman,et al.  Diseases leading to accelerated decline of reef corals in the largest South Atlantic reef complex (Abrolhos Bank, eastern Brazil). , 2008, Marine pollution bulletin.

[61]  F. Rohwer,et al.  Indirect effects of algae on coral: algae-mediated, microbe-induced coral mortality. , 2006, Ecology letters.

[62]  R. Francini-Filho,et al.  Nested sampling: an improved visual-census technique for studying reef fish assemblages , 2008 .

[63]  Craig E. Nelson,et al.  Effects of Coral Reef Benthic Primary Producers on Dissolved Organic Carbon and Microbial Activity , 2011, PloS one.

[64]  Craig E. Nelson,et al.  Depleted dissolved organic carbon and distinct bacterial communities in the water column of a rapid-flushing coral reef ecosystem , 2011, The ISME Journal.

[65]  Farooq Azam,et al.  Microbial Control of Oceanic Carbon Flux: The Plot Thickens , 1998, Science.

[66]  J. Bauer,et al.  Utilization and turnover of labile dissolved organic matter by bacterial heterotrophs in eastern North Pacific surface waters , 1996 .

[67]  G. O’Brien.  Coral Reefs in the Microbial Sea , 2011 .

[68]  F. Rodríguez-Valera,et al.  Biogeography of the ubiquitous marine bacterium Alteromonas macleodii determined by multilocus sequence analysis , 2008, Molecular ecology.

[69]  S. Ellner,et al.  How Microbial Community Composition Regulates Coral Disease Development , 2010, PLoS biology.

[70]  Forest Rohwer,et al.  Coral Reefs in the Microbial Seas , 2010 .

[71]  P. Bork,et al.  Toward molecular trait-based ecology through integration of biogeochemical, geographical and metagenomic data , 2011, Molecular systems biology.

[72]  G. Edgar,et al.  Variation in reef fish and invertebrate communities with level of protection from fishing across the Eastern Tropical Pacific seascape , 2011 .

[73]  Florent E. Angly,et al.  Metagenomic analysis of stressed coral holobionts. , 2009, Environmental microbiology.

[74]  M. Noordewier,et al.  Genome Streamlining in a Cosmopolitan Oceanic Bacterium , 2005, Science.

[75]  Bronte Tilbrook,et al.  High CO2 enhances the competitive strength of seaweeds over corals , 2011, Ecology letters.

[76]  James R. Knight,et al.  Genome sequencing in microfabricated high-density picolitre reactors , 2005, Nature.

[77]  Robert A. Edwards,et al.  Quality control and preprocessing of metagenomic datasets , 2011, Bioinform..

[78]  Y. Loya,et al.  Bacterial Strain BA-3 and a filterable factor cause a white plague-like disease in corals from the Eilat coral reef , 2005 .

[79]  S. Sunagawa,et al.  Threatened Corals Provide Underexplored Microbial Habitats , 2010, PloS one.

[80]  Sallie W. Chisholm,et al.  Niche Partitioning Among Prochlorococcus Ecotypes Along Ocean-Scale Environmental Gradients , 2006, Science.

[81]  M. Hay,et al.  Effects of herbivores, nutrient enrichment, and their interactions on macroalgal proliferation and coral growth , 2009, Coral Reefs.

[82]  I. Hewson,et al.  Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. , 2010, Integrative and comparative biology.