Calcifying coral abundance near low-pH springs: implications for future ocean acidification

Rising atmospheric CO₂ and its equilibration with surface ocean seawater is lowering both the pH and carbonate saturation state (Ω) of the oceans. Numerous calcifying organisms, including reef-building corals, may be severely impacted by declining aragonite and calcite saturation, but the fate of coral reef ecosystems in response to ocean acidification remains largely unexplored. Naturally low saturation (Ω ~ 0.5) low pH (6.70–7.30) groundwater has been discharging for millennia at localized submarine springs (called “ojos”) at Puerto Morelos, México near the Mesoamerican Reef. This ecosystem provides insights into potential long term responses of coral ecosystems to low saturation conditions. In-situ chemical and biological data indicate that both coral species richness and coral colony size decline with increasing proximity to low-saturation, low-pH waters at the ojo centers. Only three scleractinian coral species (Porites astreoides, Porites divaricata, and Siderastrea radians) occur in undersaturated waters at all ojos examined. Because these three species are rarely major contributors to Caribbean reef framework, these data may indicate that today’s more complex frame-building species may be replaced by smaller, possibly patchy, colonies of only a few species along the Mesoamerican Barrier Reef. The growth of these scleractinian coral species at undersaturated conditions illustrates that the response to ocean acidification is likely to vary across species and environments; thus, our data emphasize the need to better understand the mechanisms of calcification to more accurately predict future impacts of ocean acidification.     

Variability in Microbial Community Composition and Function Between Different Niches Within a Coral Reef

To explore how microbial community composition and function varies within a coral reef ecosystem, we performed metagenomic sequencing of seawater from four niches across Heron Island Reef, within the Great Barrier Reef. Metagenomes were sequenced from seawater samples associated with (1) the surface of the coral species Acropora palifera, (2) the surface of the coral species Acropora aspera, (3) the sandy substrate within the reef lagoon and (4) open water, outside of the reef crest. Microbial composition and metabolic function differed substantially between the four niches. The taxonomic profile showed a clear shift from an oligotroph-dominated community (e.g. SAR11, Prochlorococcus, Synechococcus) in the open water and sandy substrate niches, to a community characterised by an increased frequency of copiotrophic bacteria (e.g. Vibrio, Pseudoalteromonas, Alteromonas) in the coral seawater niches. The metabolic potential of the four microbial assemblages also displayed significant differences, with the open water and sandy substrate niches dominated by genes associated with core house-keeping processes such as amino acid, carbohydrate and protein metabolism as well as DNA and RNA synthesis and metabolism. In contrast, the coral surface seawater metagenomes had an enhanced frequency of genes associated with dynamic processes including motility and chemotaxis, regulation and cell signalling. These findings demonstrate that the composition and function of microbial communities are highly variable between niches within coral reef ecosystems and that coral reefs host heterogeneous microbial communities that are likely shaped by habitat structure, presence of animal hosts and local biogeochemical conditions.     

Novel T4 bacteriophages associated with black band disease in corals

Research into causative agents underlying coral disease have focused primarily on bacteria, whereas potential roles of viruses have been largely unaddressed. Bacteriophages may contribute to diseases through the lysogenic introduction of virulence genes into bacteria, or prevent diseases through lysis of bacterial pathogens. To identify candidate phages that may influence the pathogenicity of black band disease (BBD), communities of bacteria (16S rRNA) and T4-bacteriophages (gp23) were simultaneously profiled with amplicon sequencing among BBD-lesions and healthy-coral-tissue of Montipora hispida, as well as seawater (study site: the central Great Barrier Reef). Bacterial community compositions were distinct among BBD-lesions, healthy coral tissue and seawater samples, as observed in previous studies. Surprisingly, however, viral beta diversities based on both operational taxonomic unit (OTU)-compositions and overall viral community compositions of assigned taxa did not differ statistically between the BBD-lesions and healthy coral tissue. Nonetheless, relative abundances of three bacteriophage OTUs, affiliated to Cyanophage PRSM6 and Prochlorococcus phages P-SSM2, were significantly higher in BBD-lesions than in healthy tissue. These OTUs associated with BBD samples suggest the presence of bacteriophages that infect members of the cyanobacteria-dominated BBD community, and thus have potential roles in BBD pathogenicity.     

An introduction to the biogeochemical cycling of calcium and substitutive strontium in living coral reef mesocosms

The coral reef mesocosms designed by the Smithsonian Institution's Dr. Walter Adey, his Marine System Laboratory personnel, and staff members of the Pittsburgh Aqua-Zoo simulate most of the physical, chemical, and biological parameters found in natural Caribbean coral reefs. After developing the mesocosm in Pittsburgh, an evaluation and comparison between natural reef seawater sources and closed mesocosm seawater conditions indicated that an additional parameter should be investigated. It was hypothesized that, given time, the aragonite- and calcite (CaCO₃ crystal forms)-producing organisms in the closed mesocosms could deplete the seawater of available Ca²⁺ and substitutive Sr²⁺. Atomic absorption spectrophotometry was utilized to determine concentrations in the seawater over time. Results showed a substantial reduction in dissolved Ca and Sr in the mesocosm after approximately two years. Dissolved aragonitic Halimeda algae parts were put into the system for replacive purposes. In terms of the biogeochemical cycling of Ca²⁺ and Sr²⁺, the coral reef mesocosm organisms behaved similarly to natural reefs, which have a constant supply of dissolved Ca²⁺ and Sr²⁺. Further research utilizing radiolabeled sources of Ca²⁺, Sr²⁺, and Mg²⁺, in conjunction with in vivo scanning electron microscopy (SEM) and growth increment studies, are recommended for determining the exact biogeochemical pathways for these elements in coral reefs, and to quantify growth parameters. © 1993 Wiley-Liss, Inc.     

Microbial bioindicators of Stony Coral Tissue Loss Disease identified in corals and overlying waters using a rapid field-based sequencing approach

Stony Coral Tissue Loss Disease (SCTLD) is a devastating disease. Since 2014, it has spread along the entire Florida Reef Tract and into the greater Caribbean. It was first detected in the United States Virgin Islands in January 2019. To more quickly identify microbial bioindicators of disease, we developed a rapid pipeline for microbiome sequencing. Over a span of 10 days we collected, processed and sequenced coral and near-coral seawater microbiomes from diseased and apparently healthy Colpophyllia natans, Montastraea cavernosa, Meandrina meandrites and Orbicella franksi. Analysis of bacterial and archaeal 16S ribosomal RNA gene sequences revealed 25 bioindicator amplicon sequence variants (ASVs) enriched in diseased corals. These bioindicator ASVs were additionally recovered in near-coral seawater (<5 cm of coral surface), a potential reservoir for pathogens. Phylogenetic analysis of microbial bioindicators with sequences from the Coral Microbiome Database revealed that Vibrio, Arcobacter, Rhizobiaceae and Rhodobacteraceae sequences were related to disease-associated coral bacteria and lineages novel to corals. Additionally, four ASVs (Algicola, Cohaesibacter, Thalassobius and Vibrio) were matches to microbes previously associated with SCTLD that should be targets for future research. Overall, this work suggests that a rapid sequencing framework paired with specialized databases facilitates identification of microbial disease bioindicators.     

Real-time PCR reveals a high incidence of <Emphasis Type="Italic">Symbiodinium </Emphasis>clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling

Reef corals form associations with an array of genetically and physiologically distinct endosymbionts from the genus Symbiodinium. Some corals harbor different clades of symbionts simultaneously, and over time the relative abundances of these clades may change through a process called symbiont shuffling. It is hypothesized that this process provides a mechanism for corals to respond to environmental threats such as global warming. However, only a minority of coral species have been found to harbor more than one symbiont clade simultaneously and the current view is that the potential for symbiont shuffling is limited. Using a newly developed real-time PCR assay, this paper demonstrates that previous studies have underestimated the presence of background symbionts because of the low sensitivity of the techniques used. The assay used here targets the multi-copy rDNA ITS1 region and is able to detect Symbiodinium clades C and D with >100-fold higher sensitivity compared to conventional techniques. Technical considerations relating to intragenomic variation, estimating copy number and non-symbiotic contamination are discussed. Eighty-two colonies from four common scleractinian species (Acropora millepora, Acropora tenuis, Stylophora pistillata and Turbinaria reniformis) and 11 locations on the Great Barrier Reef were tested for background Symbiodinium clades. Although these colonies had been previously identified as harboring only a single clade based on SSCP analyses, background clades were detected in 78% of the samples, indicating that the potential for symbiont shuffling may be much larger than currently thought.     

Down under the tunic: bacterial biodiversity hotspots and widespread ammonia-oxidizing archaea in coral reef ascidians

Ascidians are ecologically important components of marine ecosystems yet the ascidian microbiota remains largely unexplored beyond a few model species. We used 16S rRNA gene tag pyrosequencing to provide a comprehensive characterization of microbial symbionts in the tunic of 42 Great Barrier Reef ascidian samples representing 25 species. Results revealed high bacterial biodiversity (3 217 unique operational taxonomic units (OTU_0.03) from 19 described and 14 candidate phyla) and the widespread occurrence of ammonia-oxidizing Thaumarchaeota in coral reef ascidians (24 of 25 host species). The ascidian microbiota was clearly differentiated from seawater microbial communities and included symbiont lineages shared with other invertebrate hosts as well as unique, ascidian-specific phylotypes. Several rare seawater microbes were markedly enriched (200–700 fold) in the ascidian tunic, suggesting that the rare biosphere of seawater may act as a conduit for horizontal symbiont transfer. However, most OTUs (71%) were rare and specific to single hosts and a significant correlation between host relatedness and symbiont community similarity was detected, indicating a high degree of host-specificity and potential role of vertical transmission in structuring these communities. We hypothesize that the complex ascidian microbiota revealed herein is maintained by the dynamic microenvironments within the ascidian tunic, offering optimal conditions for different metabolic pathways such as ample chemical substrate (ammonia-rich host waste) and physical habitat (high oxygen, low irradiance) for nitrification. Thus, ascidian hosts provide unique and fertile niches for diverse microorganisms and may represent an important and previously unrecognized habitat for nitrite/nitrate regeneration in coral reef ecosystems.     

Long-term coral community records from Lugger Shoal on the terrigenous inner-shelf of the central Great Barrier Reef,Australia

Long-term (millennial timescale) records of coral community structure can be developed from the analysis of corals preserved in radiometrically dated reef cores. Here, we present such a record (based on six cores) from Lugger Shoal, a turbid zone, nearshore reef on the inner-shelf of the central Great Barrier Reef. Lugger Shoal initiated growth ~800 cal yBP. It is constructed of large in situ Porites bommies, between which a framework of coral rubble (dominated by Acropora pulchra, Montipora mollis, Galaxea fascicularis and Cyphastrea serailia) has accumulated. Reef accretion occurred under conditions of net long-term fine-grained, terrigenous sediment accumulation, and with a coral community dominated throughout by a consistent, but low diversity, suite of coral taxa. This dataset supports recent suggestions that nearshore coral communities that establish themselves under conditions that are already close to the thresholds for coral survival may be resilient to water quality deteriorations associated with human activities.     

An evaluation of the antimicrobial properties of the eggs of 11 species of scleractinian corals

Potential sources of mortality of marine invertebrate larvae are numerous and include predation and diseases caused by marine microorganisms. Extracts from the eggs of 11 coral species were evaluated for their ability to deter surface attachment and inhibit the growth of two marine tolerant laboratory bacteria and 92 bacterial strains isolated from seawater and the surface of coral colonies on the Great Barrier Reef (GBR). Extracts of the eggs of Montipora digitata inhibited the growth of the two laboratory bacteria, Vibrio harveyii and Bacillus subtilis, and one bacterial isolate from the mucus of the coral Favia pallida in disc diffusion and liquid culture assays. No other microbial strains (n=91) from the surface of corals and the reef environment were inhibited by M. digitata extracts. No antibacterial activity was found in the egg extracts of the remaining ten coral species and none of the extracts inhibited surface attachment of various bacteria. Extrapolation of estimated surface concentrations of the biologically active extract of M. digitata suggests that the level of the growth inhibitory compounds may be sufficient to deter microbial growth in situ.     

Coral-associated bacterial communities on Ningaloo Reef, Western Australia

Coral-associated microbial communities from three coral species (Pocillopora damicornis, Acropora tenuis and Favites abdita) were examined every 3 months (January, March, June, October) over a period of 1 year on Ningaloo Reef, Western Australia. Tissue from corals was collected throughout the year and additional sampling of coral mucus and seawater samples was performed in January. Tissue samples were also obtained in October from P. damicornis coral colonies on Rottnest Island off Perth, 1200 km south of Ningaloo Reef, to provide comparisons between coral-microbial associates in different locations. The community structures of the coral-associated microorganisms were analysed using phylogenetic analysis of 16S rRNA gene clone libraries, which demonstrated highly diverse microbial profiles among all the coral species sampled. Principal component analysis revealed that samples grouped according to time and not species, indicating that coral-microbial associations may be a result of environmental drivers such as oceanographic characteristics, benthic community structure and temperature. Tissue samples from P. damicornis at Rottnest Island revealed similarities in bacteria to the samples at Ningaloo Reef. This study highlights that coral-associated microbial communities are highly diverse; however, the complex interactions that determine the stability of these associations are not necessarily dependent on coral host specificity.     

Epidemiology of skeletal eroding band on the Great Barrier Reef and the role of injury in the initiation of this widespread coral disease

Skeletal eroding band (SEB), which manifests as dense aggregations of the ciliate Halofolliculina corallasia, was the first coral disease described from the Indo-Pacific. Little is known about its etiology or impact. This study describes the distribution, prevalence and host range of SEB on a 500 km extent of the Great Barrier Reef (GBR), together with in situ rates of progression and infection following experimental injury. SEB occurred on 90–100% of reefs surveyed (n=18) in each of 3 years, demonstrating that SEB is widely distributed and persistent. SEB had the highest prevalence of any disease, affecting approximately 2% of 283,486 scleractinians and hydrocorals surveyed. Its host range was large, affecting 12 families and at least 82 scleractinian species, as well as the hydrocoral, Millepora. Corals in the families Pocilloporidae and Acroporidae were most susceptible, the former being up to five times more susceptible than other families. Progressive tissue loss was recorded on 95% of Acropora muricata colonies monitored (n = 18), with rates of SEB progression averaging ∼2 mm/day. Injury experiments demonstrated that H. corallasia, the putative pathogen of SEB, readily colonised recently exposed coral skeleton in the absence of a vector, but did not colonise intact coral tissue. Invading ciliates failed to form band-like aggregations associated with progressive tissue loss on any of three coral species tested experimentally, suggesting that, while H. corallasia readily colonises recently exposed coral skeleton, it may not be sufficient in itself to cause tissue mortality. Interactions with additional agents or factors, increasing ciliate virulence or lowering disease resistance of coral hosts may be required before halofolliculinid infections become associated with tissue loss.     

Significance of <Emphasis Type="Italic">Halimeda</Emphasis> bioherms to the global carbonate budget based on a geological sediment budget for the Northern Great Barrier Reef,Australia

Since the correlation between carbon dioxide (CO₂) levels and global temperatures was established in the ice core records, quantifying the components of the global carbon cycle has become a priority with a view to constraining models of the climate system. The marine carbonate budget is still not adequately constrained and the quantitative significance of the calcareous green alga Halimeda still remains particularly poorly understood. Previously, it has been suggested that Halimeda bioherms on the shelf of the Great Barrier Reef may contain a volume of carbonate equal to or greater than that contained within the shelf edge coral reefs. This study uses published datasets to test this hypothesis in the Northern Great Barrier Reef (NGBR) province. It is estimated that Halimeda bioherms on the outer shelf of the NGBR contain at least as much (and up to four times more) CaCO₃ sediment as the adjacent ribbon reef facies. Globally, if these findings are even only partially applicable, the contribution of shallow water carbonate sediments to the global carbon budget based on coral reefs alone is currently substantially underestimated.     

Dark calcification and the daily rhythm of calcification in the scleractinian coral, <Emphasis Type="Italic">Galaxea fascicularis</Emphasis>

The rate of calcification in the scleractinian coral Galaxea fascicularis was followed during the daytime using ⁴⁵Ca tracer. The coral began the day with a low calcification rate, which increased over time to a maximum in the afternoon. Since the experiments were carried out under a fixed light intensity, these results suggest that an intrinsic rhythm exists in the coral such that the calcification rate is regulated during the daytime. When corals were incubated for an extended period in the dark, the calcification rate was constant for the first 4 h of incubation and then declined, until after one day of dark incubation, calcification ceased, possibly as a result of the depletion of coral energy reserves. The addition of glucose and Artemia reduced the dark calcification rate for the short duration of the experiment, indicating an expenditure of oxygen in respiration. Artificial hypoxia reduced the rate of dark calcification to about 25% compared to aerated coral samples. It is suggested that G. fascicularis obtains its oxygen needs from the surrounding seawater during the nighttime, whereas during the day time the coral exports oxygen to the seawater.     

Phage therapy of coral disease

At present there are no known procedures for preventing or treating infectious diseases of corals. Toward this end, the use of phage therapy has been investigated. Lytic bacteriophages (phages) were isolated for two bacterial pathogens that are responsible for coral diseases, Vibrio coralliilyticus, which is the causative agent of bleaching and tissue lysis of Pocillopora damicornis, and Thalosomonas loyaeana, which causes the white plague-like disease of Favia favus. By using these phages in controlled aquaria experiments, it was demonstrated that each of these diseases could be controlled by the pathogen-specific phage. The data indicate that initially the phages bind to the pathogen in seawater and are then brought to the coral surface where they multiply and lyse the pathogen. The phages remained associated with the coral and could prevent subsequent infections. These data suggest that phage therapy has the potential to control the spread of infectious coral diseases.     

Local variation in herbivore feeding activity on an inshore reef of the Great Barrier Reef

Threats to coral reefs may be manifested through an increase in macroalgae. Across the globe, phase-shifts from coral to macroalgal dominance have been reported from the Caribbean, Indian and Pacific Oceans. While the Great Barrier Reef (GBR) is in relatively good condition, inshore reefs may exhibit over 50% macroalgal cover. However, our understanding of the processes preventing the macroalgal expansion remains uncertain. Using a remote video bioassay approach, this study quantified herbivory in three bays along the leeward margin of Orpheus Island. Despite significant with-in bay variation in herbivory there was no detectable statistical difference in the rates of herbivory among bays. Furthermore, of the 45 herbivore species recorded from the island, only three played a significant role in bioassay removal, Siganus canaliculatus, Siganus javus and Kyphosus vaigiensis, with only one species predominating in each bay. Reefs of the GBR may therefore be more vulnerable than previously thought, with the removal of macroalgae depending on just a few species, which exhibit considerable spatial variability in their feeding behaviour.     

Corals form characteristic associations with symbiotic nitrogen-fixing bacteria

The complex symbiotic relationship between corals and their dinoflagellate partner Symbiodinium is believed to be sustained through close associations with mutualistic bacterial communities, though little is known about coral associations with bacterial groups able to fix nitrogen (diazotrophs). In this study, we investigated the diversity of diazotrophic bacterial communities associated with three common coral species (Acropora millepora, Acropora muricata, and Pocillopora damicormis) from three midshelf locations of the Great Barrier Reef (GBR) by profiling the conserved subunit of the nifH gene, which encodes the dinitrogenase iron protein. Comparisons of diazotrophic community diversity among coral tissue and mucus microenvironments and the surrounding seawater revealed that corals harbor diverse nifH phylotypes that differ between tissue and mucus microhabitats. Coral mucus nifH sequences displayed high heterogeneity, and many bacterial groups overlapped with those found in seawater. Moreover, coral mucus diazotrophs were specific neither to coral species nor to reef location, reflecting the ephemeral nature of coral mucus. In contrast, the dominant diazotrophic bacteria in tissue samples differed among coral species, with differences remaining consistent at all three reefs, indicating that coral-diazotroph associations are species specific. Notably, dominant diazotrophs for all coral species were closely related to the bacterial group rhizobia, which represented 71% of the total sequences retrieved from tissue samples. The species specificity of coral-diazotroph associations further supports the coral holobiont model that bacterial groups associated with corals are conserved. Our results suggest that, as in terrestrial plants, rhizobia have developed a mutualistic relationship with corals and may contribute fixed nitrogen to Symbiodinium.     

Relationships between benthic cover, current strength, herbivory, and a fisheries closure in Glovers Reef Atoll, Belize

Benthic cover, current strengths, and fish abundance and diversity were examined on 150 lagoonal patch reefs and mapped to determine their distribution, inter-relationships, and relationship to the fisheries closure in Glovers Reef Atoll. Current strength was highest at both the northern and southern ends of the atoll and largely controlled by local wind and weakly by tidal forcing. Benthic functional group distributions varied throughout the atoll and had distinct areas of dominance. In contrast, dominance of coral species was weaker, reflecting the lost cover and zonation of Acropora, Porites, and Montastraea that were reported in the 1970s. Hard and soft corals dominated the windward rim, while the central and leeward lagoon had lower current strengths and sea grass and fleshy green algae were relatively more abundant. Brown erect algae were relatively more common in the north and calcifying green and red algae the southern ends of the atoll. Only Montastraea-Agaricia agaricites distributions were similar to reports from the 1970s with high relative dominance in the southern and northeast atoll. The central-northern zone, which was described as an Acropora zone in the 1970s, was not recognizable, and Porites porites, P. astreoides, Millepora alcicornis, and Favia fragum were the most abundant species during this survey. Hard and soft coral cover abundance declined away from the reef rim and tidal channels and was associated with fast seawater turnover and high surgeonfish abundance. Consequently, the windward rim area has retained the most original and persistent hard-soft coral and surgeonfish community and is considered a priority for future management, if the goal is to protect coral from fishing impacts.     

Horizontal transmission of Symbiodinium cells between adult and juvenile corals is aided by benthic sediment

Of all reef-building coral species, 80–85 % initially draw their intracellular symbionts (dinoflagellates of the genus Symbiodinium) from the environment. Although Symbiodinium cells are crucial for the growth of corals and the formation of coral reefs, little is known about how corals first encounter free-living Symbiodinium cells. We report how the supply of free-living Symbiodinium cells to the benthos by adult corals can increase the rate of horizontal symbiont acquisition for conspecific recruits. Three species of newly settled aposymbiotic (i.e., symbiont-free) corals were maintained in an open aquarium system containing: sterilized sediment and adult coral fragments combined; adult coral fragments alone; sterilized sediment alone; or seawater at Heron Island, Great Barrier Reef, Australia. In all instances, the combination of an adult coral and sediment resulted in the highest symbiont acquisition rates by juvenile corals (up to five-fold greater than seawater alone). Juvenile corals exposed to individual treatments of adult coral or sediment produced an intermediate acquisition response (<52 % of recruits), and symbiont acquisition from unfiltered seawater was comparatively low (<20 % of recruits). Additionally, benthic free-living Symbiodinium cells reached their highest densities in the adult coral + sediment treatment (up to 1.2 × 10⁴ cells mL⁻¹). Our results suggest that corals seed microhabitats with free-living Symbiodinium cells suitable for many coral species during the process of coral recruitment.

     

Acoustic mapping using a multibeam echosounder reveals cold-water coral reefs and surrounding habitats

Multibeam surveys were carried out in four areas to the west of Scotland where the coral Lophelia pertusa had previously been recorded. Distinctive seabed mounds were found in one area; video images from the mounds showed coral reef formation, and grab samples recovered L. pertusa reef framework and rubble. Skeleton samples were dated to 3,800 years BP. Grab samples contained 123 species of fauna. The reef structures, termed the Mingulay Reef Complex, were identified as topographic mound-like structures from the bathymetric data and were also visible on the backscatter images. The location of the reefs coincides with Atlantic bottom waters, close to a primary productivity centre and mixing zone, in an area where currents are likely to be accelerated by rocky seafloor ridges. This study shows that multibeam echosounders are powerful tools to locate and map deep-water coral reefs irrespective of water depth. Electronic Supplementary Material Supplementary material is available for this article at and is accessible for authorized users.