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Distinguishing coral species is not only crucial for physiological, ecological, and evolutionary studies but also to enable effective management of threatened reef ecosystems. However, traditional hypotheses that delineate coral species based on morphological traits from the coral skeleton are frequently at odds with tree-based molecular approaches. Additionally, a dearth of species-level molecular markers has made species delimitation particularly challenging in species-rich coral genera, leading to the widespread assumption that interspecific hybridization might be responsible for this apparent conundrum. Here, we used three lines of evidence—morphology, breeding trials, and molecular approaches—to identify species boundaries in a group of ecologically important tabular Acropora corals. In contrast to previous studies, our morphological analysis yielded groups that were congruent with experimental crosses as well as with coalescent-based and allele sharing-based multilocus approaches to species delimitation. Our results suggest that species of the genus Acropora are reproductively isolated and independently evolving units that can be distinguished morphologically. These findings not only pave the way for a taxonomic revision of coral species but also outline an approach that can provide a solid basis to address species delimitation and provide conservation support to a wide variety of keystone organisms. [Acropora; coral reefs; hybridization; reproductive isolation; taxonomy.]

The endosymbiosis between most corals and their photosynthetic dinoflagellate partners begins early in the host life history, when corals are larvae or juvenile polyps. The capacity of coral larvae to buffer climate-induced stress while in the process of symbiont acquisition could come with physiological trade-offs that alter behaviour, development, settlement and survivorship. Here we examined the joint effects of thermal stress and symbiosis onset on colonization dynamics, survival, metamorphosis and host gene expression of Acropora digitifera larvae. We found that thermal stress decreased symbiont colonization of hosts by 50% and symbiont density by 98.5% over 2 weeks. Temperature and colonization also influenced larval survival and metamorphosis in an additive manner, where colonized larvae fared worse or prematurely metamorphosed more often than noncolonized larvae under thermal stress. Transcriptomic responses to colonization and thermal stress treatments were largely independent, while the interaction of these treatments revealed contrasting expression profiles of genes that function in the stress response, immunity, inflammation and cell cycle regulation. The combined treatment either cancelled or lowered the magnitude of expression of heat-stress responsive genes in the presence of symbionts, revealing a physiological cost to acquiring symbionts at the larval stage with elevated temperatures. In addition, host immune suppression, a hallmark of symbiosis onset under ambient temperature, turned to immune activation under heat stress. Thus, by integrating the physical environment and biotic pressures that mediate presettlement event in corals, our results suggest that colonization may hinder larval survival and recruitment under projected climate scenarios.

The vast majority of scleractinian corals are either simultaneous hermaphrodites or gonochoric. Exceptions to these are rare. Nevertheless, species belonging to the family Fungiidae are known to exhibit a wide variety of reproductive strategies. We examined the reproductive ecology of the mushroom coralFungia fungitesin Okinawa. Our study was conducted as part of a long-term, wide-ranging project (2009–2010 and 2013–2017) which explored the unique reproductive strategies of several species belonging to the family Fungiidae. Here we report the co-occurrence of males, females, and hermaphrodite individuals in a long-term monitored population of the reproductively atypical brooder coralF. fungiteswithin the family Fungiidae.F. fungitesstatus as a single-polyped solitary coral, was used to perform manipulative experiments to determine the degree of dependence of an individual coral on its conspecific neighbors for reproduction, and examined whether a constant sperm supply is obligatory for the continuous production of planulae. Isolated females ofF. fungitesexhibited a distinctive reproductive strategy, expressed in continuously releasing planulae also in the absence of males. Observations conducted on a daily basis for 2.5months (throughout the reproductive season of 2015) revealed that some of these individuals released planulae continuously, often between tens and hundreds every day. In an effort to explain this phenomenon, three hypotheses are discussed: (1) Self-fertilization; (2) Asexual production of planulae (i.e., parthenogenetic larvae); and (3) Extended storage of sperm. Finally, we emphasize the importance of continuous and long-term monitoring of studies of coral reproduction; through further genetic studies of coral populations representing a broad range of species and their larval origin.

As global temperatures continue to rise, corals are being exposed to increasing heat stress throughout their early life stages; however, the impact of this phenomenon is poorly understood. We exposed the reef-building coral Acropora tenuis juveniles to ∼26-28 °C (control) and ∼ 31 °C (heat stress) for one week per year over three consecutive years. In the first year of heat stress,96 % of juveniles survived despite symbiotic algal densities in juvenile corals declining. In comparison, survival rates in the third year of heat stress declined to 50 %. Survival rates under natural conditions after stress also gradually decreased in the stressed groups. The rate in the reduction of survivorship was prominent in the consecutive thermally stressed groups (juveniles stressed twice in two years). Symbiotic algal density and photosynthetic activity (Fv/Fm) also declined in stressed juvenile groups. However, heat stress did not significantly affect the growth of juveniles. In the third year of heat stress, temperature negatively affected the physiology of juveniles in terms of survivorship, brightness (an indicator of bleaching), symbiotic algal density, and photosynthetic efficiency. Stress across consecutive years appeared to cause the survivorship of juvenile corals to decline, with three years of stress contributing to the severe decline of a reef. In conclusion, A. tenuis juveniles are not able to acclimatize to heat stress, with successive heat waves of7 days in the summer potentially negatively affecting resilience.

Larval dispersal and postsettlement survival of corals play significant roles in the maintenance of coral populations. Most corals acquire their symbiotic algae (Symbiodiniaceae) from the environment in each generation (horizontal transmission). For horizontal transmitters, the quick establishment of symbiosis is important for their survival, since the photosynthetic activity of symbiotic algae provides energy. However, recent studies have indicated that oxidative stress resulting from photosynthesis might also harm coral larvae. Therefore, it remains unclear whether symbionts contribute energy sources along with intrinsic lipids from eggs and assist in settlement/metamorphosis in early life stages. In the present study, we show that symbiotic algae contribute supplemental energy and are also associated with settlement. Furthermore, although juveniles acquired symbiotic algae after settlement, the acquisition of symbiotic algae in the larval stages caused higher growth (number of polyps and size) and low mortality in the juvenile stage. Our data suggest that symbiotic larvae potentially have longer dispersal periods due to their lower lipid consumption rates, which make them better able to retain buoyancy and motility, increasing the ability of symbiotic larvae to settle in favored locations compared with aposymbiotic larvae. Moreover, postsettlement juveniles may continue to benefit from symbiotic relationships formed during the larval stage. Overall, these findings reveal that the effects of symbiotic algae on Acropora tenuis coral larvae are beneficial, particularly under normal seawater temperature conditions.

The endosymbiosis between most corals and their photosynthetic dinoflagellate partners begins early in the host life history, when corals are larvae or juvenile polyps. The capacity of coral larvae to buffer climate-induced stress while in the process of symbiont acquisition could come with physiological trade-offs that alter larval behavior, development, settlement and survivorship. Here we examined the joint effects of thermal stress and symbiosis onset on colonization dynamics, survival, metamorphosis and host gene expression of Acropora digitifera larvae. We found that thermal stress decreased symbiont colonization of hosts by 50% and symbiont density by 98.5% over two weeks. Temperature and colonization also influenced larval survival and metamorphosis in an additive manner, where colonized larvae fared worse or prematurely metamorphosed more often than non-colonized larvae under thermal stress. Transcriptomic responses to colonization and thermal stress treatments were largely independent, while the interaction of these treatments revealed contrasting expression profiles of genes that function in the stress response, immunity, inflammation and cell cycle regulation. The combined treatment either canceled or lowered the magnitude of expression of heat-stress responsive genes in the presence of symbionts, revealing a physiological cost to acquiring symbionts at the larval stage with elevated temperatures. In addition, host immune suppression, a hallmark of symbiosis onset under ambient temperature, turned to immune activation under heat stress. Thus, by integrating the physical environment and biotic pressures that mediate pre-settlement event in corals, our results suggest that colonization may hinder larval survival and recruitment creating isolated, genetically similar populations under projected climate scenarios.

Many corals establish symbiosis with Symbiodiniaceae cells from surrounding environments, but very few Symbiodiniaceae cells exist in the water column. Given that the N-acetyl-D-glucosamine-binding lectin ActL attracts Symbiodiniaceae cells, we hypothesized that corals must attract Symbiodiniaceae cells using ActL to acquire them. Anti-ActL antibody inhibited acquisition of Symbiodiniaceae cells, and rearing seawater for juvenile Acropora tenuis contained ActL, suggesting that juvenile A. tenuis discharge ActL to attract these cells. Among eight Symbiodiniaceae cultured strains, ActL attracted NBRC102920 (Symbiodinium tridacnidorum) most strongly followed by CS-161 (Symbiodinium tridacnidorum), CCMP2556 (Durusdinium trenchii), and CCMP1633 (Breviolum sp.), however, it did not attract GTP-A6-Sy (Symbiodinium natans), CCMP421 (Effrenium voratum), FKM0207 (Fugacium sp.), and CS-156 (Fugacium sp.). Juvenile polyps of A. tenuis acquired limited Symbiodiniaceae cell strains, and the number of acquired Symbiodiniaceae cells in a polyp also differed from each other. The number of Symbiodiniaceae cells acquired by juvenile polyps of A. tenuis was correlated with the ActL chemotactic activity. Thus, ActL could be used to attract select Symbiodiniaceae cells and help Symbiodiniaceae cell acquisition in juvenile polyps of A. tenuis, facilitating establishment of symbiosis between A. tenuis and Symbiodiniaceae cells.

This study provides the first report of reflectance spectra of coral-spawn slicks and their detection using optical satellite data. The reflectance spectra show that coral-spawn slicks can be discriminated from other sea-surface features such as wave foam and floating Sargassum. Analysis of Planet Dove and Sentinel-2B imagery allowed successful detection of coral-spawn slicks at Ishigaki Island, Okinawa, Japan (24°31′40″N, 124°17′31″E), by using reflectance values in the green and red wavelength regions. This detection was attributable to both their high spatial resolution (3.7 m and 10 m, respectively) and high temporal resolution (1 day and 5 days, respectively), given that coral spawning occurs within a short period (up to several days), typically once a year, and that the coral-spawn slicks have narrow widths of ~10 m. The number of the detected coral-spawn slicks was small, possibly because of coral decline around Ishigaki Island caused by the 2016 worldwide mass coral bleaching event. High-frequency satellite observations, including those from satellite constellations, should provide a powerful tool for understanding coral-reef processes and features whose detection requires high spatial and temporal resolution., 論文

Coral reefs are the epitome of species diversity, yet the number of described scleractinian coral species, the framework-builders of coral reefs, remains moderate by comparison. DNA sequencing studies are rapidly challenging this notion by exposing a wealth of undescribed diversity, but the evolutionary and ecological significance of this diversity remains largely unclear. Here, we present an annotated genome for one of the most ubiquitous corals in the Indo-Pacific (Pachyseris speciosa), and uncover through a comprehensive genomic and phenotypic assessment that it comprises morphologically indistinguishable, but ecologically divergent cryptic lineages. Demographic modelling based on whole-genome resequencing disproved that morphological crypsis was due to recent divergence, and instead indicated ancient morphological stasis. Although the lineages occur sympatrically across shallow and mesophotic habitats, extensive genotyping using a rapid diagnostic assay revealed differentiation of their ecological distributions. Leveraging “common garden” conditions facilitated by the overlapping distributions, we assessed physiological and quantitative skeletal traits and demonstrated concurrent phenotypic differentiation. Lastly, spawning observations of genotyped colonies highlighted the potential role of temporal reproductive isolation in the limited admixture, with consistent genomic signatures in genes related to morphogenesis and reproduction. Overall, our findings demonstrate how ecologically and phenotypically divergent coral species can evolve despite morphological stasis, and provide new leads into the potential mechanisms facilitating such divergence in sympatry. More broadly, they indicate that our current taxonomic framework for reef-building corals may be scratching the surface of the ecologically relevant diversity on coral reefs, consequently limiting our ability to protect or restore this diversity effectively.

Anthropogenic CO2 emissions are contributing to global warming and ocean acidification. Rapid and accurate measurements of seawater carbonate chemistry are critical to understand current changes in the ocean and to predict future effects of such changes on marine organisms and ecosystems. Total alkalinity (AT) measurements can be used to directly determine the calcification rate, but they are time-consuming and require large sample volumes. Herein, we describe an automated and transportable flow-through system that can conduct continuous AT measurement using an ion sensitive field effect transistor (ISFET) – Ag/AgCl sensor and three different reference materials. The response time, stability, and uncertainty of our system were evaluated by comparing AT values of calibrated reference materials to those calculated by our system. Our system requires only small amounts of seawater (

Dinoflagellates in the family Symbiodiniaceae are intensively investigated as algal symbionts of corals and other invertebrates, underpinning coral reef ecosystems as primary producers. Diversity, including regional diversification, of free-living communities is less studied. In this study, an environmental Symbiodiniaceae community at an isolated island, Okinotori Island, Japan, was investigated to determine whether the community is endemic or common with other locations near continents and major ocean currents. Symbiotic algae in common corals at the island were the same type as those of the corals from other Japanese waters. In the environmental samples, genera Symbiodinium (formerly clade A), Cladocopium (clade C), Durusdinium (clade D), and clades F (including Freudenthalidium), G, and I, were identified through analysis of internal transcribed spacer region 2 of nuclear ribosomal RNA gene (ITS2) sequences. Interestingly, some sequences found were genetically different from those of previously reported genera/clades. These unknown sequences were genetically included in the Symbiodiniaceae linage, but they were differentiated from the previously known nine clades. The sequences formed a cluster in the phylogenetic tree based on 28S nrDNA. These sequences were thus considered members of a novel clade in the family (clade J). In total, 120 kinds of ITS2 sequences were produced; while 10 were identical to previously reported sequences, the majority were highly divergent. These genetically unique Symbiodiniaceae types, including novel clade J, may have evolved in isolation and reflect the environmental characteristics of the Okinotori Island.

Since the discovery of Chromera velia as a novel coral-associated microalga, this organism has attracted interest because of its unique evolutionary position between the photosynthetic dinoflagellates and the parasitic apicomplexans. The nature of the relationship between Chromera and its coral host is controversial. Is it a mutualism, from which both participants benefit, a parasitic relationship, or a chance association? To better understand the interaction, larvae of the common Indo-Pacific reef-building coral Acropora digitifera were experimentally infected with Chromera, and the impact on the host transcriptome was assessed at 4, 12, and 48 h post-infection using Illumina RNA-Seq technology. The transcriptomic response of the coral to Chromera was complex and implies that host immunity is strongly suppressed, and both phagosome maturation and the apoptotic machinery is modified. These responses differ markedly from those described for infection with a competent strain of the coral mutualist Symbiodinium, instead resembling those of vertebrate hosts to parasites and/or pathogens such as Mycobacterium tuberculosis. Consistent with ecological studies suggesting that the association may be accidental, the transcriptional response of A. digitifera larvae leads us to conclude that Chromera could be a coral parasite, commensal, or accidental bystander, but certainly not a beneficial mutualist., 論文

Natural light cycles are important for synchronizing behavioural and physiological rhythms over varying time periods in both plants and animals. An endogenous clock, regulated by positive and negative elements, interacting in feedback loops controls these rhythms. Many corals exhibit diel cycles of polyp expansion and contraction entrained by solar light patterns and monthly cycles of spawning or planulation that correspond to nocturnal lunar light cycles. However, despite considerable interest in studies of coral reproduction, there is currently not enough molecular information about the cellular pathways involved with synchronizing spawning/planulation in broadcast spawners and brooders. To determine whether the endogenous clock is implicated in the regulation of reproductive behaviour in corals, we characterized the transcriptome of Acropora digitifera colonies at twelve time points over a 2-month period of full and new moons, starting with the day of spawning in June 2014. We identified 608 transcripts with differential expression only on the spawning night during the coral setting phase and gamete release. Our data revealed an upregulation of light-sensing molecules and rhodopsin-like receptors that initiate signalling cascades, including the glutamate, SMAD signalling and WNT signalling pathways, neuroactive ligand-receptor interactions and calcium signalling. These are all involved in cell cycling, cell movement, tissue polarity, focal adhesion and cytoskeleton reorganization and together lead to gamete release. These findings can improve the understanding of many time-based cycles and extend our knowledge of the interplay between exogenous signals and the endogenous clock in cnidarians.

Theory predicts that passing symbionts directly from parent to offspring should benefit the host by reducing conflict between diverse symbionts and benefit the symbiont by guaranteeing transmission. However, in some symbiotic associations, such as those between corals and algae of the family Symbiodiniaceae, vertical transmission is rare, suggesting a substantial cost. Here, we show that coral larvae which contained symbionts had lower survivorship than larvae of the same species that lacked symbionts when exposed to natural sunlight. Higher activity of antioxidant defenses and higher levels of oxidative cellular damage observed in symbiotic larvae suggest that reactive oxygen species, produced by stress on the photosynthetic apparatus of the symbionts, are responsible for these higher rates of mortality under solar radiation. We hypothesize that symbionts are a burden in the early life history of broadcast spawning corals under conditions typically experienced on the ocean surface during dispersal. This is one possible reason why species with an obligate pre-motile period of between 12 and 36 h very rarely have vertical transmission of symbionts, in contrast to species whose larvae are small or swim on release that often have vertical transmission of symbionts.

Corals harbor symbiotic dinoflagellates, Symbiodinium spp., acquired from surrounding environments. Because Symbiodinium are present at low densities in the water column, corals may attract these symbionts using chemotactic compounds. To examine whether corals contain chemotactic compounds, we established an assay to measure the chemotactic activity for Symbiodinium using an extract of the coral Acropora tenuis, a major reef-building coral in Japan. Our assay revealed that Symbiodinium strain NBRC102920 (clade A), which is taken up by juvenile A. tenuis polyps, is attracted to crude A. tenuis extracts. We found that the chemotactic compounds are water-soluble, heat-labile macromolecules and that the chemotactic activity was inhibited by N-acetyl-d-glucosamine (GlcNAc). We separated the GlcNAc-binding fraction (Fr-ActL) and identified it as the most plausible candidate for the chemoattractant, since the chemotactic activity of the crude A. tenuis extract appeared to be mainly attributable to the activity of Fr-ActL and was also inhibited by the addition of GlcNAc. These results indicate that chemoattraction is mediated via the binding of Symbiodinium to Fr-ActL.

Despite the ecological significance of the relationship between reef-building corals and intracellular photosynthetic dinoflagellates of the genus Symbiodinium, very little is known about the molecular mechanisms involved in its establishment. Indeed, microarray-based analyses point to the conclusion that host gene expression is largely or completely unresponsive during the establishment of symbiosis with a competent strain of Symbiodinium. In this study, the use of Illumina RNA-Seq technology allowed detection of a transient period of differential expression involving a small number of genes (1073 transcripts

The ratios of barium to calcium (Ba/Ca) in reef coral skeletons have been used as a proxy to reconstruct temporal change in barium concentration in surface ocean. To reduce the uncertainty of the coral Ba/Ca proxy, the Ba distribution coefficients between seawater and coral skeletons were determined under different light conditions. Coral planulae (Acropora tenuis) were metamorphosed and settled in dishes with commercial peptide Hym-248 in the laboratory. Juvenile corals were infected with symbiotic algae (Durusdinium sp.) and cultured in 5 Ba concentrations (5, 10, 20, 35, and 150 μmol/mol) for 2 months. Half of the dishes were placed under low light conditions (10–33 μmol m-2 s−1), and another half of the dishes were placed under high light conditions (67–84 μmol m-2 s−1). The Ba/Ca ratios in the coral skeletons were highly correlated with those in ambient seawater under both high and low conditions (R2 > 0.8). The Ba distribution coefficients between seawater with 5–35 μmol/mol of Ba concentration and coral skeletons were 0.72 and 2.83 under high and low light conditions, respectively. These results suggest that biological processes related to light availability could influence to Ba/Cacoral.

Information on biodiversity is essential to evaluate the ecological status of coral reefs. Sounds produced by reef-associated organisms have been used as a biodiversity indicator. However, the interference from abiotic sounds and the lack of a comprehensive audio library have impeded effective evaluation. This study investigated the application of underwater soundscapes as a remote-sensing method to detect biological and anthropogenic activities. Using techniques including the visualization of long-duration recordings, source separation, and clustering, soundscapes were separated into sounds of anthropogenic and biological sources. Our results revealed the dynamics of biological sounds among coral reefs off Sesoko Island, Okinawa, Japan. Biological sounds were much more prominent in shallow-water reefs than in upper-mesophotic reefs, but their spectral features and compositions differed. The shallow-water reefs were dominated by broadband sounds of crustaceans and low-frequency transient fish calls, whereas the upper-mesophotic reefs were characterized by a diverse array of fish choruses and transient sounds. We also discovered that shipping noise heavily interfered with the soundscapes from the upper-mesophotic reefs and represented an invisible threat to life in the low-light habitat. The applied techniques of soundscape information retrieval revealed the distinct ecological status of coral reefs and the behavior change of sound-producing organisms in high temporal resolution. Implementation of soundscape monitoring can generate ecological information on habitat quality, reef biodiversity, human activities, and their interactions. Global collaboration on underwater soundscapes will establish a data-informed platform and help stakeholders assess the resilience of coral reefs to environmental and anthropogenic stressors.

Sex change has been widely studied in animals and plants. However, the conditions favoring sex change, its mode and timing remain poorly known. Here, for the first time in stony corals, we report on a protandrous (youngest individuals are males) repetitive sex change exhibited by the fungiid coral Herpolitha limax across large spatial scales (the coral reefs of Japan, Jordan and Israel) and temporal scales (2004–2017). In contrast to most corals, this species is a daytime spawner (08:00–10:00 AM) that spawned at the same time/same date across all the study sites. The sporadically scattered populations of H. limax among the coral reefs of Eilat (Israel) and Aqaba (Jordan) exhibited significantly slower growth, earlier sex change, and lower percentages of reproduction and sex change in comparison to the densely aggregated populations in Okinawa (Japan). At all sites, sex ratio varied among years, but was almost always biased towards maleness. Growth rate decreased with size. We conclude that comparable to dioecious plants that display labile sexuality in response to energetic and/or environmental constraints, the repetitive sex change displayed by H. limax increases its overall fitness reinforcing the important role of reproductive plasticity in the Phylum Cnidaria in determining their evolutionary success., 論文

Mesophotic coral ecosystems (MCEs) in Japan are currently only reported from the Ryukyu Islands and remain poorly known compared to shallow reefs in the region. MCEs in the Ryukyus were first examined in the 1960s and are among the earliest-studied MCEs globally. MCEs in the region support a high diversity of flora and fauna due to a combination of factors including the warm poleward-flowing Kuroshio Current, the complex geomorphology and diversity of habitats, and the proximity to the Coral Triangle. Recent research into the biology and ecology of mesophotic corals has examined questions such as ecological connectivity between mesophotic and shallow corals and revealed that several coral species span shallow to lower mesophotic depths (>60 m). Observations of reproduction in Seriatopora hystrix and Acropora tenella suggest that the propagule release period of both species is broadly synchronous in shallow and mesophotic corals, although the reproductive season is considerably shorter in mesophotic corals. MCEs in the Ryukyu Islands face stressors similar to shallow coral reefs such as climate change and rapid coastal development. However, the knowledge required to understand the response of MCEs to these threats is sparse. Despite evidence that at least some MCEs appear capable of recovering from disturbances (such as typhoons), investigations on how coastal development affects MCEs and how to mitigate threats to MCEs are urgently needed.