Spatial scales of bacterial diversity in cold-water coral reef ecosystems

Background

Cold-water coral reef ecosystems are recognized as biodiversity hotspots in the deep sea, but insights into their associated bacterial communities are still limited. Deciphering principle patterns of bacterial community variation over multiple spatial scales may however prove critical for a better understanding of factors contributing to cold-water coral reef stability and functioning.

Methodology/Principal Findings

Bacterial community structure, as determined by Automated Ribosomal Intergenic Spacer Analysis (ARISA), was investigated with respect to (i) microbial habitat type and (ii) coral species and color, as well as the three spatial components (iii) geomorphologic reef zoning, (iv) reef boundary, and (v) reef location. Communities revealed fundamental differences between coral-generated (branch surface, mucus) and ambient microbial habitats (seawater, sediments). This habitat specificity appeared pivotal for determining bacterial community shifts over all other study levels investigated. Coral-derived surfaces showed species-specific patterns, differing significantly between Lophelia pertusa and Madrepora oculata, but not between L. pertusa color types. Within the reef center, no community distinction corresponded to geomorphologic reef zoning for both coral-generated and ambient microbial habitats. Beyond the reef center, however, bacterial communities varied considerably from local to regional scales, with marked shifts toward the reef periphery as well as between different in- and offshore reef sites, suggesting significant biogeographic imprinting but weak microbe-host specificity.

Conclusions/Significance

This study presents the first multi-scale survey of bacterial diversity in cold-water coral reefs, spanning a total of five observational levels including three spatial scales. It demonstrates that bacterial communities in cold-water coral reefs are structured by multiple factors acting at different spatial scales, which has fundamental implications for the monitoring of microbial diversity and function in those ecosystems.     

Coping with Commitment: Projected Thermal Stress on Coral Reefs under Different Future Scenarios

Background

Periods of anomalously warm ocean temperatures can lead to mass coral bleaching. Past studies have concluded that anthropogenic climate change may rapidly increase the frequency of these thermal stress events, leading to declines in coral cover, shifts in the composition of corals and other reef-dwelling organisms, and stress on the human populations who depend on coral reef ecosystems for food, income and shoreline protection. The ability of greenhouse gas mitigation to alter the near-term forecast for coral reefs is limited by the time lag between greenhouse gas emissions and the physical climate response.

Methodology/Principal Findings

This study uses observed sea surface temperatures and the results of global climate model forced with five different future emissions scenarios to evaluate the “committed warming” for coral reefs worldwide. The results show that the physical warming commitment from current accumulation of greenhouse gases in the atmosphere could cause over half of the world''s coral reefs to experience harmfully frequent (p≥0.2 year⁻¹) thermal stress by 2080. An additional “societal” warming commitment, caused by the time required to shift from a business-as-usual emissions trajectory to a 550 ppm CO₂ stabilization trajectory, may cause over 80% of the world''s coral reefs to experience harmfully frequent events by 2030. Thermal adaptation of 1.5°C would delay the thermal stress forecast by 50–80 years.

Conclusions/Significance

The results suggest that adaptation – via biological mechanisms, coral community shifts and/or management interventions – could provide time to change the trajectory of greenhouse gas emissions and possibly avoid the recurrence of harmfully frequent events at the majority (97%) of the world''s coral reefs this century. Without any thermal adaptation, atmospheric CO₂ concentrations may need to be stabilized below current levels to avoid the degradation of coral reef ecosystems from frequent thermal stress events.     

Variable Responses of Benthic Communities to Anomalously Warm Sea Temperatures on a High-Latitude Coral Reef

High-latitude reefs support unique ecological communities occurring at the biogeographic boundaries between tropical and temperate marine ecosystems. Due to their lower ambient temperatures, they are regarded as potential refugia for tropical species shifting poleward due to rising sea temperatures. However, acute warming events can cause rapid shifts in the composition of high-latitude reef communities, including range contractions of temperate macroalgae and bleaching-induced mortality in corals. While bleaching has been reported on numerous high-latitude reefs, post-bleaching trajectories of benthic communities are poorly described. Consequently, the longer-term effects of thermal anomalies on high-latitude reefs are difficult to predict. Here, we use an autonomous underwater vehicle to conduct repeated surveys of three 625 m² plots on a coral-dominated high-latitude reef in the Houtman Abrolhos Islands, Western Australia, over a four-year period spanning a large-magnitude thermal anomaly. Quantification of benthic communities revealed high coral cover (>70%, comprising three main morphospecies) prior to the bleaching event. Plating Montipora was most susceptible to bleaching, but in the plot where it was most abundant, coral cover did not change significantly because of post-bleaching increases in branching Acropora. In the other two plots, coral cover decreased while macroalgal cover increased markedly. Overall, coral cover declined from 73% to 59% over the course of the study, while macroalgal cover increased from 11% to 24%. The significant differences in impacts and post-bleaching trajectories among plots underline the importance of understanding the underlying causes of such variation to improve predictions of how climate change will affect reefs, especially at high-latitudes.     

Turning up the Heat: Increasing Temperature and Coral Bleaching at the High Latitude Coral Reefs of the Houtman Abrolhos Islands

Background

Coral reefs face increasing pressures particularly when on the edge of their distributions. The Houtman Abrolhos Islands (Abrolhos) are the southernmost coral reef system in the Indian Ocean, and one of the highest latitude reefs in the world. These reefs have a unique mix of tropical and temperate marine fauna and flora and support 184 species of coral, dominated by Acropora species. A significant La Niña event during 2011 produced anomalous conditions of increased temperature along the whole Western Australian coastline, producing the first-recorded widespread bleaching of corals at the Abrolhos.

Methodology/ Principal Findings

We examined long term trends in the marine climate at the Abrolhos using historical sea surface temperature data (HadISST data set) from 1900–2011. In addition in situ water temperature data for the Abrolhos (from data loggers installed in 2008, across four island groups) were used to determine temperature exposure profiles. Coupled with the results of coral cover surveys conducted annually since 2007; we calculated bleaching thresholds for monitoring sites across the four Abrolhos groups.

Conclusions/ Significance

In situ temperature data revealed maximum daily water temperatures reached 29.54°C in March 2011 which is 4.2°C above mean maximum daily temperatures (2008–2010). The level of bleaching varied across sites with an average of ∼12% of corals bleached. Mortality was high, with a mean ∼50% following the 2011 bleaching event. Prior to 2011, summer temperatures reached a mean (across all monitoring sites) of 25.1°C for 2.5 days. However, in 2011 temperatures reached a mean of 28.1°C for 3.3 days. Longer term trends (1900–2011) showed mean annual sea surface temperatures increase by 0.01°C per annum. Long-term temperature data along with short-term peaks in 2011, outline the potential for corals to be exposed to more frequent bleaching risk with consequences for this high latitude coral reef system at the edge of its distribution.     

Predicting the Location and Spatial Extent of Submerged Coral Reef Habitat in the Great Barrier Reef World Heritage Area,Australia

Aim

Coral reef communities occurring in deeper waters have received little research effort compared to their shallow-water counterparts, and even such basic information as their location and extent are currently unknown throughout most of the world. Using the Great Barrier Reef as a case study, habitat suitability modelling is used to predict the distribution of deep-water coral reef communities on the Great Barrier Reef, Australia. We test the effectiveness of a range of geophysical and environmental variables for predicting the location of deep-water coral reef communities on the Great Barrier Reef.

Location

Great Barrier Reef, Australia.

Methods

Maximum entropy modelling is used to identify the spatial extent of two broad communities of habitat-forming megabenthos phototrophs and heterotrophs. Models were generated using combinations of geophysical substrate properties derived from multibeam bathymetry and environmental data derived from Bio-ORACLE, combined with georeferenced occurrence records of mesophotic coral communities from autonomous underwater vehicle, remotely operated vehicle and SCUBA surveys. Model results are used to estimate the total amount of mesophotic coral reef habitat on the GBR.

Results

Our models predict extensive but previously undocumented coral communities occurring both along the continental shelf-edge of the Great Barrier Reef and also on submerged reefs inside the lagoon. Habitat suitability for phototrophs is highest on submerged reefs along the outer-shelf and the deeper flanks of emergent reefs inside the GBR lagoon, while suitability for heterotrophs is highest in the deep waters along the shelf-edge. Models using only geophysical variables consistently outperformed models incorporating environmental data for both phototrophs and heterotrophs.

Main Conclusion

Extensive submerged coral reef communities that are currently undocumented are likely to occur throughout the Great Barrier Reef. High-quality bathymetry data can be used to identify these reefs, which may play an important role in resilience of the GBR ecosystem to climate change.     

Impact of Herbivore Identity on Algal Succession and Coral Growth on a Caribbean Reef

Background

Herbivory is an important top-down force on coral reefs that regulates macroalgal abundance, mediates competitive interactions between macroalgae and corals, and provides resilience following disturbances such as hurricanes and coral bleaching. However, reductions in herbivore diversity and abundance via disease or over-fishing may harm corals directly and may indirectly increase coral susceptibility to other disturbances.

Methodology and Principal Findings

In two experiments over two years, we enclosed equivalent densities and masses of either single-species or mixed-species of herbivorous fishes in replicate, 4 m² cages at a depth of 17 m on a reef in the Florida Keys, USA to evaluate the effects of herbivore identity and species richness on colonization and development of macroalgal communities and the cascading effects of algae on coral growth. In Year 1, we used the redband parrotfish (Sparisoma aurofrenatum) and the ocean surgeonfish (Acanthurus bahianus); in Year 2, we used the redband parrotfish and the princess parrotfish (Scarus taeniopterus). On new substrates, rapid grazing by ocean surgeonfish and princess parrotfish kept communities in an early successional stage dominated by short, filamentous algae and crustose coralline algae that did not suppress coral growth. In contrast, feeding by redband parrotfish allowed an accumulation of tall filaments and later successional macroalgae that suppressed coral growth. These patterns contrast with patterns from established communities not undergoing primary succession; on established substrates redband parrotfish significantly reduced upright macroalgal cover while ocean surgeonfish and princess parrotfish allowed significant increases in late successional macroalgae.

Significance

This study further highlights the importance of biodiversity in affecting ecosystem function in that different species of herbivorous fishes had very different impacts on reef communities depending on the developmental stage of the community. The species-specific effects of herbivorous fishes suggest that a species-rich herbivore fauna can be critical in providing the resilience that reefs need for recovery from common disturbances such as coral bleaching and storm damage.     

Unprecedented Mass Bleaching and Loss of Coral across 12° of Latitude in Western Australia in 2010–11

Background

Globally, coral bleaching has been responsible for a significant decline in both coral cover and diversity over the past two decades. During the summer of 2010–11, anomalous large-scale ocean warming induced unprecedented levels of coral bleaching accompanied by substantial storminess across more than 12° of latitude and 1200 kilometers of coastline in Western Australia (WA).

Methodology/Principal Findings

Extreme La-Niña conditions caused extensive warming of waters and drove considerable storminess and cyclonic activity across WA from October 2010 to May 2011. Satellite-derived sea surface temperature measurements recorded anomalies of up to 5°C above long-term averages. Benthic surveys quantified the extent of bleaching at 10 locations across four regions from tropical to temperate waters. Bleaching was recorded in all locations across regions and ranged between 17% (±5.5) in the temperate Perth region, to 95% (±3.5) in the Exmouth Gulf of the tropical Ningaloo region. Coincident with high levels of bleaching, three cyclones passed in close proximity to study locations around the time of peak temperatures. Follow-up surveys revealed spatial heterogeneity in coral cover change with four of ten locations recording significant loss of coral cover. Relative decreases ranged between 22%–83.9% of total coral cover, with the greatest losses in the Exmouth Gulf.

Conclusions/Significance

The anomalous thermal stress of 2010–11 induced mass bleaching of corals along central and southern WA coral reefs. Significant coral bleaching was observed at multiple locations across the tropical-temperate divide spanning more than 1200 km of coastline. Resultant spatially patchy loss of coral cover under widespread and high levels of bleaching and cyclonic activity, suggests a degree of resilience for WA coral communities. However, the spatial extent of bleaching casts some doubt over hypotheses suggesting that future impacts to coral reefs under forecast warming regimes may in part be mitigated by southern thermal refugia.     

Fatty acid composition indicating diverse habitat use in coral reef fishes in the Malaysian South China Sea

Background

In order to understand feeding ecology and habitat use of coral reef fish, fatty acid composition was examined in five coral reef fishes, Thalassoma lunare, Lutjanus lutjanus, Abudefduf bengalensis, Scarus rivulatus and Scolopsis affinis collected in the Bidong Island of Malaysian South China Sea.

Results

Proportions of saturated fatty acids (SAFA) ranged 57.2% 74.2%, with the highest proportions in fatty acids, the second highest was monounsaturated fatty acids (MUFA) ranged from 21.4% to 39.0% and the proportion of polyunsaturated fatty acids (PUFA) was the lowest ranged from 2.8% to 14.1%. Each fatty acid composition differed among fishes, suggesting diverse feeding ecology, habitat use and migration during the fishes’ life history in the coral reef habitats.

Conclusions

Diets of the coral fish species might vary among species in spite of that each species are living sympatrically. Differences in fatty acid profiles might not just be considered with respect to the diets, but might be based on the habitat and migration.     

Declining coral skeletal extension for forereef colonies of Siderastrea siderea on the Mesoamerican Barrier Reef System, Southern Belize

Background

Natural and anthropogenic stressors are predicted to have increasingly negative impacts on coral reefs. Understanding how these environmental stressors have impacted coral skeletal growth should improve our ability to predict how they may affect coral reefs in the future. We investigated century-scale variations in skeletal extension for the slow-growing massive scleractinian coral Siderastrea siderea inhabiting the forereef, backreef, and nearshore reefs of the Mesoamerican Barrier Reef System (MBRS) in the western Caribbean Sea.

Methodology/Principal Findings

Thirteen S. siderea cores were extracted, slabbed, and X-rayed. Annual skeletal extension was estimated from adjacent low- and high-density growth bands. Since the early 1900s, forereef S. siderea colonies have shifted from exhibiting the fastest to the slowest average annual skeletal extension, while values for backreef and nearshore colonies have remained relatively constant. The rates of change in annual skeletal extension were −0.020±0.005, 0.011±0.006, and −0.008±0.006 mm yr⁻¹ per year [mean±SE] for forereef, backreef, and nearshore colonies respectively. These values for forereef and nearshore S. siderea were significantly lower by 0.031±0.008 and by 0.019±0.009 mm yr⁻¹ per year, respectively, than for backreef colonies. However, only forereef S. siderea exhibited a statistically significant decline in annual skeletal extension over the last century.

Conclusions/Significance

Our results suggest that forereef S. siderea colonies are more susceptible to environmental stress than backreef and nearshore counterparts, which may have historically been exposed to higher natural baseline stressors. Alternatively, sediment plumes, nutrients, and pollution originating from watersheds of Guatemala and Honduras may disproportionately impact the forereef environment of the MBRS. We are presently reconstructing the history of environmental stressors that have impacted the MBRS to constrain the cause(s) of the observed reductions in coral skeletal growth. This should improve our ability to predict and potentially mitigate the effects of future environmental stressors on coral reef ecosystems.     

Resilience of Coral-Associated Bacterial Communities Exposed to Fish Farm Effluent

Background

The coral holobiont includes the coral animal, algal symbionts, and associated microbial community. These microbes help maintain the holobiont homeostasis; thus, sustaining robust mutualistic microbial communities is a fundamental part of long-term coral reef survival. Coastal pollution is one major threat to reefs, and intensive fish farming is a rapidly growing source of this pollution.

Methodology & Principal Findings

We investigated the susceptibility and resilience of the bacterial communities associated with a common reef-building coral, Porites cylindrica, to coastal pollution by performing a clonally replicated transplantation experiment in Bolinao, Philippines adjacent to intensive fish farming. Ten fragments from each of four colonies (total of 40 fragments) were followed for 22 days across five sites: a well-flushed reference site (the original fragment source); two sites with low exposure to milkfish (Chanos chanos) aquaculture effluent; and two sites with high exposure. Elevated levels of dissolved organic carbon (DOC), chlorophyll a, total heterotrophic and autotrophic bacteria abundance, virus like particle (VLP) abundances, and culturable Vibrio abundance characterized the high effluent sites. Based on 16S rRNA clone libraries and denaturing gradient gel electrophoresis (DGGE) analysis, we observed rapid, dramatic changes in the coral-associated bacterial communities within five days of high effluent exposure. The community composition on fragments at these high effluent sites shifted towards known human and coral pathogens (i.e. Arcobacter, Fusobacterium, and Desulfovibrio) without the host corals showing signs of disease. The communities shifted back towards their original composition by day 22 without reduction in effluent levels.

Significance

This study reveals fish farms as a likely source of pathogens with the potential to proliferate on corals and an unexpected short-term resilience of coral-associated bacterial communities to eutrophication pressure. These data highlight a need for improved aquaculture practices that can achieve both sustainable industry goals and long-term coral reef survival.     

Nitrogen Biogeochemistry in the Caribbean Sponge,Xestospongia muta: A Source or Sink of Dissolved Inorganic Nitrogen?

Background

Sponges have long been known to be ecologically important members of the benthic fauna on coral reefs. Recently, it has been shown that sponges are also important contributors to the nitrogen biogeochemistry of coral reefs. The studies that have been done show that most sponges are net sources of dissolved inorganic nitrogen (DIN; NH₄ ⁺ and NO₃ ⁻) and that nitrification, mediated by their symbiotic prokaryotes, is the primary process involved in supplying DIN to adjacent reefs.

Methodology/Principal Findings

A natural experiment was conducted with the Caribbean sponge Xestospongia muta from three different locations (Florida Keys, USA; Lee Stocking Island, Bahamas and Little Cayman, Cayman Islands). The DIN fluxes of sponges were studied using nutrient analysis, stable isotope ratios, and isotope tracer experiments. Results showed that the fluxes of DIN were variable between locations and that X. muta can be either a source or sink of DIN. Stable isotope values of sponge and symbiotic bacterial fractions indicate that the prokaryotic community is capable of taking up both NH₄ ⁺ and NO₃ ⁻ while the differences in δ ¹⁵N between the sponge and bacterial fractions from the NH₄ ⁺ tracer experiment suggest that there is translocation of labeled N from the symbiotic bacteria to the host.

Conclusions/Significance

Nitrogen cycling in X. muta appears to be more complex than previous studies have shown and our results suggest that anaerobic processes such as denitrification or anammox occur in these sponges in addition to aerobic nitrification. Furthermore, the metabolism of this sponge and its prokaryotic symbionts may have a significant impact on the nitrogen biogeochemistry on Caribbean coral reefs by releasing large amounts of DIN, including higher NH₄ ⁺ concentrations that previously reported.     

Effects of light, food availability and temperature stress on the function of photosystem II and photosystem I of coral symbionts

Background

Reef corals are heterotrophic coelenterates that achieve high productivity through their photosynthetic dinoflagellate symbionts. Excessive seawater temperature destabilises this symbiosis and causes corals to “bleach,” lowering their photosynthetic capacity. Bleaching poses a serious threat to the persistence of coral reefs on a global scale. Despite expanding research on the causes of bleaching, the mechanisms remain a subject of debate.

Methodology/Principal Findings

This study determined how light and food availability modulate the effects of temperature stress on photosynthesis in two reef coral species. We quantified the activities of Photosystem II, Photosystem I and whole chain electron transport under combinations of normal and stressful growth temperatures, moderate and high light levels and the presence or absence of feeding of the coral hosts. Our results show that PS1 function is comparatively robust against temperature stress in both species, whereas PS2 and whole chain electron transport are susceptible to temperature stress. In the symbiotic dinoflagellates of Stylophora pistillata the contents of chlorophyll and major photosynthetic complexes were primarily affected by food availability. In Turbinaria reniformis growth temperature was the dominant influence on the contents of the photosynthetic complexes. In both species feeding the host significantly protected photosynthetic function from high temperature stress.

Conclusions/Significance

Our findings support the photoinhibition model of coral bleaching and demonstrate that PS1 is not a major site for thermal damage during bleaching events. Feeding mitigates bleaching in two scleractinian corals, so that reef responses to temperature stresses will likely be influenced by the coinciding availabilities of prey for the host.     

Phylogenetic relationships among NE Atlantic Plocamionida Topsent (1927) (Porifera, Poecilosclerida): under-estimated diversity in reef ecosystems

Background

Small and cryptic sponges associated with cold-water coral reefs are particularly numerous and challenging to identify, but their ecological and biochemical importance is likely to compete with megabenthic specimens.

Methodology/Principal Findings

Here we use a combination of the standard M1M6 and I3M11 partitions of the COI fragment, partial rDNA 28S sequences and morphology to delineate small encrusting Plocamionida species. In total, 46 specimens were retrieved from seven shallow to deep-water coral locations, crossing 3,000 km along the European margins. Our work provides evidence that the Plocamionida ambigua f. tylotata and f. grandichelata can be considered valid species, whereas Plocamionida ambigua f. tornata corresponds to the species P. ambigua. Within the monophyletic group of Plocamionida, P. microcionides is shown as really divergent from the other taxa, and four putative new Plocamionida species are suggested.

Conclusions/Significance

This study shows that the use of molecular and morphological information in an integrative approach is a powerful tool for the identification of sponge species, and suggests that an under-estimated biodiversity of sponges occurs in cold-water coral reefs.     

Prioritizing Land and Sea Conservation Investments to Protect Coral Reefs

Background

Coral reefs have exceptional biodiversity, support the livelihoods of millions of people, and are threatened by multiple human activities on land (e.g. farming) and in the sea (e.g. overfishing). Most conservation efforts occur at local scales and, when effective, can increase the resilience of coral reefs to global threats such as climate change (e.g. warming water and ocean acidification). Limited resources for conservation require that we efficiently prioritize where and how to best sustain coral reef ecosystems.

Methodology/Principal Findings

Here we develop the first prioritization approach that can guide regional-scale conservation investments in land- and sea-based conservation actions that cost-effectively mitigate threats to coral reefs, and apply it to the Coral Triangle, an area of significant global attention and funding. Using information on threats to marine ecosystems, effectiveness of management actions at abating threats, and the management and opportunity costs of actions, we calculate the rate of return on investment in two conservation actions in sixteen ecoregions. We discover that marine conservation almost always trumps terrestrial conservation within any ecoregion, but terrestrial conservation in one ecoregion can be a better investment than marine conservation in another. We show how these results could be used to allocate a limited budget for conservation and compare them to priorities based on individual criteria.

Conclusions/Significance

Previous prioritization approaches do not consider both land and sea-based threats or the socioeconomic costs of conserving coral reefs. A simple and transparent approach like ours is essential to support effective coral reef conservation decisions in a large and diverse region like the Coral Triangle, but can be applied at any scale and to other marine ecosystems.     

Harnessing Natural Recovery Processes to Improve Restoration Outcomes: An Experimental Assessment of Sponge-Mediated Coral Reef Restoration

Background

Restoration is increasingly implemented to reestablish habitat structure and function following physical anthropogenic disturbance, but scientific knowledge of effectiveness of methods lags behind demand for guidelines. On coral reefs, recovery is largely dependent on coral reestablishment, and substratum stability is critical to the survival of coral fragments and recruits. Concrete is often used to immobilize rubble, but its ecological performance has not been rigorously evaluated, and restoration has generally fallen short of returning degraded habitat to pre-disturbance conditions. Fragments of erect branching sponges mediate reef recovery by facilitating rubble consolidation, yet such natural processes have been largely overlooked in restoring reefs.

Methods

On two reefs in Curacao, four treatments - coral rubble alone, rubble seeded with sponge fragments, rubble bound by concrete, and concrete “rubble” bound by concrete - were monitored over four years to investigate rubble consolidation with and without sponges and the ecological performance of treatments in terms of the number and diversity of coral recruits. Species specific rates of sponge fragment attachment to rubble, donor sponge growth and tissue replacement, and fragment survival inside rubble piles were also investigated to evaluate sponge species performance and determine rates for sustainably harvesting tissue.

Findings/Significance

Rubble piles seeded with sponges retained height and shape to a significantly greater degree, lost fewer replicates to water motion, and were significantly more likely to be consolidated over time than rubble alone. Significantly more corals recruited to sponge-seeded rubble than to all other treatments. Coral diversity was also greatest for rubble with sponges and it was the only treatment to which framework building corals recruited. Differences in overall sponge species performance suggest species selection is important to consider. Employing organisms that jump start successional pathways and facilitate recovery can significantly improve restoration outcomes; however, best practices require techniques be tailored to each system.     

Diversity Partitioning of Stony Corals Across Multiple Spatial Scales Around Zanzibar Island,Tanzania

Background

The coral reefs of Zanzibar Island (Unguja, Tanzania) encompass a considerable proportion of the global coral-reef diversity and are representative of the western Indian Ocean region. Unfortunately, these reefs have been recently subjected to local and regional disturbances. The objectives of this study were to determine whether there are potentially non-random processes forcing the observed coral diversity patterns, and highlight where and at which spatial scales these processes might be most influential.

Methodology/Principal Findings

A hierarchical (nested) sampling design was employed across three spatial scales, ranging from transects (≤20 m), stations (<100 m), to sites (<1000 m), to examine coral diversity patterns. Two of the four sites, Chumbe and Mnemba, were located within Marine Protected Areas (MPAs), while the other two sites, Changuu and Bawe, were not protected. Additive partitioning of coral diversity was used to separate regional (total) diversity (γ) into local α diversity and among-sample β diversity components. Individual-based null models were used to identify deviations from random distribution across the three spatial scales. We found that Chumbe and Mnemba had similar diversity components to those predicted by the null models. However, the diversity at Changuu and Bawe was lower than expected at all three spatial scales tested. Consequently, the relative contribution of the among-site diversity component was significantly greater than expected. Applying partitioning analysis for each site separately revealed that the within-transect diversity component in Changuu was significantly lower than the null expectation.

Conclusions/Significance

The non-random outcome of the partitioning analyses helped to identify the among-sites scale (i.e., 10''s of kilometers) and the within-transects scale (i.e., a few meters; especially at Changuu) as spatial boundaries within which to examine the processes that may interact and disproportionately differentiate coral diversity. In light of coral community compositions and diversity patterns we strongly recommend that Bawe be declared a MPA.     

Co-occurrence of herbivorous fish functional groups correlates with enhanced coral reef benthic state

Aim

Biodiversity loss is impacting essential ecosystem functions and services across the globe. Recently, our interest in the benefits of biodiversity for ecosystem function has shifted focus from measurements of species richness to functional diversity and composition. However, the additional importance of other community characteristics, such as species evenness and co-occurrence, for diversity-driven ecosystem function is less known. We used herbivorous coral reef fish as a model system to investigate how co-occurrence of different functional groups, rather than purely functional diversity, within an assemblage might affect the coral reef benthic state.

Location

Western Atlantic.

Time period

2007–2017.

Major taxa studied

Herbivorous reef fish.

Methods

We analysed benthic and fish assemblage data from 601 sites across 12 countries in the western Atlantic. Using diversity–interaction models, we investigated how the composition and relative abundances of reef fish functional groups were correlated with benthic cover and estimates of coral calcification rates. We used statistical interactions to explore the importance of co-occurrence of herbivorous fish functional groups for the coral reef benthic state.

Results

We found that co-occurrence of herbivorous fish functional groups, in addition to functional diversity, was correlated with reduced algal cover and increased coral accretion. Moreover, pairwise statistical interactions between functional groups were significantly correlated with an improvement in the coral reef benthic state.

Main conclusions

Our results support the idea that functional group co-occurrence, in addition to functional diversity, within herbivorous fish offers additional benefits to the coral reef benthic state. We identify farming damselfish and excavating parrotfish as potential key determinants of the coral reef benthic state and highlight that co-occurrence of cropping and scraping herbivores might promote coral accretion. Our findings support the argument that protecting herbivore abundance without regard to the species and functional groups present is not enough to preserve coral reef health and that fine-scale community composition must be considered.     

Severe 2010 cold-water event caused unprecedented mortality to corals of the Florida reef tract and reversed previous survivorship patterns

Background

Coral reefs are facing increasing pressure from natural and anthropogenic stressors that have already caused significant worldwide declines. In January 2010, coral reefs of Florida, United States, were impacted by an extreme cold-water anomaly that exposed corals to temperatures well below their reported thresholds (16°C), causing rapid coral mortality unprecedented in spatial extent and severity.

Methodology/Principal Findings

Reef surveys were conducted from Martin County to the Lower Florida Keys within weeks of the anomaly. The impacts recorded were catastrophic and exceeded those of any previous disturbances in the region. Coral mortality patterns were directly correlated to in-situ and satellite-derived cold-temperature metrics. These impacts rival, in spatial extent and intensity, the impacts of the well-publicized warm-water bleaching events around the globe. The mean percent coral mortality recorded for all species and subregions was 11.5% in the 2010 winter, compared to 0.5% recorded in the previous five summers, including years like 2005 where warm-water bleaching was prevalent. Highest mean mortality (15%–39%) was documented for inshore habitats where temperatures were <11°C for prolonged periods. Increases in mortality from previous years were significant for 21 of 25 coral species, and were 1–2 orders of magnitude higher for most species.

Conclusions/Significance

The cold-water anomaly of January 2010 caused the worst coral mortality on record for the Florida Reef Tract, highlighting the potential catastrophic impacts that unusual but extreme climatic events can have on the persistence of coral reefs. Moreover, habitats and species most severely affected were those found in high-coral cover, inshore, shallow reef habitats previously considered the “oases” of the region, having escaped declining patterns observed for more offshore habitats. Thus, the 2010 cold-water anomaly not only caused widespread coral mortality but also reversed prior resistance and resilience patterns that will take decades to recover.     

Cell Turnover and Detritus Production in Marine Sponges from Tropical and Temperate Benthic Ecosystems

This study describes in vivo cell turnover (the balance between cell proliferation and cell loss) in eight marine sponge species from tropical coral reef, mangrove and temperate Mediterranean reef ecosystems. Cell proliferation was determined through the incorporation of 5-bromo-2′-deoxyuridine (BrdU) and measuring the percentage of BrdU-positive cells after 6 h of continuous labeling (10 h for Chondrosia reniformis). Apoptosis was identified using an antibody against active caspase-3. Cell loss through shedding was studied quantitatively by collecting and weighing sponge-expelled detritus and qualitatively by light microscopy of sponge tissue and detritus. All species investigated displayed substantial cell proliferation, predominantly in the choanoderm, but also in the mesohyl. The majority of coral reef species (five) showed between 16.1±15.9% and 19.0±2.0% choanocyte proliferation (mean±SD) after 6 h and the Mediterranean species, C. reniformis, showed 16.6±3.2% after 10 h BrdU-labeling. Monanchora arbuscula showed lower choanocyte proliferation (8.1±3.7%), whereas the mangrove species Mycale microsigmatosa showed relatively higher levels of choanocyte proliferation (70.5±6.6%). Choanocyte proliferation in Haliclona vansoesti was variable (2.8–73.1%). Apoptosis was negligible and not the primary mechanism of cell loss involved in cell turnover. All species investigated produced significant amounts of detritus (2.5–18% detritus bodyweight⁻¹·d⁻¹) and cell shedding was observed in seven out of eight species. The amount of shed cells observed in histological sections may be related to differences in residence time of detritus within canals. Detritus production could not be directly linked to cell shedding due to the degraded nature of expelled cellular debris. We have demonstrated that under steady-state conditions, cell turnover through cell proliferation and cell shedding are common processes to maintain tissue homeostasis in a variety of sponge species from different ecosystems. Cell turnover is hypothesized to be the main underlying mechanism producing sponge-derived detritus, a major trophic resource transferred through sponges in benthic ecosystems, such as coral reefs.