Widespread polyphyly in stony corals (order Scleractinia) has prompted efforts to revise their systematics through approaches that integrate molecular and micromorphological evidence. To date, these approaches have not been comprehensively applied to the dominant genera in mesophotic coral ecosystems (MCEs) because several species in these genera occur primarily at depths that are poorly explored and from which sample collections are limited. This study is the first integrated morphological and molecular systematic analysis of the genera Leptoseris and Pavona to examine material both from shallow-water reefs (<30 m) and from mid- to lower-MCEs (>60 m). Skeletal and tissue samples were collected throughout the Hawaiian Archipelago between 2–127 m. A novel mitochondrial marker (cox1-1-rRNA intron) was sequenced for 70 colonies, and the micromorphologies of 94 skeletons, plus selected type material, were analyzed. The cox1-1-rRNA intron resolved 8 clades, yet Leptoseris and Pavona were polyphyletic. Skeletal micromorphology, especially costal ornamentation, showed strong correspondence and discrete differences between mitochondrial groups. One putative new Leptoseris species was identified and the global depth range of the genus Pavona was extended to 89 m, suggesting that the diversity of mesophotic scleractinians has been underestimated. Examination of species’ depth distributions revealed a pattern of depth zonation: Species common in shallow-water were absent or rare >40 m, whereas others occurred only >60 m. These patterns emphasize the importance of integrated systematic analyses and more comprehensive sampling by depth in assessing the connectivity and diversity of MCEs.
Leptoseris; Pavona; Mesophotic coral ecosystems; Integrated systematics; Molecular phylogenetics; Micromorphology; cox1-1-rRNA intron; Depth zonation; Zooxanthellate corals; Taxonomy
Classical morphological taxonomy places the approximately 1400 recognized species of Scleractinia (hard corals) into 27 families, but many aspects of coral evolution remain unclear despite the application of molecular phylogenetic methods. In part, this may be a consequence of such studies focusing on the reef-building (shallow water and zooxanthellate) Scleractinia, and largely ignoring the large number of deep-sea species. To better understand broad patterns of coral evolution, we generated molecular data for a broad and representative range of deep sea scleractinians collected off New Caledonia and Australia during the last decade, and conducted the most comprehensive molecular phylogenetic analysis to date of the order Scleractinia.
Partial (595 bp) sequences of the mitochondrial cytochrome oxidase subunit 1 (CO1) gene were determined for 65 deep-sea (azooxanthellate) scleractinians and 11 shallow-water species. These new data were aligned with 158 published sequences, generating a 234 taxon dataset representing 25 of the 27 currently recognized scleractinian families.
There was a striking discrepancy between the taxonomic validity of coral families consisting predominantly of deep-sea or shallow-water species. Most families composed predominantly of deep-sea azooxanthellate species were monophyletic in both maximum likelihood and Bayesian analyses but, by contrast (and consistent with previous studies), most families composed predominantly of shallow-water zooxanthellate taxa were polyphyletic, although Acroporidae, Poritidae, Pocilloporidae, and Fungiidae were exceptions to this general pattern. One factor contributing to this inconsistency may be the greater environmental stability of deep-sea environments, effectively removing taxonomic “noise” contributed by phenotypic plasticity. Our phylogenetic analyses imply that the most basal extant scleractinians are azooxanthellate solitary corals from deep-water, their divergence predating that of the robust and complex corals. Deep-sea corals are likely to be critical to understanding anthozoan evolution and the origins of the Scleractinia.
GFP-like fluorescent proteins (FPs) are the key color determinants in reef-building corals (class Anthozoa, order Scleractinia) and are of considerable interest as potential genetically encoded fluorescent labels. Here we report 40 additional members of the GFP family from corals. There are three major paralogous lineages of coral FPs. One of them is retained in all sampled coral families and is responsible for the non-fluorescent purple-blue color, while each of the other two evolved a full complement of typical coral fluorescent colors (cyan, green, and red) and underwent sorting between coral groups. Among the newly cloned proteins are a “chromo-red” color type from Echinopora forskaliana (family Faviidae) and pink chromoprotein from Stylophora pistillata (Pocilloporidae), both evolving independently from the rest of coral chromoproteins. There are several cyan FPs that possess a novel kind of excitation spectrum indicating a neutral chromophore ground state, for which the residue E167 is responsible (numeration according to GFP from A. victoria). The chromoprotein from Acropora millepora is an unusual blue instead of purple, which is due to two mutations: S64C and S183T. We applied a novel probabilistic sampling approach to recreate the common ancestor of all coral FPs as well as the more derived common ancestor of three main fluorescent colors of the Faviina suborder. Both proteins were green such as found elsewhere outside class Anthozoa. Interestingly, a substantial fraction of the all-coral ancestral protein had a chromohore apparently locked in a non-fluorescent neutral state, which may reflect the transitional stage that enabled rapid color diversification early in the history of coral FPs. Our results highlight the extent of convergent or parallel evolution of the color diversity in corals, provide the foundation for experimental studies of evolutionary processes that led to color diversification, and enable a comparative analysis of structural determinants of different colors.
Sexuality and reproductive mode are two fundamental life-history traits that exhibit largely unexplained macroevolutionary patterns among the major groups of multicellular organisms. For example, the cnidarian class Anthozoa (corals and anemones) is mainly comprised of gonochoric (separate sex) brooders or spawners, while one order, Scleractinia (skeleton-forming corals), appears to be mostly hermaphroditic spawners. Here, using the most complete phylogeny of scleractinians, we reconstruct how evolutionary transitions between sexual systems (gonochorism versus hermaphrodism) and reproductive modes (brooding versus spawning) have generated large-scale taxonomic patterns in these characters. Hermaphrodites have independently evolved in three large, distantly related lineages consisting of mostly reef-building species. Reproductive mode in corals has evolved at twice the rate of sexuality, while the evolution of sexuality has been heavily biased: gonochorism is over 100 times more likely to be lost than gained, and can only be acquired by brooders. This circuitous evolutionary pathway accounts for the prevalence of hermaphroditic spawners among reef-forming scleractinians, despite their ancient gonochoric heritage.
coral reef; evolution; life history; phylogeny; reproduction
Cnidaria (corals, sea anemones, hydroids, jellyfish) is a phylum of relatively simple aquatic animals characterized by the presence of the cnidocyst: a cell containing a giant capsular organelle with an eversible tubule (cnida). Species within Cnidaria have life cycles that involve one or both of the two distinct body forms, a typically benthic polyp, which may or may not be colonial, and a typically pelagic mostly solitary medusa. The currently accepted taxonomic scheme subdivides Cnidaria into two main assemblages: Anthozoa (Hexacorallia + Octocorallia) – cnidarians with a reproductive polyp and the absence of a medusa stage – and Medusozoa (Cubozoa, Hydrozoa, Scyphozoa, Staurozoa) – cnidarians that usually possess a reproductive medusa stage. Hypothesized relationships among these taxa greatly impact interpretations of cnidarian character evolution.
We expanded the sampling of cnidarian mitochondrial genomes, particularly from Medusozoa, to reevaluate phylogenetic relationships within Cnidaria. Our phylogenetic analyses based on a mitochogenomic dataset support many prior hypotheses, including monophyly of Hexacorallia, Octocorallia, Medusozoa, Cubozoa, Staurozoa, Hydrozoa, Carybdeida, Chirodropida, and Hydroidolina, but reject the monophyly of Anthozoa, indicating that the Octocorallia + Medusozoa relationship is not the result of sampling bias, as proposed earlier. Further, our analyses contradict Scyphozoa [Discomedusae + Coronatae], Acraspeda [Cubozoa + Scyphozoa], as well as the hypothesis that Staurozoa is the sister group to all the other medusozoans.
Cnidarian mitochondrial genomic data contain phylogenetic signal informative for understanding the evolutionary history of this phylum. Mitogenome-based phylogenies, which reject the monophyly of Anthozoa, provide further evidence for the polyp-first hypothesis. By rejecting the traditional Acraspeda and Scyphozoa hypotheses, these analyses suggest that the shared morphological characters in these groups are plesiomorphies, originated in the branch leading to Medusozoa. The expansion of mitogenomic data along with improvements in phylogenetic inference methods and use of additional nuclear markers will further enhance our understanding of the phylogenetic relationships and character evolution within Cnidaria.
Cnidaria; Medusozoa; Acraspeda; Anthozoa; mito-phylogenomics
Scleractinian corals are currently a focus of major interest because of their ecological importance and the uncertain fate of coral reefs in the face of increasing anthropogenic pressure. Despite this, remarkably little is known about the evolutionary origins of corals. The Scleractinia suddenly appear in the fossil record about 240 Ma, but the range of morphological variation seen in these Middle Triassic fossils is comparable to that of modern scleractinians, implying much earlier origins that have so far remained elusive. A significant weakness in reconstruction(s) of early coral evolution is that deep-sea corals have been poorly represented in molecular phylogenetic analyses.
By adding new data from a large and representative range of deep-water species to existing molecular datasets and applying a relaxed molecular clock, we show that two exclusively deep-sea families, the Gardineriidae and Micrabaciidae, diverged prior to the Complexa/Robusta coral split around 425 Ma, thereby pushing the evolutionary origin of scleractinian corals deep into the Paleozoic.
The early divergence and distinctive morphologies of the extant gardineriid and micrabaciid corals suggest a link with Ordovician "scleractiniamorph" fossils that were previously assumed to represent extinct anthozoan skeletonized lineages. Therefore, scleractinian corals most likely evolved from Paleozoic soft-bodied ancestors. Modern shallow-water Scleractinia, which are dependent on symbionts, appear to have had several independent origins from solitary, non-symbiotic precursors. The Scleractinia have survived periods of massive climate change in the past, suggesting that as a lineage they may be less vulnerable to future changes than often assumed.
The cosmopolitan solitary deep-water scleractinian coral Desmophyllum dianthus (Esper, 1794) was selected as a representative model species of the polyphyletic Caryophylliidae family to (1) examine phylogenetic relationships with respect to the principal Scleractinia taxa, (2) check population structure, (3) test the widespread connectivity hypothesis and (4) assess the utility of different nuclear and mitochondrial markers currently in use. To carry out these goals, DNA sequence data from nuclear (ITS and 28S) and mitochondrial (16S and COI) markers were analyzed for several coral species and for Mediterranean populations of D. dianthus. Three phylogenetic methodologies (ML, MP and BI), based on data from the four molecular markers, all supported D. dianthus as clearly belonging to the “robust” clade, in which the species Lophelia pertusa and D. dianthus not only grouped together, but also shared haplotypes for some DNA markers. Molecular results also showed shared haplotypes among D. dianthus populations distributed in regions separated by several thousands of kilometers and by clear geographic barriers. These results could reflect limited molecular and morphological taxonomic resolution rather than real widespread connectivity. Additional studies are needed in order to find molecular markers and morphological features able to disentangle the complex phylogenetic relationship in the Order Scleractinia and to differentiate isolated populations, thus avoiding the homoplasy found in some morphological characters that are still considered in the literature.
The ecological success of shallow-water reef-building corals (Hexacorallia: Scleractinia) is framed by their intimate endosymbiosis with photosynthetic dinoflagellates in the genus Symbiodinium (zooxanthellae). In contrast, the closely related black corals (Hexacorallia: Anthipatharia) are described as azooxanthellate (lacking Symbiodinium), a trait thought to reflect their preference for low-light environments that do not support photosynthesis. We examined 14 antipatharian species collected between 10 and 396 m from Hawai'i and Johnston Atoll for the presence of Symbiodinium using molecular typing and histology. Symbiodinium internal transcribed spacer-2 (ITS-2) region sequences were retrieved from 43 per cent of the antipatharian samples and 71 per cent of the examined species, and across the entire depth range. The ITS-2 sequences were identical or very similar to those commonly found in shallow-water scleractinian corals throughout the Pacific. Histological analyses revealed low densities of Symbiodinium cells inside antipatharian gastrodermal tissues (0–92 cells mm−3), suggesting that the Symbiodinium are endosymbiotic. These findings confirm that the capacity to engage in endosymbiosis with Symbiodinium is evolutionarily conserved across the cnidarian subclass Hexacorallia, and that antipatharians associate with Symbiodinium types found in shallow-water scleractinians. This study represents the deepest record for Symbiodinium to date, and suggests that some members of this dinoflagellate genus have extremely diverse habitat preferences and broad environmental ranges.
precious coral; endosymbiosis; mesophotic coral reef ecosystems; Antipatharia; internal transcribed spacer-2
Most reef-building corals in the order Scleractinia depend on endosymbiotic algae in the genus Symbiodinium for energy and survival. Significant levels of taxonomic diversity in both partners result in numerous possible combinations of coral-Symbiodinium associations with unique functional characteristics. We created and analyzed the first coral-Symbiodinium networks utilizing a global dataset of interaction records from coral reefs in the tropical Indo-Pacific and Atlantic Oceans for 1991 to 2010. Our meta-analysis reveals that the majority of coral species and Symbiodinium types are specialists, but failed to detect any one-to-one obligate relationships. Symbiont specificity is correlated with a host’s transmission mode, with horizontally transmitting corals being more likely to interact with generalist symbionts. Globally, Symbiodinium types tend to interact with only vertically or horizontally transmitting corals, and only a few generalist types are found with both. Our results demonstrate a strong correlation between symbiont specificity, symbiont transmission mode, and community partitioning. The structure and dynamics of these network interactions underlie the fundamental biological partnership that determines the condition and resilience of coral reef ecosystems.
Regulatory genes control the expression of other genes and are key components of developmental processes such as segmentation and embryonic construction of the skull in vertebrates. Here we examine the variability and evolution of three vertebrate regulatory genes, addressing issues of their utility for phylogenetics and comparing the rates of genetic change seen in regulatory loci to the rates seen in other genes in the parrotfishes. The parrotfishes are a diverse group of colorful fishes from coral reefs and seagrasses worldwide and have been placed phylogenetically within the family Labridae. We tested phylogenetic hypotheses among the parrotfishes, with a focus on the genera Chlorurus and Scarus, by analyzing eight gene fragments for 42 parrotfishes and eight outgroup species. We sequenced mitochondrial 12s rRNA (967 bp), 16s rRNA (577 bp), and cytochrome b (477 bp). From the nuclear genome, we sequenced part of the protein-coding genes rag2 (715 bp), tmo4c4 (485 bp), and the developmental regulatory genes otx1 (672 bp), bmp4 (488 bp), and dlx2 (522 bp). Bayesian, likelihood, and parsimony analyses on the resulting 4903 bp of DNA sequence produced similar topologies that confirm the monophyly of the scarines and provide a phylogeny at the species level for portions of the genera Scarus and Chlorurus. Four major clades of Scarus were recovered, with three distributed in the Indo-Pacific and one containing Caribbean/Atlantic taxa. Molecular rates suggest a Miocene origin of the parrotfishes (22 mya) and a recent divergence of species within Scarus and Chlorurus, within the past 5 million years. Developmentally important genes made a significant contribution to phylogenetic structure, and rates of genetic evolution were high in bmp4, similar to other coding nuclear genes, but low in otx1 and the dlx2 exons. Synonymous and nonsynonymous substitution patterns in developmental regulatory genes support the hypothesis of stabilizing selection during the history of these genes, with several phylogenetic regions of accelerated nonsynonymous change detected in the phylogeny.
phylogenetics; coral reef fishes; parrotfishes; regulatory genes; molecular clock; bmp4; dlx2; otx1
The pseudocolonial coral Lophelia pertusa (Scleractinia, Caryophylliidae) is a eurybathic, stenothermal cosmopolitan cold-water species. It occurs in two color varieties, white and red. L. pertusa builds vast cold-water coral reefs along the continental margins, which are among the most diverse deep-sea habitats. Microbiology of L. pertusa has been in scientific focus for only a few years, but the question of whether the coral holds a host-specific bacterial community has not been finally answered. Bacteria on coral samples from the Trondheimsfjord (Norway) were characterized by the culture-independent 16S rRNA gene-based techniques terminal restriction fragment length polymorphism and sequence analysis. L. pertusa revealed a high microbial richness. Clone sequences were dominated by members of the Alpha- and Gammaproteobacteria. Other abundant taxa were Bacteroidetes, Actinobacteria, Verrucomicrobia, Firmicutes, and Planctomycetes. The bacterial community of L. pertusa not only differed conspicuously from that of the environment but also varied with both the location and color variety of its host. Therefore, the microbial colonization cannot be termed “specific” sensu stricto. However, similarities to other coral-bacterium associations suggest the existence of “cold-water coral-specific” bacterial groups sensu lato. L. pertusa-associated bacteria appear to play a significant role in the nutrition of their host by degradation of sulfur compounds, cellulose, chitin, and end products of the coral's anaerobic metabolism. Some coral-associated microbes were regarded as opportunistic pathogens. Dominance of mixotrophic members of the Rhodobacteraceae in white L. pertusa could explain the wider dispersal of this phenotype by supplementary nutrition.
The phylum Cnidaria is an ancient group of venomous animals, specialized in the production and delivery of toxins. Many species belonging to the class Anthozoa have been studied and their venoms often contain a group of peptides, less than 10 kDa, that act upon ion channels. These peptides and their targets interact with high affinity producing neurotoxic and cardiotoxic effects, and even death, depending on the dose and the administration pathway. Zoanthiniaria is an order of the Subclass Hexacorallia, class Anthozoa, and unlike sea anemone (order Actiniaria), neither its diversity of toxins nor the in vivo effects of the venoms has been exhaustively explored. In this study we assessed some toxicological tests on mice with a low molecular weight fraction obtained by gel filtration in Sephadex G-50 from Zoanthus sociatus crude extract. The gel filtration chromatogram at 280 nm revealed two major peaks, the highest absorbance corresponding to the low molecular weight fraction. The toxicological effects seem to be mostly autonomic and cardiotoxic, causing death in a dose dependent manner with a LD50 of 792 μg/kg. Moreover, at a dose of 600 μg/kg the active fraction accelerated the KCl-induced lethality in mice.
biological activity; toxins; Zoanthus sociatus; Anthozoa; Cnidaria; LD50 mice
A substantial proportion of the world's living species, including one-third of the reef-building corals, are threatened with extinction and in pressing need of conservation action. In order to reduce biodiversity loss, it is important to consider species' contribution to evolutionary diversity along with their risk of extinction for the purpose of setting conservation priorities. Here I reconstruct the most comprehensive tree of life for the order Scleractinia (1,293 species) that includes all 837 living reef species, and employ a composite measure of phylogenetic distinctiveness and extinction risk to identify the most endangered lineages that would not be given top priority on the basis of risk alone. The preservation of these lineages, not just the threatened species, is vital for safeguarding evolutionary diversity. Tests for phylogeny-associated patterns show that corals facing elevated extinction risk are not clustered on the tree, but species that are susceptible, resistant or resilient to impacts such as bleaching and disease tend to be close relatives. Intensification of these threats or extirpation of the endangered lineages could therefore result in disproportionate pruning of the coral tree of life.
The Cnidaria phylum includes organisms that are among the most venomous animals. The Anthozoa class includes sea anemones, hard corals, soft corals and sea pens. The composition of cnidarian venoms is not known in detail, but they appear to contain a variety of compounds. Currently around 250 of those compounds have been identified (peptides, proteins, enzymes and proteinase inhibitors) and non-proteinaceous substances (purines, quaternary ammonium compounds, biogenic amines and betaines), but very few genes encoding toxins were described and only a few related protein three-dimensional structures are available. Toxins are used for prey acquisition, but also to deter potential predators (with neurotoxicity and cardiotoxicity effects) and even to fight territorial disputes. Cnidaria toxins have been identified on the nematocysts located on the tentacles, acrorhagi and acontia, and in the mucous coat that covers the animal body. Sea anemone toxins comprise mainly proteins and peptides that are cytolytic or neurotoxic with its potency varying with the structure and site of action and are efficient in targeting different animals, such as insects, crustaceans and vertebrates. Sea anemones toxins include voltage-gated Na+ and K+ channels toxins, acid-sensing ion channel toxins, Cytolysins, toxins with Kunitz-type protease inhibitors activity and toxins with Phospholipase A2 activity. In this review we assessed the phylogentic relationships of sea anemone toxins, characterized such toxins, the genes encoding them and the toxins three-dimensional structures, further providing a state-of-the-art description of the procedures involved in the isolation and purification of bioactive toxins.
Cnidaria; sea anemone; phylogeny; toxin; toxin gene
A novel symbiosis between scleractinians and hydroids (Zanclea spp.) was recently discovered using taxonomic approaches for hydroid species identification. In this study, we address the question whether this is a species-specific symbiosis or a cosmopolitan association between Zanclea and its coral hosts. Three molecular markers, including mitochondrial 16S and nuclear 28S ribosomal genes, and internal transcribed spacer (ITS), were utilized to examine the existence of Zanclea species from 14 Acropora species and 4 other Acroporidae genera including 142 coral samples collected from reefs in Kenting and the Penghu Islands, Taiwan, Togian Island, Indonesia, and Osprey Reef and Orpheus Island on the Great Barrier Reef, Australia. Molecular phylogenetic analyses of the 16S and 28S genes showed that Acropora-associated Zanclea was monophyletic, but the genus Zanclea was not. Analysis of the ITS, and 16S and 28S genes showed either identical or extremely low genetic diversity (with mean pairwise distances of 0.009 and 0.006 base substitutions per site for the 16S and 28S genes, respectively) among Zanclea spp. collected from diverse Acropora hosts in different geographic locations, suggesting that a cosmopolitan and probably genus-specific association occurs between Zanclea hydroids and their coral hosts.
Host-associated adaptation is emerging as a potential driver of population differentiation and speciation for marine organisms with major implications for ecosystem structure and function. Coralliophila abbreviata are corallivorous gastropods that live and feed on most of the reef-building corals in the tropical western Atlantic and Caribbean. Populations of C. abbreviata associated with the threatened acroporid corals, Acropora palmata and A. cervicornis, display different behavioral, morphological, demographic, and life-history characteristics than those that inhabit other coral host taxa, indicating that host-specific selective forces may be acting on C. abbreviata. Here, we used newly developed polymorphic microsatellite loci and mitochondrial cytochrome b sequence data to assess the population genetic structure, connectivity, and demographic history of C. abbreviata populations from three coral host taxa (A. palmata, Montastraea spp., Mycetophyllia spp.) and six geographic locations across the Caribbean. Analysis of molecular variance provided some evidence of weak and possibly geographically variable host-associated differentiation but no evidence of differentiation among sampling locations or major oceanographic regions, suggesting high gene flow across the Caribbean. Phylogenetic network and Bayesian clustering analyses supported a hypothesis of a single panmictic population as individuals failed to cluster by host or sampling location. Demographic analyses consistently supported a scenario of population expansion during the Pleistocene, a time of major carbonate reef development in the region. Although further study is needed to fully elucidate the interactive effects of host-associated selection and high gene flow in this system, our results have implications for local and regional community interactions and impact of predation on declining coral populations.
Coral-grounds are reef communities that colonize rocky substratum but do not form framework or three-dimensional reef structures. To investigate why, we used video transects and underwater photography to determine the composition, structure and status of a coral-ground community located on the edge of a rocky terrace in front of a tourist park, Xcaret, in the northern Mesoamerican Reef tract, Mexico. The community has a relatively low coral, gorgonian and sponge cover (<10%) and high algal cover (>40%). We recorded 23 species of Scleractinia, 14 species of Gorgonacea and 30 species of Porifera. The coral community is diverse but lacks large coral colonies, being dominated instead by small, sediment-tolerant, and brooding species. In these small colonies, the abundance of potentially lethal interactions and partial mortality is high but decreases when colonies are larger than 40 cm. Such characteristics are consistent with an environment control whereby storm waves periodically remove larger colonies and elevate sediment flux. The community only survives these storm conditions due to its slope-break location, which ensures lack of burial and continued local recruitment. A comparison with similar coral-ground communities in adjacent areas suggests that the narrow width of the rock terrace hinders sediment stabilization, thereby ensuring that communities cannot escape bottom effects and develop into three-dimensional reef structures on geological time scales.
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.
The coral species Leptoseris troglodyta
sp. n. (Scleractinia, Agariciidae) is described as new to science. It is the first known azooxanthellate shallow-water agariciid and is recorded from the ceilings of caves at 5-35 m depth in West Pacific coral reefs. The corals have monocentric cup-shaped calices. They may become colonial through extramural budding from the basal coenosteum, which may cause adjacent calices to fuse. The size, shape and habitat of Leptoseris troglodyta are unique compared to other Leptoseris species, many of which have been recorded from mesophotic depths. The absence of zooxanthellae indicates that it may survive well in darkness, but endolithic algae in some corals indicate that they may be able to get some light. The presence of menianes on the septal sides, which may help to absorb light at greater depths in zooxanthellate corals, have no obvious adaptive relevance in the new species and could have been inherited from ancestral species that perhaps were zooxanthellate. The new species may be azooxanthellate as derived through the loss of zooxanthellae, which would be a reversal in Leptoseris phylogeny.
Cavernicolous; colonial; dwarfism; extramural budding; monocentric; skiophilous; solitary; troglobiotic
Microbial associations with corals are common and are most likely symbiotic, although their diversity and relationships with environmental factors and host species remain unclear. In this study, we adopted a 16S rRNA gene tag-pyrosequencing technique to investigate the bacterial communities associated with three stony Scleractinea and two soft Octocorallia corals from three locations in the Red Sea. Our results revealed highly diverse bacterial communities in the Red Sea corals, with more than 600 ribotypes detected and up to 1,000 species estimated from a single coral species. Altogether, 21 bacterial phyla were recovered from the corals, of which Gammaproteobacteria was the most dominant group, and Chloroflexi, Chlamydiae, and the candidate phylum WS3 were reported in corals for the first time. The associated bacterial communities varied greatly with location, where environmental conditions differed significantly. Corals from disturbed areas appeared to share more similar bacterial communities, but larger variations in community structures were observed between different coral species from pristine waters. Ordination methods identified salinity and depth as the most influential parameters affecting the abundance of Vibrio, Pseudoalteromonas, Serratia, Stenotrophomonas, Pseudomonas, and Achromobacter in the corals. On the other hand, bacteria such as Chloracidobacterium and Endozoicomonas were more sensitive to the coral species, suggesting that the host species type may be influential in the associated bacterial community, as well. The combined influences of the coral host and environmental factors on the associated microbial communities are discussed. This study represents the first comparative study using tag-pyrosequencing technology to investigate the bacterial communities in Red Sea corals.
Metabolic interactions with endosymbiotic photosynthetic dinoflagellate Symbiodinium spp. are fundamental to reef-building corals (Scleractinia) thriving in nutrient-poor tropical seas. Yet, detailed understanding at the single-cell level of nutrient assimilation, translocation, and utilization within this fundamental symbiosis is lacking. Using pulse-chase 15N labeling and quantitative ion microprobe isotopic imaging (NanoSIMS; nanoscale secondary-ion mass spectrometry), we visualized these dynamic processes in tissues of the symbiotic coral Pocillopora damicornis at the subcellular level. Assimilation of ammonium, nitrate, and aspartic acid resulted in rapid incorporation of nitrogen into uric acid crystals (after ~45 min), forming temporary N storage sites within the dinoflagellate endosymbionts. Subsequent intracellular remobilization of this metabolite was accompanied by translocation of nitrogenous compounds to the coral host, starting at ~6 h. Within the coral tissue, nitrogen is utilized in specific cellular compartments in all four epithelia, including mucus chambers, Golgi bodies, and vesicles in calicoblastic cells. Our study shows how nitrogen-limited symbiotic corals take advantage of sudden changes in nitrogen availability; this opens new perspectives for functional studies of nutrient storage and remobilization in microbial symbioses in changing reef environments.
The methodology applied, combining transmission electron microscopy with nanoscale secondary-ion mass spectrometry (NanoSIMS) imaging of coral tissue labeled with stable isotope tracers, allows quantification and submicrometric localization of metabolic fluxes in an intact symbiosis. This study opens the way for investigations of physiological adaptations of symbiotic systems to nutrient availability and for increasing knowledge of global nitrogen and carbon biogeochemical cycling.
In the Mexican Caribbean, the exotic lionfish Pterois volitans has become a species of great concern because of their predatory habits and rapid expansion onto the Mesoamerican coral reef, the second largest continuous reef system in the world. This is the first report of DNA identification of stomach contents of lionfish using the barcode of life reference database (BOLD).
We confirm with barcoding that only Pterois volitans is apparently present in the Mexican Caribbean. We analyzed the stomach contents of 157 specimens of P. volitans from various locations in the region. Based on DNA matches in the Barcode of Life Database (BOLD) and GenBank, we identified fishes from five orders, 14 families, 22 genera and 34 species in the stomach contents. The families with the most species represented were Gobiidae and Apogonidae. Some prey taxa are commercially important species. Seven species were new records for the Mexican Caribbean: Apogon mosavi, Coryphopterus venezuelae, C. thrix, C. tortugae, Lythrypnus minimus, Starksia langi and S. ocellata. DNA matches, as well as the presence of intact lionfish in the stomach contents, indicate some degree of cannibalism, a behavior confirmed in this species by the first time. We obtained 45 distinct crustacean prey sequences, from which only 20 taxa could be identified from the BOLD and GenBank databases. The matches were primarily to Decapoda but only a single taxon could be identified to the species level, Euphausia americana.
This technique proved to be an efficient and useful method, especially since prey species could be identified from partially-digested remains. The primary limitation is the lack of comprehensive coverage of potential prey species in the region in the BOLD and GenBank databases, especially among invertebrates.
Corals are notoriously difficult to identify at the species-level due to few diagnostic characters and variable skeletal morphology. This 'coral species problem' is an impediment to understanding the evolution and biodiversity of this important and threatened group of organisms. We examined the evolution of the nuclear ribosomal internal transcribed spacer (ITS) and mitochondrial markers (COI, putative control region) in Porites, one of the most taxonomically challenging and ecologically important genera of reef-building corals.
Nuclear and mitochondrial markers were congruent, clearly resolving many traditionally recognized species; however, branching and mounding varieties were genetically indistinguishable within at least two clades, and specimens matching the description of 'Porites lutea' sorted into three genetically divergent groups. Corallite-level features were generally concordant with genetic groups, although hyper-variability in one group (Clade I) overlapped and obscured several others, and Synarea (previously thought to be a separate subgenus) was closely related to congeners despite its unique morphology. Scanning electron microscopy revealed subtle differences between genetic groups that may have been overlooked previously as taxonomic characters.
This study demonstrates that the coral skeleton can be remarkably evolutionarily plastic, which may explain some taxonomic difficulties, and obscure underlying patterns of endemism and diversity.
Anemonefishes (genera: Amphiprion and Premnas; family Pomacentridae) are a group of 28 species of coral reef fishes that are found in obligate symbiosis with large tropical sea anemones. A phylogenetic hypothesis based on morphological analyses of this group suggests that the ancestral anemonefish was a generalist with similar morphology to other pomacentrids, and that it gave rise to other anemonefish species that were more specialized for living with particular species of host anemones. To test this hypothesis we constructed a molecular phylogeny for the anemonefishes by sequencing 1140 base pairs of the cytochrome b gene and 522 base pairs of the 16S rRNA gene for six species of anemonefishes (representatives of all subgenera and species complexes) and two other pomacentrid species. Three methods of phylogenetic analysis all strongly supported the conclusion that anemonefishes are a monophyletic group. The molecular phylogeny differs from the tree based on morphological data in that the two species of specialized anemonefishes (Premnas biaculeatus and Amphiprion ocellaris) were assigned to a basal position within the clade, and the extreme host generalist (Amphiprion clarkii) to a more derived position. Thus, the initial anemonefish ancestors were probably host specialists and subsequent speciation events led to a combination of generalist and specialist groups. Further phylogenetic studies of additional anemonefish species are required to substantiate this hypothesis.
Free-swimming larvae of tropical corals go through a critical life-phase when they return from the open ocean to select a suitable settlement substrate. During the planktonic phase of their life cycle, the behaviours of small coral larvae (<1 mm) that influence settlement success are difficult to observe in situ and are therefore largely unknown. Here, we show that coral larvae respond to acoustic cues that may facilitate detection of habitat from large distances and from upcurrent of preferred settlement locations. Using in situ choice chambers, we found that settling coral larvae were attracted to reef sounds, produced mainly by fish and crustaceans, which we broadcast underwater using loudspeakers. Our discovery that coral larvae can detect and respond to sound is the first description of an auditory response in the invertebrate phylum Cnidaria, which includes jellyfish, anemones, and hydroids as well as corals. If, like settlement-stage reef fish and crustaceans, coral larvae use reef noise as a cue for orientation, the alleviation of noise pollution in the marine environment may gain further urgency.