Bacterial Communities of Two Ubiquitous Great Barrier Reef Corals Reveals Both Site- and Species-Specificity of Common Bacterial Associates

Background

Coral-associated bacteria are increasingly considered to be important in coral health, and altered bacterial community structures have been linked to both coral disease and bleaching. Despite this, assessments of bacterial communities on corals rarely apply sufficient replication to adequately describe the natural variability. Replicated data such as these are crucial in determining potential roles of bacteria on coral.

Methodology/Principal Findings

Denaturing Gradient Gel Electrophoresis (DGGE) of the V3 region of the 16S ribosomal DNA was used in a highly replicated approach to analyse bacterial communities on both healthy and diseased corals. Although site-specific variations in the bacterial communities of healthy corals were present, host species-specific bacterial associates within a distinct cluster of gamma-proteobacteria could be identified, which are potentially linked to coral health. Corals affected by “White Syndrome” (WS) underwent pronounced changes in their bacterial communities in comparison to healthy colonies. However, the community structure and bacterial ribotypes identified in diseased corals did not support the previously suggested theory of a bacterial pathogen as the causative agent of the syndrome.

Conclusions/Significance

This is the first study to employ large numbers of replicated samples to assess the bacterial communities of healthy and diseased corals, and the first culture-independent assessment of bacterial communities on WS affected Acroporid corals on the GBR. Results indicate that a minimum of 6 replicate samples are required in order to draw inferences on species, spatial or health-related changes in community composition, as a set of clearly distinct bacterial community profiles exist in healthy corals. Coral bacterial communities may be both site and species specific. Furthermore, a cluster of gamma-proteobacterial ribotypes may represent a group of specific common coral and marine invertebrate associates. Finally, the results did not support the contention that a single bacterial pathogen may be the causative agent of WS Acroporids on the GBR.     

Light Respiratory Processes and Gross Photosynthesis in Two Scleractinian Corals

The light dependency of respiratory activity of two scleractinian corals was examined using O₂ microsensors and CO₂ exchange measurements. Light respiration increased strongly but asymptotically with elevated irradiance in both species. Light respiration in Pocillopora damicornis was higher than in Pavona decussata under low irradiance, indicating species-specific differences in light-dependent metabolic processes. Overall, the coral P. decussata exhibited higher CO₂ uptake rates than P. damicornis over the experimental irradiance range. P. decussata also harboured twice as many algal symbionts and higher total protein biomass compared to P. damicornis, possibly resulting in self-shading of the symbionts and/or changes in host tissue specific light distribution. Differences in light respiration and CO₂ availability could be due to host-specific characteristics that modulate the symbiont microenvironment, its photosynthesis, and hence the overall performance of the coral holobiont.     

The Physiological Mechanisms of Acclimatization in Tropical Reef Corals

SYNOPSIS. The ability of scleractinian corals to survive changesthat are predicted in the global environment over the next centurywill lie in their physiological mechanisms of acclimatization.Corals display rapid modifications in behavior, morphology andphysiology enabling them to photoacclimate to changing lightconditions, a scenario that demonstrates considerable biologicalflexibility. Here we argue that the acclimatization mechanismsin corals are fundamentally similar to those exhibited by otherinvertebrate taxa. We discuss protein metabolism as a mechanismunderlying acclimatization responses in reef corals, and explorethe relationship between protein turnover, metabolic rate, growthrate, and acclimatization capacity. Our preliminary analysessuggest that corals with low growth rates (µCa/mgN/h)and high metabolic rates (µO₂/cm²/hr), such as the massivespecies, acclimatize more effectively than those with high growthrates and low metabolic rates, a feature that is characteristicof branching species. We conclude that studies of protein turnover,combined with temporally relevant investigations into the dynamicaspects of coral dinoflagellate symbioses will provide considerableinsight into why corals exhibit such a high level of variationin response to the same environmental challenge. Furthermore,a more detailed understanding of acclimatization mechanismsis essential if we are to predict how a coral assemblage willrespond to present and future environmental challenges.     

Sensitivity of Heterogeneous Marine Benthic Habitats to Subtle Stressors

It is important to understand the consequences of low level disturbances on the functioning of ecological communities because of the pervasiveness and frequency of this type of environmental change. In this study we investigated the response of a heterogeneous, subtidal, soft-sediment habitat to small experimental additions of organic matter and calcium carbonate to examine the sensitivity of benthic ecosystem functioning to changes in sediment characteristics that relate to the environmental threats of coastal eutrophication and ocean acidification. Our results documented significant changes between key biogeochemical and sedimentary variables such as gross primary production, ammonium uptake and dissolved reactive phosphorus flux following treatment additions. Moreover, the application of treatments affected relationships between macrofauna communities, sediment characteristics (e.g., chlorophyll a content) and biogeochemical processes (oxygen and nutrient fluxes). In this experiment organic matter and calcium carbonate showed persistent opposing effects on sedimentary processes, and we demonstrated that highly heterogeneous sediment habitats can be surprisingly sensitive to subtle perturbations. Our results have important biological implications in a world with relentless anthropogenic inputs of atmospheric CO₂ and nutrients in coastal waters.     

Size and Performance of Juvenile Marine Invertebrates: Potential Contrasts Between Intertidal and Subtidal Benthic Habitats

Newly settled or hatched juveniles of marine benthic invertebratesgenerally experience very high mortality. Juvenile mortalitycan profoundly affect adult populations, but little is knownabout how individual variation in juvenile quality affects performance.Several recent studies have demonstrated that differences insize, larval nutrient stores, or larval feeding history canstrongly affect the performance (measured as growth and survivorship)of juveniles. Additional research suggests that the strengthof the effect of juvenile size on performance may be mediatedby variation in environmental stress in the intertidal, a habitatcharacterized by strong fluctuations in abiotic factors. Themajor sources of juvenile snail mortality are likely to differin intertidal and subtidal habitats; abiotic stresses relatedto exposure, such as desiccation, are important in the intertidalbut far less severe in subtidal environments. Previously observedtrends in hatching or settlement size between intertidal andsubtidal species from three gastropod taxa may be due to differingselective regimes acting on initial juvenile size.     

Evidence for Two Main Domestication Trajectories in Saccharomyces cerevisiae Linked to Distinct Bread-Making Processes

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Effect of Phase Shift from Corals to Zoantharia on Reef Fish Assemblages

Consequences of reef phase shifts on fish communities remain poorly understood. Studies on the causes, effects and consequences of phase shifts on reef fish communities have only been considered for coral-to-macroalgae shifts. Therefore, there is a large information gap regarding the consequences of novel phase shifts and how these kinds of phase shifts impact on fish assemblages. This study aimed to compare the fish assemblages on reefs under normal conditions (relatively high cover of corals) to those which have shifted to a dominance of the zoantharian Palythoa cf. variabilis on coral reefs in Todos os Santos Bay (TSB), Brazilian eastern coast. We examined eight reefs, where we estimated cover of corals and P. cf. variabilis and coral reef fish richness, abundance and body size. Fish richness differed significantly between normal reefs (48 species) and phase-shift reefs (38 species), a 20% reduction in species. However there was no difference in fish abundance between normal and phase shift reefs. One fish species, Chaetodon striatus, was significantly less abundant on normal reefs. The differences in fish assemblages between different reef phases was due to differences in trophic groups of fish; on normal reefs carnivorous fishes were more abundant, while on phase shift reefs mobile invertivores dominated.     

Spatial Variation in Abundance,Size and Orientation of Juvenile Corals Related to the Biomass of Parrotfishes on the Great Barrier Reef,Australia

For species with complex life histories such as scleractinian corals, processes occurring early in life can greatly influence the number of individuals entering the adult population. A plethora of studies have examined settlement patterns of coral larvae, mostly on artificial substrata, and the composition of adult corals across multiple spatial and temporal scales. However, relatively few studies have examined the spatial distribution of small (≤50 mm diameter) sexually immature corals on natural reef substrata. We, therefore, quantified the variation in the abundance, composition and size of juvenile corals (≤50 mm diameter) among 27 sites, nine reefs, and three latitudes spanning over 1000 km on Australia’s Great Barrier Reef. Overall, 2801 juveniles were recorded with a mean density of 6.9 (±0.3 SE) ind.m⁻², with Acropora, Pocillopora, and Porites accounting for 84.1% of all juvenile corals surveyed. Size-class structure, orientation on the substrate and taxonomic composition of juvenile corals varied significantly among latitudinal sectors. The abundance of juvenile corals varied both within (6–13 ind.m⁻²) and among reefs (2.8–11.1 ind.m⁻²) but was fairly similar among latitudes (6.1–8.2 ind.m⁻²), despite marked latitudinal variation in larval supply and settlement rates previously found at this scale. Furthermore, the density of juvenile corals was negatively correlated with the biomass of scraping and excavating parrotfishes across all sites, revealing a potentially important role of parrotfishes in determining distribution patterns of juvenile corals on the Great Barrier Reef. While numerous studies have advocated the importance of parrotfishes for clearing space on the substrate to facilitate coral settlement, our results suggest that at high biomass they may have a detrimental effect on juvenile coral assemblages. There is, however, a clear need to directly quantify rates of mortality and growth of juvenile corals to understand the relative importance of these mechanisms in shaping juvenile, and consequently adult, coral assemblages.     

The Recovery of Benthic Invertebrate Communities Following Dewateringin Two Braided Rivers

The recovery of benthic invertebrates was investigated in the braided Tukituki and Waipawa Rivers (North Island, New Zealand) following extended channel dewatering of sites for 6, 10 or 14 weeks during summer 1997/1998. After rewatering, invertebrates rapidly colonised each denuded site and, although some invertebrates were numerically dominant at different times, 95⁺% of the taxa list were present after 7 days of rewatering. The number of individuals also increased over time, but significantly greater numbers were collected in reference sites and those dry for 6 weeks compared to sites dewatered for longer periods. Taxa such as Tanytarsus spp., Maoridiamesa spp. (Diptera: Chironomidae) and the riffle beetle Elmidae (Coleoptera) were abundant early, while Deleatidium spp. (Ephemeroptera: Leptophlebiidae) dominated communities later. The greater abundance of Deleatidium in sites dewatered for a short time may be because desiccation was less significant at determining taxa present at these sites, or that reference sites provided a closer source of colonists and periphyton propagules to allow a more rapid numerical recovery of this taxon. In contrast, Elmidae dominated communities at sites dewatered for longer periods because Elmidae may be more resilient to desiccation than Deleatidium. These data suggest that the duration of dewatering may regulate taxonomic composition in the short term by subjecting taxa to desiccation and/or food resource restrictions, but not in the long term because food resources recovered over time and sites with similar physicochemical conditions should have similar communities.     

Reef Endemism,Host Specificity and Temporal Stability in Populations of Symbiotic Dinoflagellates from Two Ecologically Dominant Caribbean Corals

Background

The dinoflagellate genus Symbiodinium forms symbioses with numerous protistan and invertebrate metazoan hosts. However, few data on symbiont genetic structure are available, hindering predictions of how these populations and their host associations will fair in the face of global climate change.

Methodology/Principal Findings

Here, Symbiodinium population structure from two of the Caribbean''s ecologically dominant scleractinian corals, Montastraea faveolata and M. annularis, was examined. Tagged colonies on Florida Keys and Bahamian (i.e., Exuma Cays) reefs were sampled from 2003–2005 and their Symbiodinium diversity assessed via internal transcribed spacer 2 (ITS2) rDNA and three Symbiodinium Clade B-specific microsatellite loci. Generally, the majority of host individuals at a site harbored an identical Symbiodinium ITS2 “type” B1 microsatellite genotype. Notably, symbiont genotypes were largely reef endemic, suggesting a near absence of dispersal between populations. Relative to the Bahamas, sympatric M. faveolata and M. annularis in the Florida Keys harbored unique Symbiodinium populations, implying regional host specificity in these relationships. Furthermore, within-colony Symbiodinium population structure remained stable through time and environmental perturbation, including a prolonged bleaching event in 2005.

Conclusions/Significance

Taken together, the population-level endemism, specificity and stability exhibited by Symbiodinium raises concerns about the long-term adaptive capacity and persistence of these symbioses in an uncertain future of climate change.     

Heavy Metal Pollution in Reef Corals of Tuticorin Coast,Southeast Coast of India

This work investigates the metal pollution documented in the skeletons of selected coral species like Acropora formosa, Montipora digitata and Porites andrewsi from the Tuticorin Coast, one of the least studied areas in the Bay of Bengal. Relating heavy metal concentrations to morphological features of skeletons, highest concentrations of all the metals (except Cu and Zn) were found in ramose or branching types of corals. Irrespective of their growth characteristics or patterns, all these species displayed higher concentrations of Pb, Ni, Mn, and Cd within the skeletal part. The study area is currently exposed to a larger degree of metal pollution (natural and anthropogenic) than even before, as a result of the increasing environmental contamination from sewage discharges, the misuse of agricultural chemicals and fertilizers, and top soil erosion. The concentrations of heavy metals obtained in the present study are compared with values from earlier works around the world. This study indicates that corals are vulnerable to the accumulation of high concentrations of heavy metals in their skeletons and therefore can serve as proxies to monitor environmental pollution.     

Responses of Two Scleractinian Corals to Cobalt Pollution and Ocean Acidification

The effects of ocean acidification alone or in combination with warming on coral metabolism have been extensively investigated, whereas none of these studies consider that most coral reefs near shore are already impacted by other natural anthropogenic inputs such as metal pollution. It is likely that projected ocean acidification levels will aggravate coral reef health. We first investigated how ocean acidification interacts with one near shore locally abundant metal on the physiology of two major reef-building corals: Stylophora pistillata and Acropora muricata. Two pH levels (pH_T 8.02; pCO₂ 366 μatm and pH_T 7.75; pCO₂ 1140 μatm) and two cobalt concentrations (natural, 0.03 μg L^-1 and polluted, 0.2 μg L^-1) were tested during five weeks in aquaria. We found that, for both species, cobalt input decreased significantly their growth rates by 28% while it stimulated their photosystem II, with higher values of rETR_max (relative Electron Transport Rate). Elevated pCO₂ levels acted differently on the coral rETR_max values and did not affect their growth rates. No consistent interaction was found between pCO₂ levels and cobalt concentrations. We also measured in situ the effect of higher cobalt concentrations (1.06 ± 0.16 μg L^-1) on A. muricata using benthic chamber experiments. At this elevated concentration, cobalt decreased simultaneously coral growth and photosynthetic rates, indicating that the toxic threshold for this pollutant has been reached for both host cells and zooxanthellae. Our results from both aquaria and in situ experiments, suggest that these coral species are not particularly sensitive to high pCO₂ conditions but they are to ecologically relevant cobalt concentrations. Our study reveals that some reefs may be yet subjected to deleterious pollution levels, and even if no interaction between pCO₂ levels and cobalt concentration has been found, it is likely that coral metabolism will be weakened if they are subjected to additional threats such as temperature increase, other heavy metals, and eutrophication.     

A Diverse Assemblage of Reef Corals Thriving in a Dynamic Intertidal Reef Setting (Bonaparte Archipelago,Kimberley, Australia)

The susceptibility of reef-building corals to climatic anomalies is well documented and a cause of great concern for the future of coral reefs. Reef corals are normally considered to tolerate only a narrow range of climatic conditions with only a small number of species considered heat-tolerant. Occasionally however, corals can be seen thriving in unusually harsh reef settings and these are cause for some optimism about the future of coral reefs. Here we document for the first time a diverse assemblage of 225 species of hard corals occurring in the intertidal zone of the Bonaparte Archipelago, north western Australia. We compare the environmental conditions at our study site (tidal regime, SST and level of turbidity) with those experienced at four other more typical tropical reef locations with similar levels of diversity. Physical extremes in the Bonaparte Archipelago include tidal oscillations of up to 8 m, long subaerial exposure times (>3.5 hrs), prolonged exposure to high SST and fluctuating turbidity levels. We conclude the timing of low tide in the coolest parts of the day ameliorates the severity of subaerial exposure, and the combination of strong currents and a naturally high sediment regime helps to offset light and heat stress. The low level of anthropogenic impact and proximity to the Indo-west Pacific centre of diversity are likely to further promote resistance and resilience in this community. This assemblage provides an indication of what corals may have existed in other nearshore locations in the past prior to widespread coastal development, eutrophication, coral predator and disease outbreaks and coral bleaching events. Our results call for a re-evaluation of what conditions are optimal for coral survival, and the Bonaparte intertidal community presents an ideal model system for exploring how species resilience is conferred in the absence of confounding factors such as pollution.     

Robust Performance of Marginal Pacific Coral Reef Habitats in Future Climate Scenarios

Coral reef ecosystems are under dual threat from climate change. Increasing sea surface temperatures and thermal stress create environmental limits at low latitudes, and decreasing aragonite saturation state creates environmental limits at high latitudes. This study examines the response of unique coral reef habitats to climate change in the remote Pacific, using the National Center for Atmospheric Research Community Earth System Model version 1 alongside the species distribution algorithm Maxent. Narrow ranges of physico-chemical variables are used to define unique coral habitats and their performance is tested in future climate scenarios. General loss of coral reef habitat is expected in future climate scenarios and has been shown in previous studies. This study found exactly that for most of the predominant physico-chemical environments. However, certain coral reef habitats considered marginal today at high latitude, along the equator and in the eastern tropical Pacific were found to be quite robust in climate change scenarios. Furthermore, an environmental coral reef refuge previously identified in the central south Pacific near French Polynesia was further reinforced. Studying the response of specific habitats showed that the prevailing conditions of this refuge during the 20^th century shift to a new set of conditions, more characteristic of higher latitude coral reefs in the 20^th century, in future climate scenarios projected to 2100.     

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.     

Current Patterns and the Distribution of Benthic Habitats in a Coastal Lagoon of Mauritius

The oceanography around Mauritius (in the Western Indian Ocean) remains largely unstudied, hence there is an acute scarcity of marine environmental data for management purposes. Rigorous water depth and current measurements were made on a system of grids inside Le Morne lagoon (in the south western part of Mauritius) in March–April 2000 to generate semi-quantitative models of general flow pattern in the form of contour maps using SURFER 6 computer programme. A simultaneous survey on composition of bottom cover was conducted to examine possible relationships with current speed. A separate investigation recorded surface and bottom currents prevailing amongst various habitat types to demonstrate the nature of the resulting damping effect on surface current speed. Significant correlations generated from data analysis were discussed as a basis for real biophysical relationships. Some of the limitations in the current analysis and some of the seemingly contradictory results are acknowledged and addressed in the light of the general assumption that the structure of the lagoon is conditioned by current speeds. Much stronger current speeds just outside the reef (e.g. >0.5 m s⁻¹) than inside the lagoon (e.g. <0.32 m s⁻¹) indicated a substantial slow-down of water current by the reef barrier. Inshore bottom currents were weaker than at the surface and current speed correlated well with water depth. Bottom and surface current directions were generally similar, i.e. going northward during flood tide and southward during ebb. The lagoon would be classified as ‘restricted’, exhibiting well-defined tidal circulation, which is modified by wind forcing. Dense fields of branching Acropora corals slowed down surface current speed by as much as 87%, but the relationship between current speed and bottom cover appears to be variable, depending on the specific location within the lagoon under consideration. The contour plots of the flow pattern model generated reasonably high qualitative modelling of spatial current speed pattern in the lagoon, with stronger currents generally along the reef areas, at the reef passes and in the deeper zones. However, these plots did not match closely those displaying distribution of bottom cover, thus confirming results obtained from pair-wise correlation tests, namely the lack of a significant relationship between current speed and bottom cover. Most of the correlations would appear to represent biological relationships, with different types of communities enabling or excluding other types. Thus, the biophysical structure of the lagoon would be driven a priori by the distribution and abundance of corals rather than current speeds, which contradicts the above hypothesis. Recurrent natural hazards subject the benthic communities to a state of ‘perpetual knock-down and recovery’. Recovery, however, can be seriously impaired by the chronic ongoing degradation of the coastal marine environment of Mauritius. An urgent review of its coastal zone management and protection strategy would be desirable for the island.     

Benthic diatom community composition in three regions of the Great Barrier Reef,Australia

Despite their ecological importance, very little is known about the taxonomy and ecology of benthic diatoms in coral-reef ecosystems. Diatom densities and community compositions were investigated in three distinct regions of the Great Barrier Reef (GBR): (a) Wet Tropics (WT), (b) Princess Charlotte Bay (PCB), and (c) the Outer Shelf (OS). About 209 taxa were observed in the GBR sediments studied, with an average abundance of 2.55 × 10⁶ cells ml⁻¹ in the upper 1 cm of sediment. Total diatom abundances were about twice as high in inshore reefs of PCB and WT compared with OS reefs. A redundancy analysis (RDA) of diatom composition clearly grouped the three regions separately but showed little influence of grain size, nitrogen and organic carbon content of the sediments. The only distinct correlates were inorganic carbon and the distance to the mainland associated with OS communities. Analysis of similarity (ANOSIM) of diatom community composition revealed significant differences between all three regions. Indicator values showed that most highly abundant taxa occurred in all regions. However, several taxa were clearly identified as characteristic of particular regions. It is hypothesised that variations in nutrient and light availability are the most likely explanation for the observed differences in community composition.     

Benthic microalgae in coral reef sediments of the southern Great Barrier Reef,Australia

The abundance and productivity of benthic microalgae in coral reef sediments are poorly known compared with other, more conspicuous (e.g. coral zooxanthellae, macroalgae) primary producers of coral reef habitats. A survey of the distribution, biomass, and productivity of benthic microalgae on a platform reef flat and in a cross-shelf transect in the southern Great Barrier Reef indicated that benthic microalgae are ubiquitous, abundant (up to 995.0 mg chlorophyll (chl) a m^–2), and productive (up to 110 mg O₂ m^–2 h^–1) components of the reef ecosystem. Concentrations of benthic microalgae, expressed as chlorophyll a per surface area, were approximately 100-fold greater than the integrated water column concentrations of microalgae throughout the region. Benthic microalgal biomass was greater on the shallow water platform reef than in the deeper waters of the cross-shelf transect. In both areas the benthic microalgal communities had a similar composition, dominated by pennate diatoms, dinoflagellates, and cyanobacteria. Benthic microalgal populations were potentially nutrient-limited, based on responses to nitrogen and phosphorus enrichments in short-term (7-day) microcosm experiments. Benthic microalgal productivity, measured by O₂ evolution, indicated productive communities responsive to light and nutrient availability. The benthic microalgal concentrations observed (92–995 mg chl a m^–2) were high relative to other reports, particularly compared with temperate regions. This abundance of productive plants in both reef and shelf sediments in the southern Great Barrier Reef suggests that benthic microalgae are key components of coral reef ecosystems.Communicated by Environmental Editor, B.C. Hatcher