Drivers of bacterial diversity dynamics in permeable carbonate and silicate coral reef sands from the Red Sea

Permeable sediments and associated microbial communities play a fundamental role in nutrient recycling within coral reef ecosystems by ensuring high levels of primary production in oligotrophic environments. A previous study on organic matter degradation within biogenic carbonate and terrigenous silicate reef sands in the Red Sea suggested that observed sand-specific differences in microbial activity could be caused by variations in microbial biomass and diversity. Here, we tested this hypothesis by comparing bacterial abundance and community structure in both sand types, and by further exploring the structuring effects of time (season) and space (sediment depth, in/out-reef). Changes in bacterial community structure, as determined via automated ribosomal intergenic spacer analysis (ARISA), were primarily driven by sand mineralogy at specific seasons, sediment depths and reef locations. By coupling ARISA with 16S-ITS rRNA sequencing, we detected significant community shifts already at the bacterial class level, with Proteobacteria (Gamma-, Delta-, Alpha-) and Actinobacteria being prominent members of the highly diverse communities. Overall, our findings suggest that reef sand-associated bacterial communities vary substantially with sand type. Especially in synergy with environmental variation over time and space, mineralogical differences seem to play a central role in maintaining high levels of bacterial community heterogeneity. The local co-occurrence of carbonate and silicate sands may thus significantly increase the availability of microbial niches within a single coral reef ecosystem.     

The deep-water coral Lophelia pertusa in Norwegian waters: distribution and fishery impacts

The paper presents documentation on the distribution of, and damages to, deep-water reefs of the coral Lophelia pertusa in Norwegian waters. The reef areas have traditionally been rich fishing grounds for long-line and gillnet fisheries, and the coral habitat is known to support a high diversity of benthic species. Anecdotal reports claim that trawlers often use the gear, wires, chains and trawl doors to crush the corals and clear the area before fishing starts. To get an overview of the situation, information about the distribution and damage were collected from the literature, fishermen, and our own investigations. The results show that the corals are abundant particularly on the mid Norwegian continental shelf between 200 and 400 m depth. In general it seems that the largest densities are distributed along the continental break and at ridges of morainic origin. The reports from fishermen suggested severe damage to the corals and in situ observations using ROV confirmed the presence of mechanically damaged corals located on trawling grounds. A first estimate of the fishery impact indicates that between 30 and 50% of the reef areas are damaged or impacted. Fishermen claim that catches are significantly lowered in areas where the reefs are damaged. Potential ecological consequences of the destruction are discussed.     

The status of coral reef ecology research in the Red Sea

The Red Sea has long been recognized as a region of high biodiversity and endemism. Despite this diversity and early history of scientific work, our understanding of the ecology of coral reefs in the Red Sea has lagged behind that of other large coral reef systems. We carried out a quantitative assessment of ISI-listed research published from the Red Sea in eight specific topics (apex predators, connectivity, coral bleaching, coral reproductive biology, herbivory, marine protected areas, non-coral invertebrates and reef-associated bacteria) and compared the amount of research conducted in the Red Sea to that from Australia’s Great Barrier Reef (GBR) and the Caribbean. On average, for these eight topics, the Red Sea had 1/6th the amount of research compared to the GBR and about 1/8th the amount of the Caribbean. Further, more than 50 % of the published research from the Red Sea originated from the Gulf of Aqaba, a small area (<2 % of the area of the Red Sea) in the far northern Red Sea. We summarize the general state of knowledge in these eight topics and highlight the areas of future research priorities for the Red Sea region. Notably, data that could inform science-based management approaches are badly lacking in most Red Sea countries. The Red Sea, as a geologically “young” sea located in one of the warmest regions of the world, has the potential to provide insight into pressing topics such as speciation processes as well as the capacity of reef systems and organisms to adapt to global climate change. As one of the world’s most biodiverse coral reef regions, the Red Sea may yet have a significant role to play in our understanding of coral reef ecology at a global scale.     

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.     

Vertical zonation of coral reef fishes in the Sudanese Red Sea

The vertical zonation of 38 species of fish inhabiting coral reefs in the Sudanese Red Sea is described. A marked degree of vertical zonation of the fishes is shown to exist. The usefulness of a depth oriented survey method for studying reef fish is discussed in relation to these results.General relationships between vertical zonation and species diversity are noted.     

High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii

The Hawaiian Islands represent one of the most geographically remote locations in the Indo-Pacific, and are a refuge for rare, endemic life. The diversity of symbiotic dinoflagellates (Symbiodinium sp.) inhabiting zooxanthellate corals and other symbiotic cnidarians from the High Islands region was surveyed. From the 18 host genera examined, there were 20 genetically distinct symbiont types (17 in clade C, 1 in clade A, 1 in clade B, and 1 in clade D) distinguished by internal transcribed spacer region 2 sequences. Most types were found to associate with a particular host genus or species and nearly half of them have not been identified in surveys of Western and Eastern Pacific hosts. A clear dominant generalist symbiont is lacking among Hawaiian cnidarians. This is in marked contrast with the symbiont community structures of the western Pacific and Caribbean, which are dominated by a few prevalent generalist symbionts inhabiting numerous host taxa. Geographic isolation, low host diversity, and a high proportion of coral species that directly transmit their symbionts from generation to generation are implicated in the formation of a coral reef community exhibiting high symbiont diversity and specificity.Communicated by H.R. Lasker     

Beta diversity of cold-water coral reef communities off western Scotland

Spatial heterogeneity in coral reef communities is well documented. This “species turnover” (beta diversity) on shallow warm-water reefs strongly conforms to spatial gradients in the environment as well as spatially autocorrelated biotic processes such as dispersal and competition. But the extent to which the environment and spatial autocorrelation create beta diversity on deep cold-water coral reefs such as those formed by Lophelia pertusa (Scleractinia) is unknown. The effects of remotely sensed and ground-truthed data were tested on the community composition of sessile suspension-feeding communities from the Mingulay Reef Complex, a landscape of inshore Lophelia reefs off the Scottish west coast. Canonical correspondence analysis determined that a statistically significant proportion (68%) of the variance in community composition could be explained by remotely sensed environmental variables (northerly and easterly aspect, seabed rugosity, depth), ground-truthed environmental variables (species richness and reef macrohabitat) and geospatial location. This variation was further partitioned into fractions explained by pure effects of the environment (51%), spatially structured environmental variables (12%) and spatial autocorrelation (5%). Beta diversity in these communities reflected the effects of both measured and unmeasured and spatially dependent environmental variables that vary across the reef complex, i.e., hydrography. Future work will quantify the significance and relative contributions of these variables in creating beta diversity in these rich communities.     

Variation in diversity of coral reef fish between French Polynesian atolls

The diversity of coral reef fish in seven atolls in French Polynesia is analyzed with respect to geomorphological characteristics of the atolls. The results show that size of the lagoon is more important than confinement in affecting overall fish diversity. This result suggests that island biogeographic theory, as developed by MacArthur and Wilson for terrestrial animals, also applies to reef fish in that more area gives more habitat complexity which, in turn, supports higher fish diversity. However, species diversity within a given family appears to be affected more by ecological parameters, such as living coral cover, food diversity, and reproductive behavior, than geomorphological features.     

Heavy metals distribution in the coral reef ecosystems of the Northern Red Sea

Concentrations of seven heavy metals (Cu, Zn, Pb, Cd, Ni, Co and Fe) were measured in the seawater, sediments, common scleractinian reef-building corals and soft corals (Octocorallia : Alcyonacea) at seven reef sites in the Northern Red Sea: I (Hurghada), II (Ras Za’farana), III (El-Ain Al-Sukhna), IV (El-Tur), V (Sha’b Rashdan), VI (Sharm El-Sheikh) and VII (Dahab). Levels of heavy metals were considerably elevated in seawater, sediments and corals collected from reef sites exposed to increased environmental contamination, as a result of diversified natural and anthropogenic inputs. Soft corals of genera Lithophyton, Sarcophyton and Sinularia showed higher concentrations of Zn, Pb, Cd and Ni than hard coral genera Acropora and Stylophora. Soft coral Sarcophyton trocheliophorum collected from El Ain Al-Suhkna (Gulf of Suez) had greater concentration of Cu, followed by hard corals Acropora pharaonis and Acropora hemprichi. The elevated levels of Zn, Cd and Ni were reported in the dry tissue of soft coral Sinularia spp. On the other hand, the soft coral Lithophyton arboreum displayed the highest concentration of Pb at Sha’b Rashdan (Gulf of Suez) and elevated concentration of Zn at Sharm El-Sheikh. Sediments showed significantly higher concentration of Fe than corals. The higher levels of Fe in hard corals than soft corals reflected the incorporation of Fe into the aragonite and the chelation with the organic matrix of the skeleton. The greater abundance of soft corals in metal-contaminated reef sites and the elevated levels of metals in their tissue suggesting that the soft corals could develop a tolerance mechanism to relatively high concentrations of metals. Although the effects of heavy metals on reef corals were not isolated from the possible effects of other stresses, the percentage cover of dead corals were significantly higher as the concentrations of heavy metals increased.     

Bacterial diversity associated with the Brazilian endemic reef coral Mussismilia braziliensis

Aims:  We performed the first characterization of the microbiota associated with the reef coral Mussismilia braziliensis by means of a culture-independent approach.
Methods and Results:  The main groups were Proteobacteria , Cyanobacteria and unclassified bacteria according to the 16S rDNA libraries. Most of the sequences of the mucus of healthy and diseased M. braziliensis did not find close matches in GenBank (i.e. >97% 16S rDNA similarity). Most of the sequences of seawater and mucus of healthy coral fell into tight clusters (17 and 15 clusters respectively). In contrast, most of the sequences of mucus of diseased coral did not form clusters. The rarefaction curves indicate saturation in the recovery of higher taxa (approximately 40 phyla). However, the number of species in the coral mucus ( n  = 130–170) and seawater ( n  = 170) did not reach a plateau.
Conclusions:  The coral microbiota encompasses several potentially novel species and higher taxa. The microbiota of M. braziliensis appears to be species-specific. Diseased coral may have provided a suitable place for colonization by opportunistic bacteria, resulting in a greater bacterial diversity.
Significance and Impact of the Study:  The first study on the diversity of the microbiota of the endemic and endangered of extinction coral M. braziliensis .     

Associations between climate stress and coral reef diversity in the western Indian Ocean

Climatic–oceanographic stress and coral reef diversity were mapped in the western Indian Ocean (WIO) in order to determine if there were associations between high diversity coral reefs and regions with low‐to‐moderate climate stress. A multivariate stress model developed to estimate environmental exposure to stress, an empirical index of the coral community's susceptibility to stress, and field data on numbers of fish and corals taxa from 197 WIO sites were overlain to evaluate these associations. Exposure to stress was modeled from satellite data based on nine geophysical–biological oceanographic characteristics known to influence coral bleaching (i.e. temperature, light, and current variables). The environmental stress model and the coral community's susceptibility index were moderately correlated (r=?0.51) with southern and eastern parts of the WIO identified as areas with low environmental stress and coral communities with greater dominance of bleaching stress‐sensitive taxa. Numbers of coral and fish taxa were positive and moderately correlated (r=0.47) but high diversity regions for fish were in the north and west while diversity was highest for corals in central regions from Tanzania to northwestern Madagascar. Combining three and four of these variables into composite maps identified a region from southern Kenya to northern Mozambique across to northern–eastern Madagascar and the Mascarene Islands and the Mozambique–South Africa border as areas where low‐moderate environmental exposure overlaps with moderate‐high taxonomic diversity. In these areas management efforts aimed at maintaining high‐diversity and intact ecosystems are considered least likely to be undermined by climate disturbances in the near term. Reducing additional human disturbances, such as fishing and pollution, in these areas is expected to improve the chances for their persistence. These reefs are considered a high priority for increased local, national, and international management efforts aimed at establishing coral reef refugia for climate change impacts.     

Methane assimilation and trophic interactions with marine Methylomicrobium in deep-water coral reef sediment off the coast of Norway

Deep-water coral reefs are seafloor environments with diverse biological communities surrounded by cold permanent darkness. Sources of energy and carbon for the nourishment of these reefs are presently unclear. We investigated one aspect of the food web using DNA stable-isotope probing (DNA-SIP). Sediment from beneath a Lophelia pertusa reef off the coast of Norway was incubated until assimilation of 5 micromol 13CH4 g(-1) wet weight occurred. Extracted DNA was separated into 'light' and 'heavy' fractions for analysis of labelling. Bacterial community fingerprinting of PCR-amplified 16S rRNA gene fragments revealed two predominant 13C-specific bands. Sequencing of these bands indicated that carbon from 13CH4 had been assimilated by a Methylomicrobium and an uncultivated member of the Gammaproteobacteria. Cloning and sequencing of 16S rRNA genes from the heavy DNA, in addition to genes encoding particulate methane monooxygenase and methanol dehydrogenase, all linked Methylomicrobium with methane metabolism. Putative cross-feeders were affiliated with Methylophaga (Gammaproteobacteria), Hyphomicrobium (Alphaproteobacteria) and previously unrecognized methylotrophs of the Gammaproteobacteria, Alphaproteobacteria, Deferribacteres and Bacteroidetes. This first marine methane SIP study provides evidence for the presence of methylotrophs that participate in sediment food webs associated with deep-water coral reefs.     

Reduced Symbiodiniaceae diversity in Palythoa tuberculosa at a heavily acidified coral reef

Symbiodiniaceae diversity in hosts is known to change with the environment and particularly with temperature and light intensity. However, higher levels of pCO₂, as could be expected under future ocean acidification scenarios, have been documented to show little to no effect in influencing the diversity of Symbiodiniaceae in hosts in previous studies. In this study, we examined hypervariable psbA^ncr sequences to identify the Cladocopium (former Symbiodinium ‘Clade C’) diversity within the zooxanthellate zoantharian Palythoa tuberculosa at an acidified reef in southern Japan. Palythoa tuberculosa were collected from a reef at the volcanic island of Iwotorishima in southern Japan; specimens from a high pCO₂ site and from a nearby control (normal pCO₂) site (Inoue et al. in Nat Clim Change 3:683–687, 2013). We observed a statistically significant reduction in Cladocopium diversity at the high pCO₂ site with only one Cladocopium lineage present, compared to at the control site with two lineages present. Our results demonstrate that higher pCO₂ can potentially negatively influence the diversity of host Symbiodiniaceae within anthozoan hosts, an important implication in the face of ongoing ocean acidification and climate change.

     

Endemic and widespread coral reef fishes have similar mitochondrial genetic diversity

Endemic species are frequently assumed to have lower genetic diversity than species with large distributions, even if closely related. This assumption is based on research from the terrestrial environment and theoretical evolutionary modelling. We test this assumption in the marine environment by analysing the mitochondrial genetic diversity of 33 coral reef fish species from five families sampled from Pacific Ocean archipelagos. Surprisingly, haplotype and nucleotide diversity did not differ significantly between endemic and widespread species. The probable explanation is that the effective population size of some widespread fishes locally is similar to that of many of the endemics. Connectivity across parts of the distribution of the widespread species is probably low, so widespread species can operate like endemics at the extreme or isolated parts of their range. Mitochondrial genetic diversity of many endemic reef fish species may not either limit range size or be a source of vulnerability.     

Long-term persistence of low coral cover and abundance on a disturbed coral reef flat in the northern Red Sea

Levels of coral cover and abundance on a coral reef flat in Eilat (Israeli Red Sea) were estimated in 2001 by surveying nineteen 10-m transects, and compared to the levels reported in the same area between 1966 and 1973. Lower values compared to 1966 levels are evident, and there has been only a modest recovery following a catastrophic low tide that killed a large proportion of the corals in 1970. Percent cover of soft and stony corals (16.1%) was less than half of that reported for 1969 (35%), when a sharp decrease in coral abundance had already been observed. The total number of soft and stony coral colonies observed was 300, compared to 541 in 1966. In contrast to 1966, when half of the transects surveyed contained more than 30 coral colonies, no transects with this number of corals were observed. The cover of seven of the most common stony coral species was 841 cm, which is twice the coral cover of that in 1973, but only 22% of the 1969 level. Millepora dichotoma, an abundant species before 1970, has almost disappeared, and the soft coral Litophyton, abundant in 1972, was not observed. Anthropogenic nutrient enrichment is apparently among the causes for the lack of coral recovery in the studied reef flat. Reefs located further away from sources of pollution have recovered quickly after natural and anthropogenic disturbances and have retained their coral abundance and diversity.     

Genotypic diversity and spatial-temporal distribution of Symbiodinium clones in an abundant reef coral

Genetic data are rapidly advancing our understanding of various biological systems including the ecology and evolution of coral-algal symbioses. The fine-scale interactions between individual genotypes of host and symbiont remain largely unstudied and constitute a major gap in knowledge. By applying microsatellite markers developed for both host and symbiont, we investigated the intracolony diversity, prevalence and stability of Symbiodinium glynni (type D1) multilocus genotypes in association with dense populations of Pocillopora at two sites in the Gulf of California. The genetic diversity and allelic frequencies in reef populations of S. glynni remained stable over 3 years. Common clone genotypes persisted over this period, and no temporal population subdivision (Φ(PT) = 0.021 and -0.003) was detected. Collections from circular plots showed no statistical correlation between related Pocillopora individuals and their associations with particular S. glynni genotypes, with no spatial structuring or clonal aggregation across a reef for the symbiont. From permanent linear transects, samples were analysed from multiple locations within a colony and some were resampled approximately 1 year later. Many of these multisampled colonies (approximately 53%) were dominated by a single S. glynni genotype and tended to associate with the same symbiont genotype(s) over time, while colony ramets often possessed unrelated symbiont genotypes. In contrast to the species level, associations between genotypes of Pocillopora and S. glynni are apparently more flexible over space and time. The abundance of sexually recombinant genotypes of S. glynni combined with greater flexibility might provide adaptive mechanisms for these symbioses to evolve rapidly to changes in environmental conditions and allow particular symbiont genotypes to spread through a host population.     

Red Sea coral reef trajectories over 2 decades suggest increasing community homogenization and decline in coral size

Three independent line intercept transect surveys on northern Red Sea reef slopes conducted in 1988/9 and 1997/8 in Egypt and from 2006-9 in Saudi Arabia were used to compare community patterns and coral size. Coral communities showed scale-dependent variability, highest at fine spatial and taxonomic scale (species-specific within and among reef patterns). At coarser scale (generic pattern across regions), patterns were more uniform (regionally consistent generic dominance on differently exposed reef slopes and at different depths). Neither fine- nor coarse-scale patterns aligned along the sampled 1700 km latitudinal gradient. Thus, a latitudinal gradient that had been described earlier from comparable datasets, separating the Red Sea into three faunistic zones, was no longer apparent. This may indicate subtle changes in species distributions. Coral size, measured as corrected average intercept of corals in transects, had decreased from 1997 to 2009, after having remained constant from 1988 to 1997. Recruitment had remained stable (～12 juvenile corals per m(2)). Size distributions had not changed significantly but large corals had declined over 20 years. Thus, data from a wide range of sites taken over two decades support claims by others that climate change is indeed beginning to show clear effects on Red Sea reefs.     

Genetic diversity and connectivity in a brooding reef coral at the limit of its distribution

Remote populations are predicted to be vulnerable owing to their isolation from potential source reefs, and usually low population size and associated increased extinction risk. We investigated genetic diversity, population subdivision and connectivity in the brooding reef coral Seriatopora hystrix at the limits of its Eastern Australian (EA) distribution and three sites in the southern Great Barrier Reef (GBR). Over the approximately 1270 km survey range, high levels of population subdivision were detected (global F_ST = 0.224), with the greatest range in pairwise F_ST values observed among the three southernmost locations: Lord Howe Island, Elizabeth Reef and Middleton Reef. Flinders Reef, located between the GBR and the more southerly offshore reefs, was highly isolated and showed the signature of a recent bottleneck. High pairwise F_ST values and the presence of multiple genetic clusters indicate that EA subtropical coral populations have been historically isolated from each other and the GBR. One putative first-generation migrant was detected from the GBR into the EA subtropics. Occasional long-distance dispersal is supported by changes in species composition at these high-latitude reefs and the occurrence of new species records over the past three decades. While subtropical populations exhibited significantly lower allelic richness than their GBR counterparts, genetic diversity was still moderately high. Furthermore, subtropical populations were not inbred and had a considerable number of private alleles. The results suggest that these high-latitude S. hystrix populations are supplemented by infrequent long-distance migrants from the GBR and may have adequate population sizes to maintain viability and resist severe losses of genetic diversity.     

High diversity,abundance and distinct fish assemblages on submerged coral reef pinnacles compared to shallow emergent reefs

Coral Reefs - Coral reefs exhibit consistent patterns in biodiversity across multiple spatial scales, from local to global clines in species richness, abundance and community structure. Knowledge...