Decline of a distinct coral reef holobiont community under ocean acidification.

BACKGROUND: Microbes play vital roles across coral reefs both in the environment and inside and upon macrobes (holobionts), where they support critical functions such as nutrition and immune system modulation. These roles highlight the potential ecosystem-level importance of microbes, yet most knowledge of microbial functions on reefs is derived from a small set of holobionts such as corals and sponges. Declining seawater pH - an important global coral reef stressor - can cause ecosystem-level change on coral reefs, providing an opportunity to study the role of microbes at this scale. We use an in situ experimental approach to test the hypothesis that under such ocean acidification (OA), known shifts among macrobe trophic and functional groups may drive a general ecosystem-level response extending across macrobes and microbes, leading to reduced distinctness between the benthic holobiont community microbiome and the environmental microbiome. RESULTS: We test this hypothesis using genetic and chemical data from benthic coral reef community holobionts sampled across a pH gradient from CO2 seeps in Papua New Guinea. We find support for our hypothesis; under OA, the microbiome and metabolome of the benthic holobiont community become less compositionally distinct from the sediment microbiome and metabolome, suggesting that benthic macrobe communities are colonised by environmental microbes to a higher degree under OA conditions. We also find a simplification and homogenisation of the benthic photosynthetic community, and an increased abundance of fleshy macroalgae, consistent with previously observed reef microbialisation. CONCLUSIONS: We demonstrate a novel structural shift in coral reefs involving macrobes and microbes: that the microbiome of the benthic holobiont community becomes less distinct from the sediment microbiome under OA. Our findings suggest that microbialisation and the disruption of macrobe trophic networks are interwoven general responses to environmental stress, pointing towards a universal, undesirable, and measurable form of ecosystem changed. Video Abstract.

Spineless and overlooked: DNA metabarcoding of autonomous reef monitoring structures reveals intra- and interspecific genetic diversity in Mediterranean invertebrates.

The ability to gather genetic information using DNA metabarcoding of bulk samples obtained directly from the environment is crucial to determine biodiversity baselines and understand population dynamics in the marine realm. While DNA metabarcoding is effective in evaluating biodiversity at community level, genetic patterns within species are often concealed in metabarcoding studies and overlooked for marine invertebrates. In the present study, we implement recently developed bioinformatics tools to investigate intraspecific genetic variability for invertebrate taxa in the Mediterranean Sea. Using metabarcoding samples from Autonomous Reef Monitoring Structures (ARMS) deployed in three locations, we present haplotypes and diversity estimates for 145 unique species. While overall genetic diversity was low, we identified several species with high diversity records and potential cryptic lineages. Further, we emphasize the spatial scale of genetic variability, which was observed from locations to individual sampling units (ARMS). We carried out a population genetic analysis of several important yet understudied species, which highlights the current knowledge gap concerning intraspecific genetic patterns for the target taxa in the Mediterranean basin. Our approach considerably enhances biodiversity monitoring of charismatic and understudied Mediterranean species, which can be incorporated into ARMS surveys.

Coral reef benthic community changes in the Anthropocene: Biogeographic heterogeneity, overlooked configurations, and methodology.

Non-random community changes are becoming more frequent in many ecosystems. In coral reefs, changes towards communities dominated by other than hard corals are increasing in frequency, with severe impacts on ecosystem functioning and provision of ecosystem services. Although new research suggests that a variety of alternative communities (i.e. not dominated by hard corals) exist, knowledge on the global diversity and functioning of alternative coral reef benthic communities, especially those not dominated by algae, remains scattered. In this systematic review and meta-analysis of 523 articles, we analyse the different coral reef benthic community changes reported to date and discuss the advantages and limitations of the methods used to study these changes. Furthermore, we used field cover data (1116 reefs from the ReefCheck database) to explore the biogeographic and latitudinal patterns in dominant benthic organisms. We found a mismatch between literature focus on coral-algal changes (over half of the studies analysed) and observed global natural patterns. We identified strong biogeographic patterns, with the largest and most biodiverse biogeographic regions (Western and Central Indo-Pacific) presenting previously overlooked soft-coral-dominated communities as the most abundant alternative community. Finally, we discuss the potential biases associated with methods that overlook ecologically important cryptobenthic communities and the potential of new technological advances in improving monitoring efforts. As coral reef communities inevitably and swiftly change under changing ocean conditions, there is an urgent need to better understand the distribution, dynamics as well as the ecological and societal impacts of these new communities.

A quantitative comparison of towed-camera and diver-camera transects for monitoring coral reefs.

Novel tools and methods for monitoring marine environments can improve efficiency but must not compromise long-term data records. Quantitative comparisons between new and existing methods are therefore required to assess their compatibility for monitoring. Monitoring of shallow water coral reefs is typically conducted using diver-based collection of benthic images along transects. Diverless systems for obtaining underwater images (e.g. towed-cameras, remotely operated vehicles, autonomous underwater vehicles) are increasingly used for mapping coral reefs. Of these imaging platforms, towed-cameras offer a practical, low cost and efficient method for surveys but their utility for repeated measures in monitoring studies has not been tested. We quantitatively compare a towed-camera approach to repeated surveys of shallow water coral reef benthic assemblages on fixed transects, relative to benchmark data from diver photo-transects. Differences in the percent cover detected by the two methods was partly explained by differences in the morphology of benthic groups. The reef habitat and physical descriptors of the site-slope, depth and structural complexity-also influenced the comparability of data, with differences between the tow-camera and the diver data increasing with structural complexity and slope. Differences between the methods decreased when a greater number of images were collected per tow-camera transect. We attribute lower image quality (variable perspective, exposure and focal distance) and lower spatial accuracy and precision of the towed-camera transects as the key reasons for differences in the data from the two methods and suggest changes to the sampling design to improve the application of tow-cameras to monitoring.

A rapid spread of the stony coral tissue loss disease outbreak in the Mexican Caribbean.

Caribbean reef corals have experienced unprecedented declines from climate change, anthropogenic stressors and infectious diseases in recent decades. Since 2014, a highly lethal, new disease, called stony coral tissue loss disease, has impacted many reef-coral species in Florida. During the summer of 2018, we noticed an anomalously high disease prevalence affecting different coral species in the northern portion of the Mexican Caribbean. We assessed the severity of this outbreak in 2018/2019 using the AGRRA coral protocol to survey 82 reef sites across the Mexican Caribbean. Then, using a subset of 14 sites, we detailed information from before the outbreak (2016/2017) to explore the consequences of the disease on the condition and composition of coral communities. Our findings show that the disease outbreak has already spread across the entire region by affecting similar species (with similar disease patterns) to those previously described for Florida. However, we observed a great variability in prevalence and tissue mortality that was not attributable to any geographical gradient. Using long-term data, we determined that there is no evidence of such high coral disease prevalence anywhere in the region before 2018, which suggests that the entire Mexican Caribbean was afflicted by the disease within a few months. The analysis of sites that contained pre-outbreak information showed that this event considerably increased coral mortality and severely changed the structure of coral communities in the region. Given the high prevalence and lethality of this disease, and the high number of susceptible species, we encourage reef researchers, managers and stakeholders across the Western Atlantic to accord it the highest priority for the near future.

Cobble community DNA as a tool to monitor patterns of biodiversity within kelp forest ecosystems.

Kelp forest ecosystems dominate 150,000 km of global temperate coastline, rivalling the coastal occurrence of coral reefs. Despite the astounding biological diversity and productive ecological communities associated with kelp forests, patterns of species richness and composition are difficult to monitor and compare. Crustose coralline algae are a critically important substrate for propagule settlement for a range of kelp forest species. Coralline-covered cobbles are home to hundreds of species of benthic animals and algae and form a replicable unit for ecological assays. Here, we use DNA metabarcoding of bulk DNA extracts sampled from cobbles to explore patterns of species diversity in kelp forests of the central California coast. The data from 97 cobbles within kelp forest ecosystems at three sites in Central California show the presence of 752 molecular operational taxonomic units (MOTUs) and 53 MOTUs assigned up to the species level with >95% similarity to current databases. We are able to detect spatial patterns of important management targets such as abalone recruits, and localized abundance of sea stars in 2012. Comparison of classic ecological surveys of these sites reveals large differences in species targets for these two approaches. In order to make such comparisons more quantitative, we use Presence/Absence Metabarcoding, using the fraction of replicate cobbles showing a species as a measure of its local abundance. This approach provides a fast and repeatable survey method that can be applied for biodiversity assessments across systems to shed light on the impact of different ecological disturbances and the role played by marine protected areas.

Disentangling the complex microbial community of coral reefs using standardized Autonomous Reef Monitoring Structures (ARMS).

Autonomous Reef Monitoring Structures (ARMS) have been applied worldwide to describe eukaryotic cryptic reef fauna. Conversely, bacterial communities, which are critical components of coral reef ecosystem functioning, remain largely overlooked. Here we deployed 56 ARMS across the 2,000-km spread of the Red Sea to assay biodiversity, composition and inferred underlying functions of coral reef-associated bacterial communities via 16S rRNA gene sequencing. We found that bacterial community structure and diversity aligned with environmental differences. Indeed, sea surface temperature and macroalgae cover were key in explaining bacterial relative abundance. Importantly, taxonomic and functional alpha diversity decreased under more extreme environmental conditions (e.g., higher temperatures) in the southern Red Sea. This may imply a link between bacterial community diversity and functional capabilities, with implications for conservation management. Our study demonstrates the utility of ARMS to investigate the response of coral reef-associated bacterial communities to environmental change.

Beyond the visual: using metabarcoding to characterize the hidden reef cryptobiome.

In an era of coral reef degradation, our knowledge of ecological patterns in reefs is biased towards large conspicuous organisms. The majority of biodiversity, however, inhabits small cryptic spaces within the framework of the reef. To assess this biodiverse community, which we term the 'reef cryptobiome', we deployed 87 autonomous reef monitoring structures (ARMS), on 22 reefs across 16 degrees latitude of the Red Sea. Combining ARMS with metabarcoding of the mitochondrial cytochrome oxidase I gene, we reveal a rich community, including the identification of 14 metazoan phyla within 10 416 operational taxonomic units (OTUs). While mobile and sessile subsets were similarly structured along the basin, the main environmental driver was different (particulate organic matter and sea surface temperature, respectively). Distribution patterns of OTUs showed that only 1.5% were present in all reefs, while over half were present in a single reef. On both local and regional scales, the majority of OTUs were rare. The high heterogeneity in community patterns of the reef cryptobiome has implications for reef conservation. Understanding the biodiversity patterns of this critical component of reef functioning will enable a sound knowledge of how coral reefs will respond to future anthropogenic impacts.

Decline in coral cover and flattening of the reefs around Mauritius (1998-2010).

Coral reefs are degrading through the impacts of multiple anthropogenic stressors. How are coral reef communities going to change and how to protect them for future generations are important conservation questions. Using coral reef data from Mauritius, we examined changes in cover in 23 benthic groups for a 13-yr period and at 15 sites. Moreover, we determined which land-based stressor out of four (human population, agriculture, tourism, rainfall) correlated the most with the observed changes in coral reef cover. Among the stony corals, Acropora corals appeared to be the most impacted, decreasing in cover at many sites. However, the non-Acropora encrusting group increased in cover at several sites. The increase in abundance of dead corals and rubble at some sites also supported the observations of stony coral decline during the study period. Additionally, the decline in stony corals appeared to be more pronounced in second half of the study period for all sites suggesting that a global factor rather than a local factor was responsible for this decline. There was little change in cover for the other benthic groups, some of which were quite rare. Human population was significantly correlated with changes in coral reef cover for 11 sites, followed by tourism and agriculture. Rainfall, a proxy for runoff, did not appear to affect coral reef cover. Overall, our results showed that there has been a decline of stony coral cover especially the ones with complex morphologies, which in turn suggest that coral reefs around Mauritius have experienced a decline in habitat complexity during the study period. Our study also suggests that humans are an important factor contributing to the demise of coral reefs around the island.

Power analysis as a tool to identify statistically informative indicators for monitoring coral reef disturbances.

Extensive biological field surveys are costly and time consuming. To optimize sampling and ensure regular monitoring on the long term, identifying informative indicators of anthropogenic disturbances is a priority. In this study, we used 1800 candidate indicators by combining metrics measured from coral, fish, and macro-invertebrate assemblages surveyed from 2006 to 2012 in the vicinity of an ongoing mining project in the Voh-Koné-Pouembout lagoon, New Caledonia. We performed a power analysis to identify a subset of indicators which would best discriminate temporal changes due to a simulated chronic anthropogenic impact. Only 4% of tested indicators were likely to detect a 10% annual decrease of values with sufficient power (>0.80). Corals generally exerted higher statistical power than macro-invertebrates and fishes because of lower natural variability and higher occurrence. For the same reasons, higher taxonomic ranks provided higher power than lower taxonomic ranks. Nevertheless, a number of families of common sedentary or sessile macro-invertebrates and fishes also performed well in detecting changes: Echinometridae, Isognomidae, Muricidae, Tridacninae, Arcidae, and Turbinidae for macro-invertebrates and Pomacentridae, Labridae, and Chaetodontidae for fishes. Interestingly, these families did not provide high power in all geomorphological strata, suggesting that the ability of indicators in detecting anthropogenic impacts was closely linked to reef geomorphology. This study provides a first operational step toward identifying statistically relevant indicators of anthropogenic disturbances in New Caledonia's coral reefs, which can be useful in similar tropical reef ecosystems where little information is available regarding the responses of ecological indicators to anthropogenic disturbances.

Assessing coral health and disease from digital photographs and in situ surveys.

Methods for monitoring the status of marine communities are increasingly adopting the use of images captured in the field. However, it is not always clear how data collected from photographic images relate to historic data collected using traditional underwater visual census methods. Here, we compare coral health and disease data collected in situ by scuba divers with photographic images collected simultaneously at 12 coral reef sites. Five globally relevant coral diseases were detected on 194 colonies from in situ surveys and 79 colonies from photos, whilst 698 colonies from in situ surveys and 535 colonies from photos exhibited signs of compromised health other than disease. Comparisons of in situ surveys with photographic analyses indicated that the number of disease cases occurring in the examined coral populations (prevalence) was six times higher (4.5 vs. 0.8% of colonies), whilst compromised health was three times higher (14 vs. 4% of colonies) from in situ surveys. Skeletal eroding band disease, sponge overgrowth and presence of Waminoa flatworms were not detected in photographs, though they were identified in situ. Estimates of black band disease and abnormally pigmented coral tissues were similar between the two methods. Estimates of the bleached and healthy colonies were also similar between methods and photographic analyses were a strong predictor of bleached (r 2 = 0.8) and healthy (r 2 = 0.5) colony prevalence from in situ surveys. Moreover, when data on disease and compromised health states resulting in white or pale coral colony appearance were pooled, the prevalence of 'white' colonies from in situ (14%) and photographic analyses (11%) were statistically similar. Our results indicate that information on coral disease and health collected by in situ surveys and photographic analyses are not directly comparable, with in situ surveys generally providing higher estimates of prevalence and greater ability to identify some diseases and compromised states. Careful sampling of photographs can however identify signs of coral stress, including some coral diseases, which may be used to trigger early-warning management interventions.

Bayesian adaptive design: improving the effectiveness of monitoring of the Great Barrier Reef.

Monitoring programs are essential for understanding patterns, trends, and threats in ecological and environmental systems. However, such programs are costly in terms of dollars, human resources, and technology, and complex in terms of balancing short- and long-term requirements. In this work, We develop new statistical methods for implementing cost-effective adaptive sampling and monitoring schemes for coral reef that can better utilize existing information and resources, and which can incorporate available prior information. Our research was motivated by developing efficient monitoring practices for Australia's Great Barrier Reef. We develop and implement two types of adaptive sampling schemes, static and sequential, and show that they can be more informative and cost-effective than an existing (nonadaptive) monitoring program. Our methods are developed in a Bayesian framework with a range of utility functions relevant to environmental monitoring. Our results demonstrate the considerable potential for adaptive design to support improved management outcomes in comparison to set-and-forget styles of surveillance monitoring.

Deep COI sequencing of standardized benthic samples unveils overlooked diversity of Jordanian coral reefs in the northern Red Sea.

High-throughput sequencing (HTS) of DNA barcodes (metabarcoding), particularly when combined with standardized sampling protocols, is one of the most promising approaches for censusing overlooked cryptic invertebrate communities. We present biodiversity estimates based on sequencing of the cytochrome c oxidase subunit 1 (COI) gene for coral reefs of the Gulf of Aqaba, a semi-enclosed system in the northern Red Sea. Samples were obtained from standardized sampling devices (Autonomous Reef Monitoring Structures (ARMS)) deployed for 18 months. DNA barcoding of non-sessile specimens >2 mm revealed 83 OTUs in six phyla, of which only 25% matched a reference sequence in public databases. Metabarcoding of the 2 mm - 500 µm and sessile bulk fractions revealed 1197 OTUs in 15 animal phyla, of which only 4.9% matched reference barcodes. These results highlight the scarcity of COI data for cryptobenthic organisms of the Red Sea. Compared with data obtained using similar methods, our results suggest that Gulf of Aqaba reefs are less diverse than two Pacific coral reefs but much more diverse than an Atlantic oyster reef at a similar latitude. The standardized approaches used here show promise for establishing baseline data on biodiversity, monitoring the impacts of environmental change, and quantifying patterns of diversity at regional and global scales.

Please mind the gap - Visual census and cryptic biodiversity assessment at central Red Sea coral reefs.

Coral reefs harbor the most diverse assemblages in the ocean, however, a large proportion of the diversity is cryptic and, therefore, undetected by standard visual census techniques. Cryptic and exposed communities differ considerably in species composition and ecological function. This study compares three different coral reef assessment protocols: i) visual benthic reef surveys: ii) visual census of Autonomous Reef Monitoring Structures (ARMS) plates; and iii) metabarcoding techniques of the ARMS (including sessile, 106-500 µm and 500-2000 µm size fractions), that target the cryptic and exposed communities of three reefs in the central Red Sea. Visual census showed a dominance of Cnidaria (Anthozoa) and Rhodophyta on the reef substrate, while Porifera, Bryozoa and Rhodophyta were the most abundant groups on the ARMS plates. Metabarcoding, targeting the 18S rRNA gene, significantly increased estimates of the species diversity (p < 0.001); revealing that Annelida were generally the dominant phyla (in terms of reads) of all fractions and reefs. Furthermore, metabarcoding detected microbial eukaryotic groups such as Syndiniophyceae, Mamiellophyceae and Bacillariophyceae as relevant components of the sessile fraction. ANOSIM analysis showed that the three reef sites showed no differences based on the visual census data. Metabarcoding showed a higher sensitivity for identifying differences between reef communities at smaller geographic scales than standard visual census techniques as significant differences in the assemblages were observed amongst the reefs. Comparison of the techniques showed no similar patterns for the visual techniques while the metabarcoding of the ARMS showed similar patterns amongst fractions. Establishing ARMS as a standard tool in reef monitoring will not only advance our understanding of local processes and ecological community response to environmental changes, as different faunal components will provide complementary information but also improve the estimates of biodiversity in coral reef benthic communities. This study lays the foundations for further studies looking at integrating traditional reef survey methodologies with complementary approaches, such as metabarcoding, which investigate other components of the reef community.

Monitoreo de la ictiofauna usando grupos taxonómicos superiores en el Parque Nacional Cabo Pulmo, México

Ichthyofauna monitoring using higher taxa in Cabo Pulmo National Park, México. The uses of biological indicators allow to save time, resources and staff efforts when monitoring programs are conducted. The reef fishes are among the species with biggest potential as indicators since they are conspicuous, easy to identify in the field and have ecological and economical importance. The objective of this study was to evaluate the usefulness of higher taxa to predict fish ecological indices in Cabo Pulmo reef. We generated multiple stepwise regression equations with species abundance data grouped at genera and family levels as factors, and using ecological indices (H´, J´, Δ*) as dependent variables. To test the efficiency of the models, the expected indexes were compared with those observed in the field during independent test surveys. Results showed that all models were highly significant, and the best fit occurred at genus level to H´, while those used for Δ*, based on family data level, were less precise. The proportion of variables required to apply prediction models of any ecological index never exceeded 41% of the total taxa (genera or families). In conclusion, the use of regression methods to determine higher taxa indicators is adequate and represents a good potential to be used in monitoring programs. In addition, the use of genera and families as indicators provide logistic benefits as training for monitors is less intense and expensive. Finally, the use of expected-observed comparisons to measure the quality of the evaluations can be useful for managers in order to interpret and communicate results of the scientific endeavors to the society, so they in turn can participate and help to improve and facilitate long-term monitoring at Cabo Pulmo National Park. Rev. Biol. Trop. 59 (2): 871-885. Epub 2011 June 01.

El uso de indicadores biológicos es una herramienta útil para la descripción de las comunidades y permite ahorrar recursos en programas de monitoreo. Con el fin de evaluar el potencial bioindicador de grupos taxonómicos superiores en el Parque Nacional Cabo Pulmo, México, se construyeron modelos de regresión múltiple por pasos con valores de abundancia agrupados a nivel género y familia como predictores, mediante el uso de variables dependientes, los índices ecológicos de diversidad (H’), equidad (J’) y distintividad taxonómica (Δ*). Posteriormente se compararon los resultados de los modelos contra los valores de los índices ecológicos observados en un muestreo independiente. Los resultados mostraron que todos los modelos fueron altamente significativos; los valores más altos del coeficiente de determinación se obtuvieron en las regresiones aplicadas a H’, mientras que las usadas por Δ* fueron las menos precisas. Los resultados sugieren que los modelos predictivos aquí generados son susceptibles de ser aplicados en un programa de monitoreo. Este estudio sugiere la implementación de un programa de monitoreo a largo plazo basado en bioindicadores de la estructura comunitaria de peces en el Parque Nacional Cabo Pulmo, el cual combine la precisión con la facilidad de obtención de datos.

Conservation status and spatial patterns of AGRRA vitality indices in Southwestern Atlantic Reefs

Coral reefs along the Eastern Brazilian coast extend for a distance of 800km from 12° to 18°S. They are the largest and the richest reefs of Brazil coasts, and represent the Southernmost coral reefs of the Southwestern Atlantic Ocean. Few reef surveys were performed in the 90’s in reef areas of Bahia State, particularly in the Abrolhos reef complex, in the Southernmost side of the state. A monitoring program applying the Atlantic and Gulf Rapid Reef Assessment (AGRRA) protocol was initiated in 2000, in the Abrolhos National Marine Park, after the creation of the South Tropical America (STA) Regional Node of the Global Coral Reef Monitoring Network (GCRMN) by the end of 1999. From that time up to 2005, nine reef surveys were conducted along the coast of the State of Bahia, including 26 reefs, with 95 benthic sites, 280 benthic transects, 2025 quadrats and 3537 stony corals. Eighteen of the 26 investigated reefs were assessed once and eight reefs of Abrolhos were surveyed twice to four times. The MDS ordination, analysis of similarity (ANOSIM, one way and two-way nested layouts) and similarity percentages (SIMPER) tests were applied to investigate the spatial and temporal patterns of reef vitality. Four indicators of the coral vitality: live coral cover, the density of the larger corals (colonies >20cm per reef site) and of the coral recruits (colonies<2cm per square meter), and the percentage of macroalgae indicate that the nearshore reefs, which are located less than 5km from the coast, are in poorer condition than the reefs located more than 5km off the coast. A higher density of coral colonies, lower macroalgal index, higher relative percent of turf algae and higher density of coral recruits in offshore reefs compared to the nearshore reefs are the conditions that contribute more than 80% to the dissimilarity between them. The offshore reefs are in better vital condition than the nearhore reefs and have a set of vitality indices more closely related to the Northwestern Atlantic reefs than the nearshore reef. These have been most severely impacted by the effects of direct human activities such as euthrophic waters associated with sewage pollution, higher sedimentation rates and water turbidity, inadequate use of the reefs and over exploitation of their resources. The implementation of a more effective coral reef monitoring program in Bahia is mandatory, in order to improve the strategies for protection and management efforts of the reefs. Rev. Biol. Trop. 58 (Suppl. 1): 1-31. Epub 2010 May 01.

Desde el año 2000 se inició un programa de monitoreo utilizando el protocolo AGRRA en el Parque Nacional Marino de Abrolhos en el marco de la creación del Nodo STA de la GCRMN. Entre 2000 y 2005 se realizaron varias evaluaciones en 26 arrecifes. Los patrones espaciales y temporales de la vitalidad de los arrecifes fueron estudiados mediante análisis de ordenación (MDS), similaridad (ANOSIM) y porcentajes de similaridad (SIMPER). La cobertura de coral vivo, la densidad de colonias grandes (>20cm) y de reclutas (<2cm) y la cobertura de macroalgas indicaron que los arrecifes ubicados a más de 5km de la costa presentan una mejor condición que aquellos ubicados a menos de 5km de la costa. Los arrecifes más alejados registraron una mayor densidad de colonias, un bajo índice de macroalgas, un relativo más alto porcentaje de coberturas algales y una más alta densidad de reclutas en comparación con los arrecifes más cercanos. Los arrecifes más cercanos a la costa han sido más severamente afectados por las actividades humanas. Por ejemplo, eutrofización de aguas (contaminación de aguas residuales), mayor sedimentación y turbidez del agua, mal uso de los arrecifes y sobreexplotación de sus recursos. La implementación de un programa integral de monitoreo en Bahia es urgente y obligatorio para mejorar las estrategias de protección y los esfuerzos de manejo de sus arrecifes.