Precision and accuracy of common coral reef sampling protocols revisited with photogrammetry.

The rapid decline of coral reefs calls for cost-effective benthic cover data to improve reef health forecasts, policy building, management responses and evaluation. Reef monitoring has been largely based on divers' observations along transects, and secondarily on quadrat-based protocols, video and photographic records. However, the accuracy and precision of the most common sampling approaches are not yet fully understood. Here, we compared benthic cover estimates from three common sampling protocols: Reef Check (RC), Atlantic and Gulf Rapid Reef Assessment (AGRRA) and photoquadrats (PQ). The reef cover of two contrasting sites was reconstructed with ∼450 m2 orthomosaics built with high resolution Structure-from-Motion (SfM) photogrammetry, which were used as references for comparisons among protocols. In addition, we explored sample size requirements for each protocol and provided cost-effectiveness comparisons. Our results evidenced between-reef differences in the accuracy and precision of estimates with the different protocols. The three protocols performed similarly in the reef with low macroalgal cover (<0.5%), but PQ were more accurate and precise in the reef with relatively high (∼20%) macroalgal cover. The sample size for estimating coral cover with a 20% error margin and a 0.05 significance level was lower for PQ, followed by AGRRA and RC. Considering performance, cost surrogates and equipment needs, cost-effectiveness was higher for PQ. We also discuss costs, limitations and advantages/disadvantages of SfM photogrammetry as a sampling approach for coral reef monitoring.

Incised valleys drive distinctive oceanographic processes and biological assemblages within rhodolith beds.

Continental shelves encompass gently sloped seascapes that are highly productive and intensively exploited for natural resources. Islands, reefs and other emergent or quasi-emergent features punctuate these shallow (<100 m) seascapes and are well known drivers of increased biomass and biodiversity, as well as predictors of fishing and other human uses. On the other hand, relict mesoscale geomorphological features that do not represent navigation hazards, such as incised valleys (IVs), remain poorly charted. Consequently, their role in biophysical processes remains poorly assessed and sampled. Incised valleys are common within rhodolith beds (RBs), the most extensive benthic habitat along the tropical and subtropical portions of the mid and outer Brazilian shelf. Here, we report on a multi-proxy assessment carried out in a tropical-subtropical transition region (~20°S) off Eastern Brazil, contrasting physicochemical and biological variables in IVs and adjacent RBs. Valleys interfere in near bottom circulation and function as conduits for water and propagules from the slope up to the mid shelf. In addition, they provide a stable and structurally complex habitat for black corals and gorgonians that usually occur in deeper water, contrasting sharply with the algae-dominated RB. Fish richness, abundance and biomass were also higher in the IVs, with small planktivores and large-bodied, commercially important species (e.g. groupers, snappers and grunts) presenting smaller abundances or being absent from RBs. Overall, IVs are unique and vulnerable habitats that sustain diverse assemblages and important ecosystem processes. As new IVs are detected by remote sensing or bathymetric surveys, they can be incorporated into regional marine management plans as conservation targets and priority sites for detailed in situ surveys.

Multispectral multibeam backscatter response of heterogeneous rhodolith beds.

Acoustic backscatter has been used as a tool to map the seafloor in greater detail and plays an increasingly important role in seafloor mapping to meet multiple ocean management needs. An outstanding challenge to the use of backscatter for seafloor mapping is the distinction between acoustically similar substrates, such as mixed sediments from rhodoliths. Rhodolith beds are a biogenic substrate that provides important ecological services, and are typically classified as a single categorical substrate type-though nodules coverage may be spatially variable. Recently, multispectral acoustic backscatter has demonstrated great potential to improve thematic seafloor mapping compared to single-frequency systems. This work employs multispectral multibeam backscatter and underwater imagery to characterize and map rhodolith beds in the Costa das Algas Marine Protected Area (Brazil). A support vector machine classifier was used to classify multifrequency backscatter mosaics according to rhodolith classes identified from underwater imagery. Results suggest that multispectral backscatter is effective both in providing information for mapping different proportions of rhodolith coverage and in predicting the presence or absence of these nodules. The backscatter of the lowest frequency was the most useful for distinguishing variable proportions of rhodolith coverage, and the two higher frequencies were better predictors of presence and absence.

Long-term monitoring projects of Brazilian marine and coastal ecosystems.

Biodiversity assessment is a mandatory task for sustainable and adaptive management for the next decade, and long-term ecological monitoring programs are a cornerstone for understanding changes in ecosystems. The Brazilian Long-Term Ecological Research Program (PELD) is an integrated effort model supported by public funds that finance ecological studies at 34 locations. By interviewing and compiling data from project coordinators, we assessed monitoring efforts, targeting biological groups and scientific production from nine PELD projects encompassing coastal lagoons to mesophotic reefs and oceanic islands. Reef environments and fish groups were the most often studied within the long-term projects. PELD projects covered priority areas for conservation but missed sensitive areas close to large cities, as well as underrepresenting ecosystems on the North and Northeast Brazilian coast. Long-term monitoring projects in marine and coastal environments in Brazil are recent (<5 years), not yet integrated as a network, but scientifically productive with considerable relevance for academic and human resources training. Scientific production increased exponentially with project age, despite interruption and shortage of funding during their history. From our diagnosis, we recommend some actions to fill in observed gaps, such as: enhancing projects' collaboration and integration; focusing on priority regions for new projects; broadening the scope of monitored variables; and, maintenance of funding for existing projects.

Coral growth bands recorded trace elements associated with the Fundão dam collapse.

In November 2015, the collapse of the Fundão dam (Minas Gerais, Brazil) carried over 40 × 106 m3 of iron ore tailings into the Doce river and caused massive environmental and socioeconomic impacts across the watershed. The downstream mudslide scavenged contaminants deposited in the riverbed, and several potentially toxic elements were further released through reduction and solubilization of Fe oxy-hydroxides under estuarine conditions. A turbidity plume was formed off the river mouth, but the detection of contaminants' dispersion in the ocean remains poorly assessed. This situation is specially concerning because Southwestern Atlantic's largest and richest reefs are located 70-250 km to the north of the Doce river mouth, and the legal dispute over the extent of monitoring, compensation and restoration measures are based either on indirect evidence from modeling or on direct evidence from remote sensing and contaminated organisms. Coral skeletons can incorporate trace elements and are considered good monitors of marine pollution, including inputs from open cut mining. Here, we studied a Montastraea cavernosa (Linnaeus 1767) coral colony collected 220 km northward to the river mouth, using X-rays for assessing growth bands and Laser Ablation Inductively Coupled Plasma Mass Spectrometry to recover trace elements incorporated in growth bands formed between 2014 and 2018. A threefold positive Fe anomaly was identified in early 2016, associated with negative anomalies in several elements. Variation in Ba and Y was coherent with the region's sedimentation dynamics, but also increased after 2016, akin to Pb, V and Zn. Coral growth rates decreased after the disaster. Besides validating M. cavernosa as a reliable archive of ocean chemistry, our results evidence wide-reaching sub-lethal coral contamination in the Abrolhos reefs, as well as different incorporation mechanisms into corals' skeletons.

Bryozoa from the reefs off the Amazon River mouth: checklist, thirteen new species, and notes on their ecology and distribution.

The reef system off the Amazon River mouth extends from Amapá state to Maranhão state along the Brazilian Equatorial Margin, encompassing more than 10,000 km2 of rhodolith beds and high-relief hard structures on the outer shelf and upper slope. This unique hard bottom mosaic is remarkable for being influenced by the turbid and hyposaline plume from the world's largest river, and also for representing a connectivity corridor between the Caribbean and Brazil. Bryozoans were recently recognized as major reef builders in the Southwestern Atlantic, but their diversity off the Amazon River mouth remained unknown. Here, we report on recent collections obtained from 23 to 120 m depth in Northern Brazil. Sixty-five bryozoan taxa were characterized using scanning electron microscopy, including 57, five and three taxa of Cheilostomatida, Cyclostomatida and Ctenostomatida, respectively. Cribrilaria smitti and three genera (Cranosina, Glabrilaria and Thornelya) are new records for Brazil, and 13 new species are herein described: Antropora cruzeiro n. sp., Cranosina gilbertoi n. sp., Cribrilaria lateralis n. sp., Crisia brasiliensis n. sp., Glabrilaria antoniettae n. sp., Micropora amapaensis n. sp., Parasmittina amazonensis n. sp., Plesiocleidochasma arcuatum n. sp., Poricella bifurcata n. sp., Pourtalesella duoavicularia n. sp., Stephanollona domuspusilla n. sp., Therenia dianae n. sp., and Thornelya atlanticoensis n. sp. Our results highlight the biodiversity significance of the Amazon reefs and the need for more comprehensive sampling to clarify the role of bryozoans in modern turbid-zone reefs and rhodolith beds.

Decadal (2006-2018) dynamics of Southwestern Atlantic's largest turbid zone reefs.

Tropical reefs are declining rapidly due to climate changes and local stressors such as water quality deterioration and overfishing. The so-called marginal reefs sustain significant coral cover and growth but are dominated by fewer species adapted to suboptimal conditions to most coral species. However, the dynamics of marginal systems may diverge from that of the archetypical oligotrophic tropical reefs, and it is unclear whether they are more or less susceptible to anthropogenic stress. Here, we present the largest (100 fixed quadrats at five reefs) and longest time series (13 years) of benthic cover data for Southwestern Atlantic turbid zone reefs, covering sites under contrasting anthropogenic and oceanographic forcing. Specifically, we addressed how benthic cover changed among habitats and sites, and possible dominance-shift trends. We found less temporal variation in offshore pinnacles' tops than on nearshore ones and, conversely, higher temporal fluctuation on offshore pinnacles' walls than on nearshore ones. In general, the Abrolhos reefs sustained a stable coral cover and we did not record regional-level dominance shifts favoring other organisms. However, coral decline was evidenced in one reef near a dredging disposal site. Relative abundances of longer-lived reef builders showed a high level of synchrony, which indicates that their dynamics fluctuate under similar drivers. Therefore, changes on those drivers could threaten the stability of these reefs. With the intensification of thermal anomalies and land-based stressors, it is unclear whether the Abrolhos reefs will keep providing key ecosystem services. It is paramount to restrain local stressors that contributed to coral reef deterioration in the last decades, once reversal and restoration tend to become increasingly difficult as coral reefs degrade further and climate changes escalate.

Tropical rhodolith beds are a major and belittled reef fish habitat.

Understanding habitat-level variation in community structure provides an informed basis for natural resources' management. Reef fishes are a major component of tropical marine biodiversity, but their abundance and distribution are poorly assessed beyond conventional SCUBA diving depths. Based on a baited-video survey of fish assemblages in Southwestern Atlantic's most biodiverse region we show that species composition responded mainly to the two major hard-bottom megahabitats (reefs and rhodolith beds) and to the amount of light reaching the bottom. Both megahabitats encompassed typical reef fish assemblages but, unexpectedly, richness in rhodolith beds and reefs was equivalent. The dissimilar fish biomass and trophic structure in reefs and rhodolith beds indicates that these systems function based on contrasting energy pathways, such as the much lower herbivory recorded in the latter. Rhodolith beds, the dominant benthic megahabitat in the tropical Southwestern Atlantic shelf, play an underrated role as fish habitats, and it is critical that they are considered in conservation planning.

Bryozoan framework composition in the oddly shaped reefs from Abrolhos Bank, Brazil, southwestern Atlantic: taxonomy and ecology.

Bryozoans are a key group of sessile invertebrates in some reef frameworks but are typically neglected in environmental monitoring programs. Abrolhos Bank (Brazil) is the largest reef complex in the South Atlantic Ocean, encompassing several reef landscapes over an area of 46,000 km2. A transition takes place across the shelf from mangroves to soft sediments, coastal shallow reefs to a volcanic archipelago - surrounded by fringing reefs - and unique mushroom-shaped biogenic structures, with mesophotic pinnacle reefs, rhodolith beds, sink-holes and shelf break deep environments. The taxonomic composition of the bryozoan fauna was studied in 11 core samples taken from shallow to mesophotic mid-shelf reefs (4-25 m deep) on Abrolhos Bank by divers using a submersible drill. Of the 20 bryozoan species sampled, 17 are new records for Abrolhos Bank and seven species are new to science: Crassimarginatella winstonae n. sp., Parasmittina distincta n. sp., Parasmittina abrolhosensis n. sp., Hemismittoidea asymmetrica n. sp., Stylopoma variabilis n. sp., Stylopoma hastata n. sp., and Plesiocleidochasma acuminata n. sp. (described by Ramalho, Taylor Moraes). The most conspicuous species is Celleporaria atlantica. These results increase to 48 the total number of bryozoan species known in this region and reinforce the importance of this group as one of the main components apart from crustose coralline algae and corals of the reef framework-building community of Abrolhos Bank.

Long-term effects of competition and environmental drivers on the growth of the endangered coral Mussismilia braziliensis (Verril, 1867).

Most coral reefs have recently experienced acute changes in benthic community structure, generally involving dominance shifts from slow-growing hard corals to fast-growing benthic invertebrates and fleshy photosynthesizers. Besides overfishing, increased nutrification and sedimentation are important drivers of this process, which is well documented at landscape scales in the Caribbean and in the Indo-Pacific. However, small-scale processes that occur at the level of individual organisms remain poorly explored. In addition, the generality of coral reef decline models still needs to be verified on the vast realm of turbid-zone reefs. Here, we documented the outcome of interactions between an endangered Brazilian-endemic coral (Mussismilia braziliensis) and its most abundant contacting organisms (turf, cyanobacteria, corals, crustose coralline algae and foliose macroalgae). Our study was based on a long (2006-2016) series of high resolution data (fixed photoquadrats) acquired along a cross-shelf gradient that includes coastal unprotected reefs and offshore protected sites. The study region (Abrolhos Bank) comprises the largest and richest coralline complex in the South Atlantic, and a foremost example of a turbid-zone reef system with low diversity and expressive coral cover. Coral growth was significantly different between reefs. Coral-algae contacts predominated inshore, while cyanobacteria and turf contacts dominated offshore. An overall trend in positive coral growth was detected from 2009 onward in the inshore reef, whereas retraction in live coral tissue was observed offshore during this period. Turbidity (+) and cyanobacteria (-) were the best predictors of coral growth. Complimentary incubation experiments, in which treatments of Symbiodinium spp. from M. braziliensis colonies were subjected to cyanobacterial exudates, showed a negative effect of the exudate on the symbionts, demonstrating that cyanobacteria play an important role in coral tissue necrosis. Negative effects of cyanobacteria on living coral tissue may remain undetected from percent cover estimates gathered at larger spatial scales, as these ephemeral organisms tend to be rapidly replaced by longer-living macroalgae, or complex turf-like consortia. The cross-shelf trend of decreasing turbidity and macroalgae abundance suggests either a direct positive effect of turbidity on coral growth, or an indirect effect related to the higher inshore cover of foliose macroalgae, constraining cyanobacterial abundance. It is unclear whether the higher inshore macroalgal abundance (10-20% of reef cover) is a stable phase related to a long-standing high turbidity background, or a contemporary response to anthropogenic stress. Our results challenge the idea that high macroalgal cover is always associated with compromised coral health, as the baselines for turbid zone reefs may derive sharply from those of coral-dominated reefs that dwell under oligotrophic conditions.

Bryozoans are Major Modern Builders of South Atlantic Oddly Shaped Reefs.

In major modern reef regions, either in the Indo-Pacific or the Caribbean, scleractinian corals are described as the main reef framework builders, often associated with crustose coralline algae. We used underwater cores to investigate Late Holocene reef growth and characterise the main framework builders in the Abrolhos Shelf, the largest and richest modern tropical reef complex in the South Western Atlantic, a scientifically underexplored reef province. Rather than a typical coralgal reef, our results show a complex framework building system dominated by bryozoans. Bryozoans were major components in all cores and age intervals (2,000 yrs BP), accounting for up to 44% of the reef framework, while crustose coralline algae and coral accounted for less than 28 and 23%, respectively. Reef accretion rates varied from 2.7 to 0.9 mm yr-1, which are similar to typical coralgal reefs. Bryozoan functional groups encompassed 20 taxa and Celleporaria atlantica (Busk, 1884) dominated the framework at all cores. While the prevalent mesotrophic conditions may have driven suspension-feeders' dominance over photoautotrophs and mixotrophs, we propose that a combination of historical factors with the low storm-disturbance regime of the tropical South Atlantic also contributed to the region's low diversity, and underlies the unique mushroom shape of the Abrolhos pinnacles.

A habitat-based approach to predict impacts of marine protected areas on fishers.

Although marine protected areas can simultaneously contribute to biodiversity conservation and fisheries management, the global network is biased toward particular ecosystem types because they have been established primarily in an ad hoc fashion. The optimization of trade-offs between biodiversity benefits and socioeconomic values increases success of protected areas and minimizes enforcement costs in the long run, but it is often neglected in marine spatial planning (MSP). Although the acquisition of spatially explicit socioeconomic data is perceived as a costly or secondary step in MSP, it is critical to account for lost opportunities by people whose activities will be restricted, especially fishers. We developed an easily reproduced habitat-based approach to estimate the spatial distribution of opportunity cost to fishers in data-poor regions. We assumed the most accessible areas have higher economic and conservation values than less accessible areas and their designation as no-take zones represents a loss of fishing opportunities. We estimated potential distribution of fishing resources from bathymetric ranges and benthic habitat distribution and the relative importance of the different resources for each port of total catches, revenues, and stakeholder perception. In our model, we combined different cost layers to produce a comprehensive cost layer so that we could evaluate of trade-offs. Our approach directly supports conservation planning, can be applied generally, and is expected to facilitate stakeholder input and community acceptance of conservation.

An extensive reef system at the Amazon River mouth.

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 × 10(6)-km(2) 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 km(2)) 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.

Neotropical forest expansion during the last glacial period challenges refuge hypothesis.

The forest refuge hypothesis (FRH) has long been a paradigm for explaining the extreme biological diversity of tropical forests. According to this hypothesis, forest retraction and fragmentation during glacial periods would have promoted reproductive isolation and consequently speciation in forest patches (ecological refuges) surrounded by open habitats. The recent use of paleoclimatic models of species and habitat distributions revitalized the FRH, not by considering refuges as the main drivers of allopatric speciation, but instead by suggesting that high contemporary diversity is associated with historically stable forest areas. However, the role of the emerged continental shelf on the Atlantic Forest biodiversity hotspot of eastern South America during glacial periods has been ignored in the literature. Here, we combined results of species distribution models with coalescent simulations based on DNA sequences to explore the congruence between scenarios of forest dynamics through time and the genetic structure of mammal species cooccurring in the central region of the Atlantic Forest. Contrary to the FRH predictions, we found more fragmentation of suitable habitats during the last interglacial (LIG) and the present than in the last glacial maximum (LGM), probably due to topography. We also detected expansion of suitable climatic conditions onto the emerged continental shelf during the LGM, which would have allowed forests and forest-adapted species to expand. The interplay of sea level and land distribution must have been crucial in the biogeographic history of the Atlantic Forest, and forest refuges played only a minor role, if any, in this biodiversity hotspot during glacial periods.

Baseline Assessment of Mesophotic Reefs of the Vitória-Trindade Seamount Chain Based on Water Quality, Microbial Diversity, Benthic Cover and Fish Biomass Data.

Seamounts are considered important sources of biodiversity and minerals. However, their biodiversity and health status are not well understood; therefore, potential conservation problems are unknown. The mesophotic reefs of the Vitória-Trindade Seamount Chain (VTC) were investigated via benthic community and fish surveys, metagenomic and water chemistry analyses, and water microbial abundance estimations. The VTC is a mosaic of reef systems and includes fleshy algae dominated rhodolith beds, crustose coralline algae (CCA) reefs, and turf algae dominated rocky reefs of varying health levels. Macro-carnivores and larger fish presented higher biomass at the CCA reefs (4.4 kg per frame) than in the rhodolith beds and rocky reefs (0.0 to 0.1 kg per frame). A larger number of metagenomic sequences identified as primary producers (e.g., Chlorophyta and Streptophyta) were found at the CCA reefs. However, the rocky reefs contained more diseased corals (>90%) than the CCA reefs (~40%) and rhodolith beds (~10%). Metagenomic analyses indicated a heterotrophic and fast-growing microbiome in rocky reef corals that may possibly lead to unhealthy conditions possibly enhanced by environmental features (e.g. light stress and high loads of labile dissolved organic carbon). VTC mounts represent important hotspots of biodiversity that deserve further conservation actions.

Dynamics of coral reef benthic assemblages of the Abrolhos Bank, eastern Brazil: inferences on natural and anthropogenic drivers.

The Abrolhos Bank (eastern Brazil) encompasses the largest and richest coral reefs of the South Atlantic. Coral reef benthic assemblages of the region were monitored from 2003 to 2008. Two habitats (pinnacles' tops and walls) were sampled per site with 3-10 sites sampled within different reef areas. Different methodologies were applied in two distinct sampling periods: 2003-2005 and 2006-2008. Spatial coverage and taxonomic resolution were lower in the former than in the latter period. Benthic assemblages differed markedly in the smallest spatial scale, with greater differences recorded between habitats. Management regimes and biomass of fish functional groups (roving and territorial herbivores) had minor influences on benthic assemblages. These results suggest that local environmental factors such as light, depth and substrate inclination exert a stronger influence on the structure of benthic assemblages than protection from fishing. Reef walls of unprotected coastal reefs showed highest coral cover values, with a major contribution of Montastraea cavernosa (a sediment resistant species that may benefit from low light levels). An overall negative relationship between fleshy macroalgae and slow-growing reef-building organisms (i.e. scleractinians and crustose calcareous algae) was recorded, suggesting competition between these organisms. The opposite trend (i.e. positive relationships) was recorded for turf algae and the two reef-building organisms, suggesting beneficial interactions and/or co-occurrence mediated by unexplored factors. Turf algae cover increased across the region between 2006 and 2008, while scleractinian cover showed no change. The need of a continued and standardized monitoring program, aimed at understanding drivers of change in community patterns, as well as to subsidize sound adaptive conservation and management measures, is highlighted.

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 world's 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 km(2). Distribution, extent, composition and structure of this bed were assessed with side scan sonar, remotely operated vehicles, and SCUBA. The mean rate of CaCO(3) 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 world's largest biogenic CaCO(3) 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.