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

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

     

Metabolite pools of the reef building coral Montipora capitata are unaffected by Symbiodiniaceae community composition

Some reef corals form stable, dominant or codominant associations with multiple endosymbiotic dinoflagellate species (family Symbiodiniaceae). Given the immense genetic and physiological diversity within this family, Symbiodiniaceae community composition has the potential to impact the nutritional physiology and fitness of the cnidarian host and all associated symbionts. Here we assessed the impact of the symbiont community composition on the metabolome of the coral Montipora capitata in Kāne‘ohe Bay, Hawai‘i, where different colonies can be dominated by stress-tolerant Durusdinium glynnii or stress-sensitive Cladocopium spp. Based on our existing knowledge of these symbiont taxa, we hypothesised that the metabolite profile of D. glynnii-dominated corals would be consistent with poorer nutritional support of the host relative to those corals dominated by Cladocopium spp. However, comparative metabolite profiling revealed that the metabolite pools of the host and symbiont were unaffected by differences in the abundance of the two symbionts within the community. The abundance of the individual metabolites was the same in the host and in the endosymbiont regardless of whether the host was populated with D. glynnii or Cladocopium spp. These results suggest that coral-dinoflagellate symbioses have the potential to undergo physiological adjustments over time to accommodate differences in their resident symbionts. Such mechanisms may involve host heterotrophic compensation (increasing the level of nutrition generated by feeding relative to delivery from the algae), dynamic regulation of metabolic pathways when exchange of metabolites between the organisms differs, and/or modification of both the type and quantity of metabolites that are exchanged. We discuss these adjustments and the implications for the physiology and survival of reef corals under changing environmental regimes.

     

Regulation of apoptotic mediators reveals dynamic responses to thermal stress in the reef building coral Acropora millepora

Background

Mass coral bleaching is increasing in scale and frequency across the world''s coral reefs and is being driven primarily by increased levels of thermal stress arising from global warming. In order to understand the impacts of projected climate change upon corals reefs, it is important to elucidate the underlying cellular mechanisms that operate during coral bleaching and subsequent mortality. In this respect, increased apoptotic cell death activity is an important cellular process that is associated with the breakdown of the mutualistic symbiosis between the cnidarian host and their dinoflagellate symbionts.

Methodology/Principal Findings

The present study reports the impacts of different stressors (colchicine and heat stress) on three phases of apoptosis: (i) the potential initiation by differential expression of Bcl-2 members, (ii) the execution of apoptotic events by activation of caspase 3-like proteases and (iii) and finally, the cell disposal indicated by DNA fragmentation in the reef building coral Acropora millepora. In corals incubated with colchicine, an increase in caspase 3-like activity and DNA fragmentation was associated with a relative down-regulation of Bcl-2, suggesting that the initiation of apoptosis may be mediated by the suppression of an anti-apoptotic mechanism. In contrast, in the early steps of heat stress, the induction of caspase-dependent apoptosis was related to a relative up-regulation of Bcl-2 consecutively followed by a delayed decrease in apoptosis activity.

Conclusions/Significance

In the light of these results, we propose a model of heat stress in coral hosts whereby increasing temperatures engage activation of caspase 3-dependent apoptosis in cells designated for termination, but also the onset of a delayed protective response involving overexpression of Bcl-2 in surviving cells. This mitigating response to thermal stress could conceivably be an important regulatory mechanism for cell survival in corals exposed to sudden environmental changes.     

Hypoxia in paradise: widespread hypoxia tolerance in coral reef fishes

Using respirometry, we examined the hypoxia tolerance of 31 teleost fish species (seven families) inhabiting coral reefs at a 2-5 m depth in the lagoon at Lizard Island (Great Barrier Reef, Australia). All fishes studied maintained their rate of oxygen consumption down to relatively severe hypoxia (20-30% air saturation). Indeed, most fishes appeared unaffected by hypoxia until the oxygen level fell below 10% of air saturation. This, hitherto unrecognized, hypoxia tolerance among coral reef fishes could reflect adaptations to nocturnal hypoxia in tide pools. It may also be needed to enable fishes to reside deep within branching coral at night to avoid predation. Widespread hypoxia tolerance in a habitat with such an extreme biodiversity as coral reefs indicate that there is a wealth of hypoxia related adaptations to be discovered in reef fishes.     

Genotypic variation influences reproductive success and thermal stress tolerance in the reef building coral, Acropora palmata

The branching coral Acropora palmata is a foundation species of Caribbean reefs that has been decimated in recent decades by anthropogenic and natural stressors. Declines in population density and genotypic diversity likely reduce successful sexual reproduction in this self-incompatible hermaphrodite and might impede recovery. We investigated variation among genotypes in larval development under thermally stressful conditions. Six two-parent crosses and three four-parent batches were reared under three temperatures and sampled over time. Fertilization rates differed widely with two-parent crosses having lower fertilization rates (5–56 %, mean 22 % ± 22 SD) than batches (from 31 to 87 %, mean 59 % ± 28 SD). Parentage analysis of larvae in batch cultures showed differences in gamete compatibility among parents, coinciding with significant variation in both sperm morphology and egg size. While all larval batches developed more rapidly at increased water temperatures, rate of progression through developmental stages varied among batches, as did swimming speed. Together, these results indicate that loss of genotypic diversity exacerbates already severe limitations in sexual reproductive success of A. palmata. Nevertheless, surviving parental genotypes produce larvae that do vary in their phenotypic response to thermal stress, with implications for adaptation, larval dispersal and population connectivity in the face of warming sea surface temperatures.     

Metabolomics of reef benthic interactions reveals a bioactive lipid involved in coral defence

Holobionts are assemblages of microbial symbionts and their macrobial host. As extant representatives of some of the oldest macro-organisms, corals and algae are important for understanding how holobionts develop and interact with one another. Using untargeted metabolomics, we show that non-self interactions altered the coral metabolome more than self-interactions (i.e. different or same genus, respectively). Platelet activating factor (PAF) and Lyso-PAF, central inflammatory modulators in mammals, were major lipid components of the coral holobionts. When corals were damaged during competitive interactions with algae, PAF increased along with expression of the gene encoding Lyso-PAF acetyltransferase; the protein responsible for converting Lyso-PAF to PAF. This shows that self and non-self recognition among some of the oldest extant holobionts involve bioactive lipids identical to those in highly derived taxa like humans. This further strengthens the hypothesis that major players of the immune response evolved during the pre-Cambrian.     

Unraveling the role of fungal symbionts in plant abiotic stress tolerance

Fungal symbionts have been found to be associated with every plant studied in the natural ecosystem, where they colonize and reside entirely or partially in the internal tissues of their host plant. Fungal endophytes can express/form a range of different lifestyle/relationships with different host including symbiotic, mutualistic, commensalistic and parasitic in response to host genotype and environmental factors. In mutualistic association fungal endophyte can enhance growth, increase reproductive success and confer biotic and abiotic stress tolerance to its host plant. Since abiotic stress such as, drought, high soil salinity, heat, cold, oxidative stress and heavy metal toxicity is the common adverse environmental conditions that affect and limit crop productivity worldwide. It may be a promising alternative strategy to exploit fungal endophytes to overcome the limitations to crop production brought by abiotic stress. There is an increasing interest in developing the potential biotechnological applications of fungal endophytes for improving plant stress tolerance and sustainable production of food crops. Here we have described the fungal symbioses, fungal symbionts and their role in abiotic stress tolerance. A putative mechanism of stress tolerance by symbionts has also been covered.Key words: abiotic stress, endophytes, fungal symbiont, mycorrhizal fungus, Piriformospora indica, stress tolerance, symbiosis     

Application of diet theory reveals context-dependent foraging preferences in an herbivorous coral reef fish

Dietary preferences of grazers can drive spatial variability in top-down control of autotroph communities, because diet composition may depend on the relative availability of autotroph species. On Caribbean coral reefs, parrotfish grazing is important in limiting macroalgae, but parrotfish dietary preferences are poorly understood. We applied diet-switching analysis to quantify the foraging preferences of the redband parrotfish (Sparisoma aurofrenatum). At 12 Caribbean reefs, we observed 293 redband parrotfish in 5-min feeding bouts and quantified relative benthic algal cover using quadrats. The primary diet items were macroalgal turfs, Halimeda spp., and foliose macroalgae (primarily Dictyota spp. and Lobophora spp.). When each resource was evaluated independently, there were only weak relationships between resource cover and foraging effort (number of bites taken). Electivity for each resource also showed no pattern, varying from positive (preference for the resource) to negative (avoidance) across sites. However, a diet-switching analysis consisting of pairwise comparisons of relative cover and relative foraging effort revealed clearer patterns: parrotfish (a) preferred Halimeda and macroalgal turfs equally, and those two resources were highly substitutable; (b) preferred Halimeda to foliose macroalgae, but those two resources were complementary; and (c) also preferred turf to foliose macroalgae, and those resources were also complementary. Thus parrotfish grazing rates depend on relative, not absolute, abundance of macroalgal types, due to differences in substitutability among resources. Application of similar analyses may help predict potential changes in foraging effort of benthic grazers over spatial gradients that could inform expectations for reef recovery following the protection of herbivore populations.     

The use of coral nubbins in coral reef ecotoxicology testing

While there is an urgent demand to establish reliable ecotoxicological assays for reef corals, there has not been yet an available source material that can supply the high number of colony replicates needed for reliable tests. In past experiments, the major obstacle to obtaining as many fragments as possible had been the damage inflicted to donor colonies by pruning. In this paper, we present the application of coral nubbins, a novel source material for coral ecotoxicology assays. Nubbins from the branching Red Sea coral Stylophora pistillata (n>450) were used for evaluating the impacts of water soluble fractions from a crude oil, an oil dispersant and dispersed oil. Coral nubbins (minute coral fragments in the size of one to several polyps) harvested from a single colony are genetically identical to each other, may be obtained in any quantity needed and whenever research activities demand their use. Several dozens of nubbins can be obtained from a single small branch in branching coral species, a procedure that has minimal impact on donor genotypes. Nubbins production is a low cost procedure and requires limited maintenance space. Results of short and long-term acute ecotoxicological tests are revealed and discussed here, indicating the advantageous use of nubbins as ubiquitous coral material for toxicology assays and physiological studies.     

Escaping the heat: range shifts of reef coral taxa in coastal Western Australia

One of the most critical challenges facing ecologists today is to understand the changing geographic distribution of species in response to current and predicted global warming. Coastal Western Australia is a natural laboratory in which to assess the effect of climate change on reef coral communities over a temporal scale unavailable to studies conducted solely on modern communities. Reef corals composing Late Pleistocene reef assemblages exposed at five distinct localities along the west Australian coast were censused and the results compared with coral occurrence data published for the modern reefs offshore of each locality. The resulting comparative data set comprises modern and Late Pleistocene reef coral communities occurring over approximately 12° of latitude. For the modern reefs this gradient includes the zone of overlap between the Dampierian and Flindersian Provinces. Modern reef coral communities show a pronounced gradient in coral composition over the latitudinal range encompassed by the study, while the gradient in community composition is not as strong for Pleistocene communities. Tropical‐adapted taxa contracted their ranges north since Late Pleistocene time, emplacing two biogeographic provinces in a region in which a single province had existed previously. Beta diversity values for adjacent communities also reflect this change. Modern reefs show a distinct peak in beta diversity in the middle of the region; the peak is not matched by Pleistocene reefs. Beta diversity is correlated with distance only for comparisons between modern reefs in the north and the fossil assemblages, further supporting change in distribution of the biogeographic provinces in the study area. Coral taxa present in modern communities clearly expanded and contracted their geographic ranges in response to climate change. Those taxa that distinguish Pleistocene from modern reefs are predicted to migrate south in response to future climate change, and potentially persist in ‘temperature refugia’ as tropical reef communities farther north decline.     

Physiological effects of heat and cold exposure in the common reef coral Acropora millepora

Reef-forming corals are under threat globally from climate change, leading to changes in sea temperatures with both hot and cold events recorded and projected to increase in frequency and severity in the future. Tolerance to heat and cold exposure has been found to be mutually exclusive in other marine invertebrates, but it is currently unclear whether a trade-off exists between hot and cold thermal tolerance in tropical corals. This study quantified the changes in physiology in Acropora millepora from the central Great Barrier Reef subjected to three temperature treatments; sub-lethal cold, ambient and sub-lethal heat (23.0 °C, 27.0 °C and 29.5 °C, respectively). After 10 weeks, pigment content and Symbiodiniaceae density increased in cold-treated corals but decreased in heat-treated corals relative to corals at ambient conditions. Heat-treated corals gained less mass relative to both ambient and cold-treated corals. These results indicate that the physiological condition of A. millepora corals examined here improved in response to mild cold exposure compared to ambient exposure and decreased under mild heat exposure despite both these temperatures occurring in situ around 15% of the year. The energetic condition of corals in the hotter treatment was reduced compared to both ambient and cooler groups, indicating that corals may be more resilient to mild cold exposure relative to mild heat exposure. The results indicate that the corals shifted their resource allocation in response to temperature treatment, investing more energy into skeletal extension rather than maintenance. No evidence of thermal tolerance trade-offs was found, and cold thermal tolerance was not lost in more heat-tolerant individuals. An enhanced understanding of physiological responses of corals at both ends of the thermal spectrum is important for predicting the resilience of corals under projected climate change conditions.

     

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

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

Variation in susceptibility among three Caribbean coral species and their algal symbionts indicates the threatened staghorn coral,Acropora cervicornis,is particularly susceptible to elevated nutrients and heat stress

Coral Reefs - Coral cover is declining worldwide due to multiple interacting threats. We compared the effects of elevated nutrients and temperature on three Caribbean corals: Acropora cervicornis,...     

Species-specific habitat distribution of coral reef fish assemblages in relation to habitat characteristics in an Okinawan coral reef

We determined the species-specific habitat associations of coral reef fishes and environmental characteristics in an Okinawan coral reef in Japan. We focused on three families (Pomacentridae, Gobiidae and Labridae) and attempted to determine differences in habitat utilization. We selected six sites along the coast of Amitori Bay, from the entrance to the innermost part, in order to cover a wide range of habitat characteristics (exposed habitat, semi-exposed habitat and sheltered habitat). The species diversity of coral assemblages was greater at the exposed and semi-exposed habitats, whereas branching coral mostly covered the sheltered habitat. The environmental factors that determine the species-specific spatial association in fishes differed among families. Both biological characteristics (coral morphology and coral species diversity) and physical characteristics (water depth and wave exposure) affected the spatial association of pomacentrids and gobiids. In contrast, physical characteristics such as substrate complexity and water depth affected the species-specific spatial association of labrid species. Further study is needed to determine the ecological factors that regulate the species-specific habitat preference in Okinawan coral reefs.     

Molecular characterization of the first heat shock protein 70 from a reef coral.

The branching coral Stylophora pistillata, one of the most abundant hermatypic corals along the coasts of the Red Sea, has been used for many years as a model species for coral biological studies. Here we characterize the first coral heat shock protein 70 gene (SP-HSP70), cloned from S. pistillata, to be used as a tool for studying coral stress response. The cloning was carried out by a combination of PCR methods using heterologous, degenerate HSP70-based primers, followed by plaque-lift screening of a genomic library. The sequenced clone (5212 bp), contains a complete 1953 bp, intronless open reading frame, and 5' and 3' flanking regions of 1,935 and 1,324 bp, respectively. TATA, CAAT, and ATF boxes as well as 11 putative heat shock elements were identified in the SP-HSP70 5' flanking region. A polyadenylation site was identified in the 3' flanking region. SP-HSP70 protein sequence resembles the cytosolic/nuclear HSP70 cluster. RT-PCR studies confirmed SP-HSP70 mRNA expression in corals grown within their normal physiological conditions. Furthermore, SP-HSP70 has been shown to belong to the coral genome and not to its symbiotic algae one, as revealed by SP-HSP70 PCR amplification, using purified algal and coral DNA templates.     

Subtle genetic structure reveals restricted connectivity among populations of a coral reef fish inhabiting remote atolls

We utilized a spatial and temporal analyses of genetic structure, supplemented with ecological and oceanographic analysis, to assess patterns of population connectivity in a coral reef fish Chromis margaritifer among the unique and remote atolls in the eastern Indian Ocean. A subtle, but significant genetic discontinuity at 10 microsatellite DNA loci was detected between atoll systems corresponding with a low (≤ 1%) probability of advection across the hundreds of kilometers of open ocean that separates them. Thus, although genetic connections between systems are likely maintained by occasional long-distance dispersal of C. margaritifer larvae, ecological population connectivity at this spatial scale appears to be restricted. Further, within one of these atoll systems, significant spatial differentiation among samples was accompanied by a lack of temporal pairwise differentiation between recruit and adult samples, indicating that restrictions to connectivity also occur at a local scale (tens of kilometers). In contrast, a signal of panmixia was detected at the other atoll system studied. Lastly, greater relatedness and reduced genetic diversity within recruit samples was associated with relatively large differences among them, indicating the presence of sweepstakes reproduction whereby a small proportion of adults contributes to recruitment in the next generation. These results are congruent with earlier work on hard corals, suggesting that local production of larvae drives population replenishment in these atoll systems for a range of coral reef species.