<Emphasis Type="Italic">Megaviridae</Emphasis>-like particles associated with <Emphasis Type="Italic">Symbiodinium</Emphasis> spp. from the endemic coral <Emphasis Type="Italic">Mussismilia braziliensis</Emphasis>

Coral reefs are one of the most dynamic and productive marine ecosystems. The coral holobiont consists of the coral animal and a variety of associated microorganisms that include symbiotic dinoflagellates of the genus Symbiodinium, bacteria, archaea, fungi and viruses. The interactions among these components are crucial for coral health and, consequently, to the coral reef resilience to disturbance. Environmental stressors such as elevated temperature, high irradiance and ultraviolet (UV) radiation can lead to the breakdown of the coral-Symbiodinium symbiosis in a phenomenon known as “coral bleaching”. The present study provides evidence for virus-like particles (VLPs) induced in UV-irradiated Symbiodinium spp. cultures (clades A and C) that were isolated from the coral Mussismilia braziliensis, suggesting a latent viral infection in these strains. Scanning and transmission electron microscopy images of the UV stressed cultures revealed the presence of giant (ca. 450 nm) and small (ca. 40 nm) VLPs. Morphological features link the giant VLPs to the family Megaviridae. Symbiodinium spp. Megaviridae giant viruses and other associated viruses may represent dynamic forces driving and influencing health of the coral holobiont.     

Microhabitat characteristics of <Emphasis Type="Italic">Stegastes planifrons</Emphasis> and <Emphasis Type="Italic">S. adustus</Emphasis> territories

Stegastes adustus and Stegastes planifrons are two species of damselfishes commonly found in the Caribbean. These territorial fishes have been widely studied due to their major ecological role on coral reef in controlling the growth of macroalgae that compete with corals for space and, inversely, on their deleterious role in destroying coral tissues to impulse the development of algae. However, few studies were conducted on the biotic and abiotic components of their territories. In the present study, territory size and surfaces of benthic components (macroalgae, algal turf, massive corals, branching corals, Milleporidae, sponges, sand and rubbles) were estimated for the two species at two contrasted sites. At Ilet Pigeon site (IP), the two damselfishes were found at different depth and exhibited different territory sizes. S. adustus defended a larger territory characterized by massive corals, sand and Milleporidae, while S. planifrons territories were smaller, deeper and characterized by branching corals, sponges and rubble. At Passe-à-Colas site (PC), the two fish species coexisted in the same depth range and defended territories of similar size. Their territories presented higher proportions of macroalgae, but smaller surfaces of Milleporidae than at IP. At PC, the main difference between the two species was a higher surface of massive corals inside S. planifrons territories than S. adustus territories. Differences in microhabitat characteristics between the two Stegastes seemed mostly site related. This resulted from the high plasticity of two species, allowing them to persist on Caribbean coral reefs after the decline of most branching acroporids, their former favorite habitats.     

Temporal dynamics of black band disease affecting pillar coral (<Emphasis Type="Italic">Dendrogyra cylindrus</Emphasis>) following two consecutive hyperthermal events on the Florida Reef Tract

Black band disease (BBD) affects many coral species worldwide and is considered a major contributor to the decline of reef-building coral. On the Florida Reef Tract BBD is most prevalent during summer and early fall when water temperatures exceed 29 °C. BBD is rarely reported in pillar coral (Dendrogyra cylindrus) throughout the Caribbean, and here we document for the first time the appearance of the disease in this species on Florida reefs. The highest monthly BBD prevalence in the D. cylindrus population were 4.7% in 2014 and 6.8% in 2015. In each year, BBD appeared immediately following a hyperthermal bleaching event, which raises concern as hyperthermal seawater anomalies become more frequent.     

Variability in chemical defense across a shallow to mesophotic depth gradient in the Caribbean sponge <Emphasis Type="Italic">Plakortis angulospiculatus</Emphasis>

The transition between shallow and mesophotic coral reef communities in the tropics is characterized by a significant gradient in abiotic and biotic conditions that could result in potential trade-offs in energy allocation. The mesophotic reefs in the Bahamas and the Cayman Islands have a rich sponge fauna with significantly greater percent cover of sponges than in their respective shallow reef communities, but relatively low numbers of spongivores. Plakortis angulospiculatus, a common sponge species that spans the depth gradient from shallow to mesophotic reefs in the Caribbean, regenerates faster following predation and invests more energy in protein synthesis at mesophotic depths compared to shallow reef conspecifics. However, since P. angulospiculatus from mesophotic reefs typically contain lower concentrations of chemical feeding deterrents, they are not able to defend new tissue from predation as efficiently as conspecifics from shallow reefs. Nonetheless, following exposure to predators on shallow reefs, transplanted P. angulospiculatus from mesophotic depths developed chemical deterrence to predatory fishes. A survey of bioactive extracts indicated that a specific defensive metabolite, plakortide F, varied in concentration with depth, producing altered deterrence between shallow and mesophotic reef P. angulospiculatus. Different selective pressures in shallow and mesophotic habitats have resulted in phenotypic plasticity within this sponge species that is manifested in variable chemical defense and tissue regeneration at wound sites.     

<Emphasis Type="Italic">Euphyllia paradivisa</Emphasis>, a successful mesophotic coral in the northern Gulf of Eilat/Aqaba,Red Sea

Mesophotic coral ecosystems (MCEs) host a thriving community of biota that has remained virtually unexplored. Here we report for the first time on a large population of the endangered coral species Euphyllia paradivisa from the MCEs of the Gulf of Eilat/Aqaba (GOE/A), Red Sea. The mesophotic zone in some parts of the study site harbors a specialized coral community predominantly comprising E. paradivisa (73 % of the total coral cover), distributed from 36 to 72 m depth. Here we sought to elucidate the strict distribution but high abundance of E. paradivisa in the MCEs at the GOE/A. We present 4 yr of observations and experiments that provide insight into the physiological plasticity of E. paradivisa: its low mortality rates at high light intensities, high competitive abilities, successful symbiont adaptation to the shallow-water environment, and tolerance to bleaching conditions or survival during prolonged bleaching. Despite its ability to survive under high irradiance in shallow water, E. paradivisa is not found in the shallow reef of the GOE/A. We suggest several factors that may explain the high abundance and exclusivity of E. paradivisa in the MCE: its heterotrophic capabilities; its high competition abilities; the possibility of it finding a deep-reef refuge there from fish predation; and its concomitant adaptation to this environment.     

Molecular evidence of symbiotic activity between <Emphasis Type="Italic">Symbiodinium</Emphasis> and <Emphasis Type="Italic">Tridacna maxima</Emphasis> larvae

Dinoflagellates in the genus Symbiodinium (zooxanthellae) provide the photosynthesis that sustains the majority of primary production in coral reefs. They occur symbiotically with several phyla, including mollusks such as giant clams (Tridacna spp.). This mutualistic association is obligatory for the giant clams, but the exact point in which this symbiosis is established and the main translocated photosynthate are unknown. In this study, we tracked the expression of specific genes for symbiosis and glycerol synthesis during a time course experiment. Giant clam larvae were raised until 75 h post-fertilization and then infected with cultured isolates of Symbiodinium clade A3. Expression of symbiosis-specific and housekeeping genes was monitored at four time points. The expression of H⁺-ATPase, a symbiosis-specific gene in Symbiodinium, was observed at 24 h after symbiont acquisition by the clam larvae. The expression of an enzyme responsible for glycerol synthesis was also observed. Together, these results show that the symbiotic relationship was already in place 24 h after Symbiodinium acquisition, during veliger larval stage. This is the first report using a molecular symbiosis-specific marker that supports symbiotic activity between Symbiodinium and a metazoan larva of an organism that acquires symbionts horizontally. From the expression of the glycerol-synthesizing gene, it was qualitatively determined that Symbiodinium cells may produce glycerol regardless of whether they are free-living or in symbiosis.     

Modeled connectivity of <Emphasis Type="Italic">Acropora millepora</Emphasis> populations from reefs of the Spratly Islands and the greater South China Sea

The Spratly Island archipelago is a remote network of coral reefs and islands in the South China Sea that is a likely source of coral larvae to the greater region, but about which little is known. Using a particle-tracking model driven by oceanographic data from the Coral Triangle region, we simulated both spring and fall spawning events of Acropora millepora, a common coral species, over a 46-yr period (1960–2005). Simulated population biology of A. millepora included the acquisition and loss of competency, settlement over appropriate benthic habitat, and mortality based on experimental data. The simulations aimed to provide insights into the connectivity of reefs within the Spratly Islands, the settlement of larvae on reefs of the greater South China Sea, and the potential dispersal range of reef organisms from the Spratly Islands. Results suggest that (1) the Spratly Islands may be a significant source of A. millepora larvae for the Palawan reefs (Philippines) and some of the most isolated reefs of the South China Sea; and (2) the relatively isolated western Spratly Islands have limited source reefs supplying them with larvae and fewer of their larvae successfully settling on other reefs. Examination of particle dispersal without biology (settlement and mortality) suggests that larval connectivity is possible throughout the South China Sea and into the Coral Triangle region. Strong differences in the spring versus fall larval connectivity and dispersal highlight the need for a greater understanding of spawning dynamics of the region. This study confirms that the Spratly Islands are likely an important source of larvae for the South China Sea and Coral Triangle region.     

The functional importance of <Emphasis Type="Italic">Acropora austera</Emphasis> as nursery areas for juvenile reef fish on South African coral reefs

Many coral reef fish species use mangrove and seagrass beds as nursery areas. However, in certain regions, the absence or scarcity of such habitats suggests that juvenile coral reef fish may be seeking refuge elsewhere. The underlying biogenic substratum of most coral reefs is structurally complex and provides many types of refuge. However, on young or subtropical coral reefs, species may be more reliant on the living coral layer as nursery areas. Such is the case on the high-latitude coral reefs of South Africa where the coral communities consist of a thin veneer of coral overlaying late Pleistocene bedrock. Thus, the morphology of coral species may be a major determinant in the availability of refuge space. Acropora austera is a branching species that forms large patches with high structural complexity. Associated with these patches is a diverse community of fish species, particularly juveniles. Over the past decade, several large (>100 m²) A. austera patches at Sodwana Bay have been diminishing for unknown reasons and there is little evidence of their replacement or regrowth. Seven patches of A. austera (AP) and non-A. austera (NAP) were selected and monitored for 12 months using visual surveys to investigate the importance of AP as refugia and nursery areas. There were significant differences in fish communities between AP and NAP habitats. In total, 110 species were recorded within the patches compared to 101 species outside the patches. Labrids and pomacentrids were the dominant species in the AP habitats, while juvenile scarids, acanthurids, chaetodons and serranids were also abundant. The diversity and abundance of fish species increased significantly with AP size. As the most structurally complex coral species on the reefs, the loss of APs may have significant implications for the recruitment and survival of certain fish species.     

Habitat preferences of the <Emphasis Type="Italic">Pteroclava krempfi</Emphasis>-alcyonaceans symbiosis: inner vs outer coral reefs

Herein, we provide observation on the ecological relationships between the hydrozoan species Pteroclava krempfi and three alcyonacean genera: Lobophytum, Sarcophyton and Sinularia from protected and exposed reef habitats in the Maldives. The associations were found to be widespread in the investigated area with both an overall and taxon-specific symbiosis prevalence higher in the exposed reef sites. Pteroclava krempfi most frequently occurred with Lobophytum, followed by Sinularia and Sarcophyton. The prevalence of P. krempfi with soft corals was also positively correlated to percent host cover, which was higher in the outer reef sites, suggesting a host-reliant relationship for the hydrozoan. However, the nature of these relationships, as as well as the factors that drive their establishment, requires further investigation. The widespread degradation of coral reef ecosystems endangers the existence of many poorly understood, but intimate relationships that often go unrecognized.     

Assemblage-level effects of the introduced peacock hind (<Emphasis Type="Italic">Cephalopholis argus</Emphasis>) on Hawaiian reef fishes

The peacock hind Cephalopholis argus (family Serranidae), locally known as ‘roi’, was introduced from French Polynesia to Hawaii in the mid-twentieth century as a food fish. However, because of its association with ciguatera fish poisoning, it is rarely fished for food. Previous research indicates that roi could have a negative impact on native reef fish assemblages because of their high densities and prey consumption rates. However, it is unclear whether roi add to the cumulative mortality of prey (predation hypothesis), or whether predation is instead compensatory (doomed surplus hypothesis). This study experimentally assessed the effects of roi on reef fish populations through a long-term (5.5 year) predator removal experiment. A Before-After-Control-Impact study design was used to assess changes in fish assemblages following the removal of roi on 1.3 ha of patch reef. Increases in the density of prey-sized fish (<15 cm TL) were observed 18 months after roi removal. However, those effects did not translate into sustained increases in prey. While increases in potential competitors, wrasses (family Labridae), particularly the piscivorous ringtail wrasse Oxycheilinus unifasciatus, were observed on roi-free reefs, the fish assemblage did not diverge substantially in composition. Native reef fish appeared to resist the potential negative impacts of predation by roi, possibly through a refuge in size for some fish families. Management to protect intact fish assemblage size-structure could serve to bolster native resistance to invading species. In considering the threats facing coral reefs, and the possible solutions, roi removal alone will not likely replenish native fishery resources.     

The potential of azooxanthellate poriferan hosts to assess the fundamental and realized <Emphasis Type="Italic">Symbiodinium</Emphasis> niche: evaluating a novel method to initiate <Emphasis Type="Italic">Symbiodinium</Emphasis> associations

On coral reefs, Symbiodinium spp. are found in most cnidarian species, but reside in only a small number of sponge species. Of the sponges that do harbor Symbiodinium, most are found in the family Clionaidae, which represents a minor fraction of the poriferan diversity on a reef. Our goal was to determine whether Symbiodinium can be taken up by sponge hosts that do not typically harbor these algal symbionts, and then to follow the fate of any Symbiodinium that enter the intracellular space. We used the filter-feeding capacity of sponges to initiate intracellular interactions between sponge-specialist clade G Symbiodinium and six sponge species that do not associate with Symbiodinium. Using a pulse-chase experimental design, we determined that all of the species we examined captured Symbiodinium, and undamaged intracellular algae were found up to 1 h after inoculation. In a longer-term experiment, Symbiodinium populations in Amphimedon erina persisted in sponge cells for at least 5 d post-inoculation. While no evidence of digestion was detected, the population decreased exponentially after inoculation. We contrast these data with the characteristics of symbiont acquisition and establishment in Cliona varians, which normally harbors Symbiodinium. Explants from experimentally derived aposymbiotic sponges were placed in the field where they acquired Symbiodinium from ambient sources (i.e., we did not inoculate them as in the pulse-chase experiments). We began to detect Symbiodinium cells in C. varians after 12 d, and the algal population increased exponentially until densities approached those typically found in this host (after ~128 d). We discuss the implications of this work in light of growing interest in the evolution of specificity between hosts and symbionts, and the fundamental and realized niche of Symbiodinium.     

Association analysis of the glutelin synthesis genes <Emphasis Type="Italic">GluA</Emphasis> and <Emphasis Type="Italic">GluB1</Emphasis> in a <Emphasis Type="Italic">Japonica</Emphasis> rice collection

Glutelin is the most significant seed storage protein and is regarded as an important nutrient quality trait in rice. Research on the genetic basis of the glutelin content distinction in rice will provide more choices for the diets of people with kidney disease and diabetes. The GluA and GluB1 genes play important roles in the process of glutelin synthesis. In this study, 128 Japonica rice accessions with wide geographic distributions were collected to construct the association panel. Among all the 128 accessions, both sequences of the GluA and GluB1 genes were obtained, and nucleotide polymorphisms were detected. A total of 46 SNPs and eight InDels, six SNPs and four InDels were found in the GluA and GluB1 gene sequences, respectively. Eight haplotypes and two haplotypes were classified based on the SNPs in the coding region of the GluA and GluB1 genes, respectively. Moreover, the association of the polymorphic sites in the two genes with glutelin content in the tested population was estimated. The results revealed that five SNPs in the GluA gene, one SNP and one InDel in the GluB1 gene were associated with glutelin content at a significant level (P < 0.01). Corresponding markers were also designed to check the alleles of GluA and GluB1 genes. These results suggested that polymorphisms in the GluA and GluB1 genes in rice could be utilized in molecular marker-assisted selection to improve the nutrient quality of rice breeding programmes.     

Combined effects of sea water acidification and copper exposure on the symbiont-bearing foraminifer <Emphasis Type="Italic">Amphistegina gibbosa</Emphasis>

Coral reefs are threatened by global and local stressors such as ocean acidification and trace metal contamination. Reliable early warning monitoring tools are needed to assess and monitor coral reef health. Symbiont-bearing foraminifers (Amphistegina gibbosa) were kept under ambient conditions (no sea water acidification and no copper addition) or exposed to combinations of different levels of sea water pH (8.1, 7.8, 7.5 and 7.2) and environmentally relevant concentrations of dissolved copper (measured: 1.0, 1.6, 2.3 and 3.2 µg L^?1) in a mesocosm system. After 10- and 25-d exposure, foraminifers were analyzed for holobiont Ca²⁺-ATPase activity, bleaching, growth and mortality. Enzyme activity was inhibited in foraminifers exposed to pH 7.2 and 3.2 µg L^?1 Cu for 25 d. Bleaching frequency was also higher at pH 7.2 combined with copper addition. There was no significant effect of sea water acidification and copper addition on mortality. However, test size was smaller in foraminifers exposed to copper, with a positive interactive effect of sea water acidification. These findings can be explained by the higher availability of free copper ions at lower water pH. This condition would increase Cu competition with Ca²⁺ for the binding sites on the organism, thus inhibiting Ca²⁺-ATPase activity and affecting the organism’s overall fitness. Findings reported here suggest that key processes in A. gibbosa, such as calcification and photosynthesis, are affected by the combined effect of global (sea water acidification) and local (copper contamination) stressors. Considering the experimental conditions employed (mesocosm system, possible ocean acidification scenarios, low copper concentrations, biomarkers of ecological relevance and chronic exposure), our findings support the use of foraminifera and biomarkers analyzed in the present study as reliable tools to detect and monitor the ecological impacts of multiple stressors in coral reef environments.     

Horizontal transfer of the C-termini of <Emphasis Type="Italic">tccC</Emphasis> genes in <Emphasis Type="Italic">Photorhabdus</Emphasis> and <Emphasis Type="Italic">Xenorhabdus</Emphasis>

The high molecular weight insecticidal toxin complexes (Tcs), including four toxin-complex loci (tca, tcb, tcc and tcd), were first identified in Photorhabdus luminescens W14. Each member of tca, tcb or tcc is required for oral toxicity of Tcs. However, the sequence sources of the C-termini of tccC3, tccC4, tccC6 and tccC7 are unknown. Here, we performed a whole genome survey to identify the orthologs of Tc genes, and found 165 such genes in 14 bacterial genomes, including 40 genes homologous to tccC1-7 in P. luminescens TT01. The sequence sources of the C-termini of tccC2-6 were determined by sequence analysis. Further phylogenetic investigations suggested that the C-termini of 6 tccC genes experienced horizontal gene transfer events.     

Role of Arabidopsis <Emphasis Type="Italic">ABF1</Emphasis>/<Emphasis Type="Italic">3</Emphasis>/<Emphasis Type="Italic">4</Emphasis> during <Emphasis Type="Italic">det1</Emphasis> germination in salt and osmotic stress conditions

Key message

Arabidopsis det1 mutants exhibit salt and osmotic stress resistant germination. This phenotype requires HY5, ABF1, ABF3, and ABF4.

Abstract

While DE-ETIOLATED 1 (DET1) is well known as a negative regulator of light development, here we describe how det1 mutants also exhibit altered responses to salt and osmotic stress, specifically salt and mannitol resistant germination. LONG HYPOCOTYL 5 (HY5) positively regulates both light and abscisic acid (ABA) signalling. We found that hy5 suppressed the det1 salt and mannitol resistant germination phenotype, thus, det1 stress resistant germination requires HY5. We then queried publically available microarray datasets to identify genes downstream of HY5 that were differentially expressed in det1 mutants. Our analysis revealed that ABA regulated genes, including ABA RESPONSIVE ELEMENT BINDING FACTOR 3 (ABF3), are downregulated in det1 seedlings. We found that ABF3 is induced by salt in wildtype seeds, while homologues ABF4 and ABF1 are repressed, and all three genes are underexpressed in det1 seeds. We then investigated the role of ABF3, ABF4, and ABF1 in det1 phenotypes. Double mutant analysis showed that abf3, abf4, and abf1 all suppress the det1 salt/osmotic stress resistant germination phenotype. In addition, abf1 suppressed det1 rapid water loss and open stomata phenotypes. Thus interactions between ABF genes contribute to det1 salt/osmotic stress response phenotypes.

     

Interseasonal and interspecies diversities of <Emphasis Type="Italic">Symbiodinium</Emphasis> density and effective photochemical efficiency in five dominant reef coral species from Luhuitou fringing reef,northern South China Sea

Although it is well established that different coral species have different susceptibilities to thermal stress, the reasons behind this variation are still unclear. In this study, 384 samples across five dominant coral species were collected seasonally between September 2013 and August 2014 at Luhuitou fringing reef in Sanya, Hainan Island, northern South China Sea, and their algal symbiont density and effective photochemical efficiency (Φ _PSII) were measured. The results indicated that both the Symbiodinium density and Φ _PSII of corals were subject to significant interspecies and seasonal variations. Stress-tolerant coral species, including massive Porites lutea and plating Pavona decussata, had higher symbiont densities but lower Φ _PSII compared to the vulnerable branching species of Acropora over the course of all four seasons. Seasonally, coral symbiont densities were the lowest during winter, while during the same period, Φ _PSII of corals was at the highest point. Further analysis suggested that dissolved inorganic nutrients and upwelling in the reef area were probably responsible for the observed seasonal variations in symbiont density. The fact that Porites lutea has the lowest Φ _PSII during all four seasons is likely related to their symbionts’ lower capacity to provide required photosynthates for calcification. These results suggest that a coral’s thermal tolerance is primarily and positively dependent on its symbiont density and is less related to its effective photochemical efficiency.     

Distributional and ecophysiological study on the Antarctic lichens species pair <Emphasis Type="Italic">Usnea antarctica</Emphasis>/<Emphasis Type="Italic">Usnea aurantiaco</Emphasis>-<Emphasis Type="Italic">atra</Emphasis>

The factors that control lichen distribution in Antarctica are still not well understood, and in this investigation we focused on the distribution, local and continental, and gas exchange of a species pair, closely related lichens with differing reproductive strategies, Usnea aurantiaco-atra (fertile) and Usnea antarctica (sterile, sorediate). The local distributions of these species were recorded along an altitudinal gradient of nearly 300 m at South Bay, Livingston Island, and microclimate was also recorded over 1 year. The photosynthetic responses to temperature, light and thallus water content were determined under controlled conditions in the laboratory. The species were almost identical in their photosynthetic profiles. Locally, on Livingston Island, U. antarctica was confined to low altitude sites which were warmer and drier, whilst U. aurantiaco-atra was present at all altitudes. This contrasts with its distribution across Antarctica where U. antarctica grows 9° latitude further south than U. aurantiaco-atra. Temperature appears not to be the main controller of distribution in these species, but dryness of habitat, which will influence length of activity periods, may be important.     

Hyperstability masks declines in bumphead parrotfish (<Emphasis Type="Italic">Bolbometopon muricatum</Emphasis>) populations

Bolbometopon muricatum, the largest species of parrotfish, is a functionally important species that is characterised by the formation of aggregations for foraging, reproductive, and sleeping behaviours. Aggregations are restricted to shallow reef habitats, the locations of which are often known to local fishers. Bolbometopon muricatum fisheries are therefore vulnerable to overfishing and are likely to exhibit hyperstability, the maintenance of high catch per unit effort (CPUE) while population abundance declines. In this study, we provide a clear demonstration of hyperstable dynamics in a commercial B. muricatum fishery in Isabel Province, Solomon Islands. Initially, we used participatory mapping to demarcate the Kia fishing grounds into nine zones that had experienced different historic levels of fishing pressure. We then conducted comprehensive underwater visual census (UVC) and CPUE surveys across these zones over a 21-month period in 2012–2013. The individual sites for replicate UVC surveys were selected using a generalised random tessellation stratified variable probability design, while CPUE surveys involved trained provincial fisheries officers and local spearfishers. A comparison of fishery-independent abundance data and fishery-dependent CPUE data indicate extreme hyperstability, with CPUE maintained as B. muricatum abundance declines towards zero. Hyperstability may explain the sudden collapses of many B. muricatum spear fisheries across the Pacific and highlights the limitations of using data-poor fisheries assessment methods to evaluate the status of commercially valuable coral reef fishes that form predicable aggregations.