Species-Specific Responses of Corals to Bleaching Events on Anthropogenically Turbid Reefs on Okinawa Island,Japan, over a 15-year Period (1995–2009)

Coral bleaching, triggered by elevated sea-surface temperatures (SSTs) has caused a decline in coral cover and changes in the abundances of corals on reefs worldwide. Coral decline can be exacerbated by the effects of local stressors like turbidity, yet some reefs with a natural history of turbidity can support healthy and resilient coral communities. However, little is known about responses of coral communities to bleaching events on anthropogenically turbid reefs as a result of recent (post World War II) terrestrial runoff. Analysis of region-scale coral cover and species abundance at 17–20 sites on the turbid reefs of Okinawa Island (total of 79 species, 30 genera, and 13 families) from 1995 to 2009 indicates that coral cover decreased drastically, from 24.4% to 7.5% (1.1%/year), subsequent to bleaching events in 1998 and 2001. This dramatic decrease in coral cover corresponded to the demise of Acropora species (e.g., A. digitifera) by 2009, when Acropora had mostly disappeared from turbid reefs on Okinawa Island. In contrast, Merulinidae species (e.g., Dipsastraea pallida/speciosa/favus) and Porites species (e.g., P. lutea/australiensis), which are characterized by tolerance to thermal stress, survived on turbid reefs of Okinawa Island throughout the period. Our results suggest that high turbidity, influenced by recent terrestrial runoff, could have caused a reduction in resilience of Acropora species to severe thermal stress events, because the corals could not have adapted to a relatively recent decline in water quality. The coral reef ecosystems of Okinawa Island will be severely impoverished if Acropora species fail to recover.     

Unrecognized coral species diversity masks differences in functional ecology

Porites corals are foundation species on Pacific reefs but a confused taxonomy hinders understanding of their ecosystem function and responses to climate change. Here, we show that what has been considered a single species in the eastern tropical Pacific, Porites lobata, includes a morphologically similar yet ecologically distinct species, Porites evermanni. While P. lobata reproduces mainly sexually, P. evermanni dominates in areas where triggerfish prey on bioeroding mussels living within the coral skeleton, thereby generating asexual coral fragments. These fragments proliferate in marginal habitat not colonized by P. lobata. The two Porites species also show a differential bleaching response despite hosting the same dominant symbiont subclade. Thus, hidden diversity within these reef-builders has until now obscured differences in trophic interactions, reproductive dynamics and bleaching susceptibility, indicative of differential responses when confronted with future climate change.     

Dimethylsulfoniopropionate,superoxide dismutase and glutathione as stress response indicators in three corals under short-term hyposalinity stress

Corals are among the most active producers of dimethylsulfoniopropionate (DMSP), a key molecule in marine sulfur cycling, yet the specific physiological role of DMSP in corals remains elusive. Here, we examine the oxidative stress response of three coral species (Acropora millepora, Stylophora pistillata and Pocillopora damicornis) and explore the antioxidant role of DMSP and its breakdown products under short-term hyposalinity stress. Symbiont photosynthetic activity declined with hyposalinity exposure in all three reef-building corals. This corresponded with the upregulation of superoxide dismutase and glutathione in the animal host of all three species. For the symbiont component, there were differences in antioxidant regulation, demonstrating differential responses to oxidative stress between the Symbiodinium subclades. Of the three coral species investigated, only A. millepora provided any evidence of the role of DMSP in the oxidative stress response. Our study reveals variability in antioxidant regulation in corals and highlights the influence life-history traits, and the subcladal differences can have on coral physiology. Our data expand on the emerging understanding of the role of DMSP in coral stress regulation and emphasizes the importance of exploring both the host and symbiont responses for defining the threshold of the coral holobiont to hyposalinity stress.     

Coral Energy Reserves and Calcification in a High-CO2 World at Two Temperatures

Rising atmospheric CO₂ concentrations threaten coral reefs globally by causing ocean acidification (OA) and warming. Yet, the combined effects of elevated pCO₂ and temperature on coral physiology and resilience remain poorly understood. While coral calcification and energy reserves are important health indicators, no studies to date have measured energy reserve pools (i.e., lipid, protein, and carbohydrate) together with calcification under OA conditions under different temperature scenarios. Four coral species, Acropora millepora, Montipora monasteriata, Pocillopora damicornis, Turbinaria reniformis, were reared under a total of six conditions for 3.5 weeks, representing three pCO₂ levels (382, 607, 741 µatm), and two temperature regimes (26.5, 29.0°C) within each pCO₂ level. After one month under experimental conditions, only A. millepora decreased calcification (−53%) in response to seawater pCO₂ expected by the end of this century, whereas the other three species maintained calcification rates even when both pCO₂ and temperature were elevated. Coral energy reserves showed mixed responses to elevated pCO₂ and temperature, and were either unaffected or displayed nonlinear responses with both the lowest and highest concentrations often observed at the mid-pCO₂ level of 607 µatm. Biweekly feeding may have helped corals maintain calcification rates and energy reserves under these conditions. Temperature often modulated the response of many aspects of coral physiology to OA, and both mitigated and worsened pCO₂ effects. This demonstrates for the first time that coral energy reserves are generally not metabolized to sustain calcification under OA, which has important implications for coral health and bleaching resilience in a high-CO₂ world. Overall, these findings suggest that some corals could be more resistant to simultaneously warming and acidifying oceans than previously expected.     

Effect of habitat characteristics on the distribution and abundance of damselfish within a Red Sea reef

For coral reef fish with an obligate relationship to their habitat, like Pomacentrid damselfish, choosing a suitable home amongst the reef structure is key to survival. A surprisingly small number of studies have examined patterns in adult damselfish distributions compared to other ontogenetic phases. The aim of this study was to determine which reef and coral colony characteristics explained adult damselfish distribution patterns in a Red Sea reef. The characteristics investigated were reef type (continuous or patchy), coral species (seven species of Acropora), and coral morphology (coral size and branching density). The focal damselfish species were Dascyllus aruanus, D. marginatus, Chromis viridis, and C. flavaxilla. Occupancy (presence or absence of resident damselfish), group size and fish species richness were not significantly different between the seven Acropora species. However, within each coral species, damselfish were more likely to occupy larger coral colonies than smaller coral colonies. Occupancy rates were also higher in patchy reef habitats than in continuous sections of the reef, probably because average coral colony size was greater in patchy reef type. Fish group size increased significantly with coral colony volume and with larger branch spacing. Multi-species groups of fish commonly occurred and were increasingly likely with reduced branching density and increased coral size.     

The role of in situ coral nurseries in supporting mobile invertebrate epifauna

Coral nurseries are commonly employed to generate coral material for reef restoration projects, but observations of epifaunal organisms utilising the nurseries for food and shelter indicate that they can also provide important functions beyond that of coral propagation. To examine the level of biodiversity that can be supported by coral nurseries, and investigate if epifaunal communities were influenced by the presence of live coral tissue, we compared the abundance, diversity and community composition of mobile invertebrate epifauna associated with live and dead fragments of three coral species (Pocillopora acuta, Echinopora lamellosa, Platygyra sinensis) that were reared in an in situ nursery. A total of 418 mobile invertebrates spanning 63 taxa were recorded from 22 coral colonies. The three coral species hosted significantly different epifaunal communities, most likely a consequence of the difference in growth forms of the coral hosts. Significant differences in epifaunal communities were only observed between live and dead colonies of P. acuta, indicating that resource provisioning in this species is particularly influenced by the presence of live tissue. Our findings showed that coral nurseries can support a range of mobile invertebrates and function as tools to conserve threatened mobile invertebrates. This ecological function is under-studied and should be assessed in restoration programs for the conservation of corals and associated fauna.     

Les faunes coralliennes de l’Oligocène de Malte : biodiversité et paléoenvironnement

The study of the coral biodiversity of the Upper Oligocene sedimentary series (Lower Coralline Limestone, Chattian) of Malta permitted the identification of 25 scleractinian genera represented by 41 species. Three new species are proposed: Miophora naxxarensis n. sp., Nerthastraea maltensis n. sp. and Gyrosmilia maltensis n. sp. Observations made in various Oligocene sites in Malta, especially around Naxxar and Tal Bajjada, allow to establish a suite of coral associations which may vary spatially and vertically. The identified scleractinian associations can be represented by different types of coral assemblages and bioconstructions: isolated colonies, coral beds of varying density but of large spatial extent, more cohesive coral banks (coral carpets) or patch reefs forming morphologies with gentle lateral slopes. The colonial morphologies are closely linked to these different types of bioconstructions. These coral constructions have been established and developed in shallow marine areas. The coral biodiversity of the Oligocene of Malta fits well in the evolution of the Cenozoic reef phenomenon whose development reached its peak in the Oligocene with great coral richness in the Chattian in the Mediterranean area.     

Coral Fluorescent Proteins as Antioxidants

Background

A wide array of fluorescent proteins (FP) is present in anthozoans, although their biochemical characteristics and function in host tissue remain to be determined. Upregulation of FP''s frequently occurs in injured or compromised coral tissue, suggesting a potential role of coral FPs in host stress responses.

Methodology/Principal Findings

The presence of FPs was determined and quantified for a subsample of seven healthy Caribbean coral species using spectral emission analysis of tissue extracts. FP concentration was correlated with the in vivo antioxidant potential of the tissue extracts by quantifying the hydrogen peroxide (H₂O₂) scavenging rates. FPs of the seven species varied in both type and abundance and demonstrated a positive correlation between H₂O₂ scavenging rate and FP concentration. To validate this data, the H₂O₂ scavenging rates of four pure scleractinian FPs, cyan (CFP), green (GFP), red (RFP) and chromoprotein (CP), and their mutant counterparts (without chromophores), were investigated. In vitro, each FP scavenged H₂O₂ with the most efficient being CP followed by equivalent activity of CFP and RFP. Scavenging was significantly higher in all mutant counterparts.

Conclusions/Significance

Both naturally occurring and pure coral FPs have significant H₂O₂ scavenging activity. The higher scavenging rate of RFP and the CP in vitro is consistent with observed increases of these specific FPs in areas of compromised coral tissue. However, the greater scavenging ability of the mutant counterparts suggests additional roles of scleractinian FPs, potentially pertaining to their color. This study documents H₂O₂ scavenging of scleractinian FPs, a novel biochemical characteristic, both in vivo across multiple species and in vitro with purified proteins. These data support a role for FPs in coral stress and immune responses and highlights the multi-functionality of these conspicuous proteins.     

Antibacterial Activity of Pseudoalteromonas in the Coral Holobiont

Corals harbor diverse and abundant prokaryotic populations. Bacterial communities residing in the coral mucus layer may be either pathogenic or symbiotic. Some species may produce antibiotics as a method of controlling populations of competing microbial species. The present study characterizes cultivable Pseudoalteromonas sp. isolated from the mucus layer of different coral species from the northern Gulf of Eilat, Red Sea, Israel. Six mucus-associated Pseudoalteromonas spp. obtained from different coral species were screened for antibacterial activity against 23 tester strains. Five of the six Pseudoalteromonas strains demonstrated extracellular antibacterial activity against Gram-positive—but not Gram-negative—tester strains. Active substances secreted into the cell-free supernatant are heat-tolerant and inhibit growth of Bacillus cereus, Staphylococcus aureus, and of ten endogenous Gram-positive marine bacteria isolated from corals. The Pseudoalteromonas spp. isolated from Red sea corals aligned in a phylogenetic tree with previously isolated Pseudoalteromonas spp. of marine origin that demonstrated antimicrobial activity. These results suggest that coral mucus-associated Pseudoalteromonas may play a protective role in the coral holobiont's defense against potential Gram-positive coral pathogens.     

Habitat Selectivity and Reliance on Live Corals for Indo-Pacific Hawkfishes (Family: Cirrhitidae)

Hawkfishes (family: Cirrhitidae) are small conspicuous reef predators that commonly perch on, or shelter within, the branches of coral colonies. This study examined habitat associations of hawkfishes, and explicitly tested whether hawkfishes associate with specific types of live coral. Live coral use and habitat selectivity of hawkfishes was explored at six locations from Chagos in the central Indian Ocean extending east to Fiji in the Pacific Ocean. A total of 529 hawkfishes from seven species were recorded across all locations with 63% of individuals observed perching on, or sheltering within, live coral colonies. Five species (all except Cirrhitus pinnulatus and Cirrhitichthys oxycephalus) associated with live coral habitats. Cirrhitichthys falco selected for species of Pocillopora while Paracirrhites arcatus and P. forsteri selected for both Pocillopora and Acropora, revealing that these habitats are used disproportionately more than expected based on the local cover of these coral genera. Habitat selection was consistent across geographic locations, and species of Pocillopora were the most frequently used and most consistently selected even though this coral genus never comprised more than 6% of the total coral cover at any of the locations. Across locations, Paracirrhites arcatus and P. forsteri were the most abundant species and variation in their abundance corresponded with local patterns of live coral cover and abundance of Pocilloporid corals, respectively. These findings demonstrate the link between small predatory fishes and live coral habitats adding to the growing body of literature highlighting that live corals (especially erect branching corals) are critically important for sustaining high abundance and diversity of fishes on coral reefs.     

Responses of massive and branching coral species to the combined effects of water temperature and nitrate enrichment

The branching coral species Pocillopora damicornis (Linnaeus) and the massive coral species Porites lobata Dana were exposed for 30 days to different temperatures and nitrate concentrations to study the response of the coral-zooxanthella symbiosis. Results suggest that the effect of nitrate enrichment on the polyp-zooxanthella symbiosis varies according to the coral morphology. After the experimental period only 30% of P. damicornis colonies remained healthy, in contrast to 90% of P. lobata. The branching P. damicornis was significantly affected by the addition of nitrate, whereas P. lobata was significantly influenced by water temperature. The two species showed enhanced zooxanthella volume, and chlorophyll contents per cell under high nitrate concentrations. The reduced zooxanthellae density in both species indicated a detrimental influence of the interaction of high nitrate and high temperature. Tissue soluble proteins in P. lobata were significantly reduced by elevated temperature. Results showed that tissue soluble proteins and chlorophylls in P. lobata were from two- to three-fold higher than in P. damicornis. The number of zooxanthellae in P. lobata was double that of P. damicornis. Therefore, we suggest that the slow-growing species P. lobata is better able to cope with changing environmental conditions than the fast-growing coral P. damicornis.     

Host Coenzyme Q Redox State Is an Early Biomarker of Thermal Stress in the Coral Acropora millepora

Bleaching episodes caused by increasing seawater temperatures may induce mass coral mortality and are regarded as one of the biggest threats to coral reef ecosystems worldwide. The current consensus is that this phenomenon results from enhanced production of harmful reactive oxygen species (ROS) that disrupt the symbiosis between corals and their endosymbiotic dinoflagellates, Symbiodinium. Here, the responses of two important antioxidant defence components, the host coenzyme Q (CoQ) and symbiont plastoquinone (PQ) pools, are investigated for the first time in colonies of the scleractinian coral, Acropora millepora, during experimentally-induced bleaching under ecologically relevant conditions. Liquid chromatography-mass spectrometry (LC-MS) was used to quantify the states of these two pools, together with physiological parameters assessing the general state of the symbiosis (including photosystem II photochemical efficiency, chlorophyll concentration and Symbiodinium cell densities). The results show that the responses of the two antioxidant systems occur on different timescales: (i) the redox state of the Symbiodinium PQ pool remained stable until twelve days into the experiment, after which there was an abrupt oxidative shift; (ii) by contrast, an oxidative shift of approximately 10% had occurred in the host CoQ pool after 6 days of thermal stress, prior to significant changes in any other physiological parameter measured. Host CoQ pool oxidation is thus an early biomarker of thermal stress in corals, and this antioxidant pool is likely to play a key role in quenching thermally-induced ROS in the coral-algal symbiosis. This study adds to a growing body of work that indicates host cellular responses may precede the bleaching process and symbiont dysfunction.     

The reef-building coral Siderastrea siderea exhibits parabolic responses to ocean acidification and warming

Anthropogenic increases in atmospheric CO₂ over this century are predicted to cause global average surface ocean pH to decline by 0.1–0.3 pH units and sea surface temperature to increase by 1–4°C. We conducted controlled laboratory experiments to investigate the impacts of CO₂-induced ocean acidification (pCO₂ = 324, 477, 604, 2553 µatm) and warming (25, 28, 32°C) on the calcification rate of the zooxanthellate scleractinian coral Siderastrea siderea, a widespread, abundant and keystone reef-builder in the Caribbean Sea. We show that both acidification and warming cause a parabolic response in the calcification rate within this coral species. Moderate increases in pCO₂ and warming, relative to near-present-day values, enhanced coral calcification, with calcification rates declining under the highest pCO₂ and thermal conditions. Equivalent responses to acidification and warming were exhibited by colonies across reef zones and the parabolic nature of the corals'' response to these stressors was evident across all three of the experiment''s 30-day observational intervals. Furthermore, the warming projected by the Intergovernmental Panel on Climate Change for the end of the twenty-first century caused a fivefold decrease in the rate of coral calcification, while the acidification projected for the same interval had no statistically significant impact on the calcification rate—suggesting that ocean warming poses a more immediate threat than acidification for this important coral species.     

Bleaching response of coral species in the context of assemblage response

Caribbean coral reefs are declining due to a mosaic of local and global stresses, including climate change-induced thermal stress. Species and assemblage responses differ due to factors that are not easily identifiable or quantifiable. We calculated a novel species-specific metric of coral bleaching response, taxon-α and -β, which relates the response of a species to that of its assemblages for 16 species over 18 assemblages. By contextualizing species responses within the response of their assemblages, the effects of environmental factors are removed and intrinsic differences among taxa are revealed. Most corals experience either a saturation response, overly sensitive to weak stress (α > 0) but under-responsive compared to assemblage bleaching (β < 1), or a threshold response, insensitive to weak stress (α < 0) but over-responsive compared to assemblage bleaching (β > 1). This metric may help reveal key factors of bleaching susceptibility and identify species as targets for conservation.     

New taxa and revisionary systematics of alcyonacean octocorals from the Pacific coast of North America (Cnidaria,Anthozoa)

A taxonomic assessment of four species of octocorals from the northeastern Pacific Ocean (British Columbia to California) is provided. Included here are a new species of clavulariid stolonifieran Cryptophyton, a new species of the nephtheid soft coral Gersemia, an undetermined species of soft coral in the genus Alcyonium that has been referred in the literature by several other names, and a new genus is named for a plexaurid sea fan originally described in the Indo-Pacific genus Euplexaura. Discussions are included that compare the species to related taxa, or provide revisionary assessments.     

Highly Heterogeneous Bacterial Communities Associated with the South China Sea Reef Corals Porites lutea,Galaxea fascicularis and Acropora millepora

Coral harbor diverse and specific bacteria play significant roles in coral holobiont function. Bacteria associated with three of the common and phylogenetically divergent reef-building corals in the South China Sea, Porites lutea, Galaxea fascicularis and Acropora millepora, were investigated using 454 barcoded-pyrosequencing. Three colonies of each species were sampled, and 16S rRNA gene libraries were constructed individually. Analysis of pyrosequencing libraries showed that bacterial communities associated with the three coral species were more diverse than previous estimates based on corals from the Caribbean Sea, Indo-Pacific reefs and the Red Sea. Three candidate phyla, including BRC1, OD1 and SR1, were found for the first time in corals. Bacterial communities were separated into three groups: P. lutea and G. fascicular, A. millepora and seawater. P. lutea and G. fascicular displayed more similar bacterial communities, and bacterial communities associated with A. millepora differed from the other two coral species. The three coral species shared only 22 OTUs, which were distributed in Alphaproteobacteria, Deltaproteobacteria, Gammaproteobacteria, Chloroflexi, Actinobacteria, Acidobacteria and an unclassified bacterial group. The composition of bacterial communities within each colony of each coral species also showed variation. The relatively small common and large specific bacterial communities in these corals implies that bacterial associations may be structured by multiple factors at different scales and that corals may associate with microbes in terms of similar function, rather than identical species.     

Micro-crevice structure enhances coral spat survivorship

This study examined effects of microstructure (hereafter termed “micro-crevices”) on the surface of settlement substrata, which provides refuge for minute coral spats from grazing and, hence, could enhance coral spat survivorship. Survival of coral spats settling on plain tile-surfaces or in artificially-made micro-crevices on the tile-surfaces were monitored in situ using three scleractinian coral species; Echinophyllia aspera, Favites pentagona, and Platygyra contorta. All coral spats settling on the plain tile-surfaces died without traces of skeleton within the first four months of the experiments while some spats that settled in the micro-crevices still survived by the end of the one-year experimental period with survival rates of up to 12%. The results demonstrated the role of micro-crevice structure enhancing coral spat survivorship in the three coral species. Hence, given grazing activity, micro-crevice structure may be a significant factor influencing development of scleractinian coral communities.     

Variability in the Effects of Macroalgae on the Survival and Growth of Corals: The Consumer Connection

Shifts in dominance from corals to macroalgae are occurring in many coral reefs worldwide. Macroalgal canopies, while competing for space with coral colonies, may also form a barrier to herbivorous and corallivorous fish, offering protection to corals. Thus, corals could either suffer from enhanced competition with canopy-forming and understorey macroalgae or benefit from predator exclusion. Here, we tested the hypothesis that the effects of the brown, canopy-forming macroalga, Turbinaria ornata, on the survival and growth of corals can vary according to its cover, to the presence or absence of herbivorous and corallivorous fish and to the morphological types of corals. Over a period of 66 days, two coral species differing in growth form, Acropora pulchra and Porites rus, were exposed to three different covers of T. ornata (absent versus medium versus high), in the presence or absence of fish. Irrespective of the cover of T. ornata, fish exclusion reduced mortality rates of A. pulchra. Following fish exclusion, a high cover of T. ornata depressed the growth of this branched coral, whilst it had no effect when fish species were present. P. rus suffered no damage from corallivorous fish, but its growth was decreased by high covers of T. ornata, irrespective of the presence or absence of fish. These results show that negative effects of T. ornata on some coral species are subordinate to those of fish predation and are, therefore, likely to manifest only on reefs severely depleted of predators. In contrast, space dominance by T. ornata may decrease the growth of other coral species regardless of predation intensity. In general, this study shows that susceptibility to predation may determine the severity of the effects of canopy-forming macroalgae on coral growth.