Ocean acidification represents a key threat to coral reefs by reducing the calcification rate of framework builders. In addition, acidification is likely to affect the relationship between corals and their symbiotic dinoflagellates and the productivity of this association. However, little is known about how acidification impacts on the physiology of reef builders and how acidification interacts with warming. Here, we report on an 8-week study that compared bleaching, productivity, and calcification responses of crustose coralline algae (CCA) and branching (Acropora) and massive (Porites) coral species in response to acidification and warming. Using a 30-tank experimental system, we manipulated CO2 levels to simulate doubling and three-to fourfold increases [Intergovernmental Panel on Climate Change (IPCC) projection categories IV and VI] relative to present-day levels under cool and warm scenarios. Results indicated that high CO2 is a bleaching agent for corals and CCA under high irradiance, acting synergistically with warming to lower thermal bleaching thresholds. We propose that CO2 induces bleaching via its impact on photoprotective mechanisms of the photosystems. Overall, acidification impacted more strongly on bleaching and productivity than on calcification. Interestingly, the intermediate, warm CO 2 scenario led to a 30% increase in productivity in Acropora, whereas high CO 2 lead to zero productivity in both corals. CCA were most sensitive to acidification, with high CO 2 leading to negative productivity and high rates of net dissolution. Our findings suggest that sensitive reef-building species such as CCA may be pushed beyond their thresholds for growth and survival within the next few decades whereas corals will show delayed and mixed responses.climate change ͉ global warming ͉ carbon dioxide ͉ Great Barrier Reef T he concentrations of atmospheric CO 2 predicted for this century present two major challenges for coral-reef building organisms (1). Firstly, rising sea surface temperatures associated with CO 2 increase will lead to an increased frequency and severity of coral bleaching events (large-scale disintegration of the critically important coral-dinoflagellate symbiosis) with negative consequences for coral survival, growth, and reproduction (2). Secondly, Ͼ30% of the CO 2 emitted to the atmosphere by human activities is taken up by the ocean (3, 4), lowering the pH of surface waters to levels that will potentially compromise or prevent calcium carbonate accretion by organisms including reef corals (1, 5), calcifying algae (6, 7) and a diverse range of other organisms (8). Ocean acidification research has focused mainly on the consequences of shifting ocean chemistry toward suboptimal saturation states of aragonite and calcite (9) and how this will affect the calcification processes of organisms in the pelagic (10) and benthic (11, 12) environments. Previous studies have shown dissolution of coral skeletons (13) and reduced rates of reef calcification (14) with increasing CO 2 concentrations. Ocea...
Coral reefs are found in a wide range of environments, where they provide food and habitat to a large range of organisms as well as providing many other ecological goods and services. Warm-water coral reefs, for example, occupy shallow sunlit, warm, and alkaline waters in order to grow and calcify at the high rates necessary to build and maintain their calcium carbonate structures. At deeper locations (40-150 m), "mesophotic" (low light) coral reefs accumulate calcium carbonate at much lower rates (if at all in some cases) yet remain important as habitat for a wide range of organisms, including those important for fisheries. Finally, even deeper, down to 2,000 m or more, the so-called "cold-water" coral reefs are found in the dark depths. Despite their importance, coral reefs are facing significant challenges from human activities including pollution, over-harvesting, physical destruction, and climate change. In the latter case, even lower greenhouse gas emission scenarios (such as Representative Concentration Pathway RCP 4.5) are likely drive the elimination of most warm-water coral reefs by 2040-2050. Cold-water corals are also threatened by warming temperatures and ocean acidification although evidence of the direct effect of climate change is less clear. Evidence that coral reefs can adapt at rates which are sufficient for them to keep up with rapid ocean warming and acidification is minimal, especially given that corals are long-lived and hence have slow rates of evolution. Conclusions that coral reefs will migrate to higher latitudes as they warm are equally unfounded, with the observations of tropical species appearing at high latitudes "necessary but not sufficient" evidence that entire coral reef ecosystems are shifting. On the contrary, coral reefs are likely to degrade rapidly over the next 20 years, presenting fundamental challenges for the 500 million people who derive food, income, coastal protection, and a range of other services from coral reefs. Unless rapid advances to the goals of the Paris Climate Change Agreement occur over the next decade, hundreds of millions of people are likely to face increasing amounts of poverty and social disruption, and, in some cases, regional insecurity.
Assimilation of inorganic nitrogen from nutrient-poor tropical seas is an essential challenge for the endosymbiosis between reef-building corals and dinoflagellates. Despite the clear evidence that reef-building corals can use ammonium as inorganic nitrogen source, the dynamics and precise roles of host and symbionts in this fundamental process remain unclear. Here, we combine high spatial resolution ion microprobe imaging (NanoSIMS) and pulse-chase isotopic labeling in order to track the dynamics of ammonium incorporation within the intact symbiosis between the reefbuilding coral Acropora aspera and its dinoflagellate symbionts. We demonstrate that both dinoflagellate and animal cells have the capacity to rapidly fix nitrogen from seawater enriched in ammonium (in less than one hour). Further, by establishing the relative strengths of the capability to assimilate nitrogen for each cell compartment, we infer that dinoflagellate symbionts can fix 14 to 23 times more nitrogen than their coral host cells in response to a sudden pulse of ammoniumenriched seawater. Given the importance of nitrogen in cell maintenance, growth and functioning, the capability to fix ammonium from seawater into the symbiotic system may be a key component of coral nutrition. Interestingly, this metabolic response appears to be triggered rapidly by episodic nitrogen availability. The methods and results presented in this study open up for the exploration of dynamics and spatial patterns associated with metabolic activities and nutritional interactions in a multitude of organisms that live in symbiotic relationships.
As atmospheric levels of CO2 increase, reef-building corals are under greater stress from both increased sea surface temperatures and declining sea water pH. To date, most studies have focused on either coral bleaching due to warming oceans or declining calcification due to decreasing oceanic carbonate ion concentrations. Here, through the use of physiology measurements and cDNA microarrays, we show that changes in pH and ocean chemistry consistent with two scenarios put forward by the Intergovernmental Panel on Climate Change (IPCC) drive major changes in gene expression, respiration, photosynthesis and symbiosis of the coral, Acropora millepora, before affects on biomineralisation are apparent at the phenotype level. Under high CO2 conditions corals at the phenotype level lost over half their Symbiodinium populations, and had a decrease in both photosynthesis and respiration. Changes in gene expression were consistent with metabolic suppression, an increase in oxidative stress, apoptosis and symbiont loss. Other expression patterns demonstrate upregulation of membrane transporters, as well as the regulation of genes involved in membrane cytoskeletal interactions and cytoskeletal remodeling. These widespread changes in gene expression emphasize the need to expand future studies of ocean acidification to include a wider spectrum of cellular processes, many of which may occur before impacts on calcification.
BackgroundCoral reefs around the world are experiencing large-scale degradation, largely due to global climate change, overfishing, diseases and eutrophication. Climate change models suggest increasing frequency and severity of warming-induced coral bleaching events, with consequent increases in coral mortality and algal overgrowth. Critically, the recovery of damaged reefs will depend on the reversibility of seaweed blooms, generally considered to depend on grazing of the seaweed, and replenishment of corals by larvae that successfully recruit to damaged reefs. These processes usually take years to decades to bring a reef back to coral dominance.Methodology/Principal FindingsIn 2006, mass bleaching of corals on inshore reefs of the Great Barrier Reef caused high coral mortality. Here we show that this coral mortality was followed by an unprecedented bloom of a single species of unpalatable seaweed (Lobophora variegata), colonizing dead coral skeletons, but that corals on these reefs recovered dramatically, in less than a year. Unexpectedly, this rapid reversal did not involve reestablishment of corals by recruitment of coral larvae, as often assumed, but depended on several ecological mechanisms previously underestimated.Conclusions/SignificanceThese mechanisms of ecological recovery included rapid regeneration rates of remnant coral tissue, very high competitive ability of the corals allowing them to out-compete the seaweed, a natural seasonal decline in the particular species of dominant seaweed, and an effective marine protected area system. Our study provides a key example of the doom and boom of a highly resilient reef, and new insights into the variability and mechanisms of reef resilience under rapid climate change.
Reef-building corals are fundamental to the most diverse marine ecosystems, yet a detailed understanding of the processes involved in the establishment, persistence and ecology of the coral-dinoflagellate association remains largely unknown. This study explores symbiont diversity in relation to habitat by employing a broad-scale sampling regime using ITS2 and denaturing gradient gel electrophoresis. Samples from Pocillopora damicornis, Stylophora pistillata and Seriatopora hystrix all harboured host-specific clade C symbiont types at Heron Island (Great Barrier Reef, Australia). While Ser. hystrix associated with a single symbiont profile along its entire depth distribution, both P. damicornis and Sty. pistillata associated with multiple symbiont profiles that showed a strong zonation with depth. It is shown that, with an increased sampling effort, previously identified 'rare' symbiont types within this group of host species are in fact environmental specialists. A multivariate approach was used to expand on the common distinction of symbionts by a single genetic identity. It shows merit in its capacity not only to include all the variability present within the marker region but also to reliably represent ecological diversification of symbionts. Furthermore, the cohesive species concept is explored to explain how niche partitioning may drive diversification of closely related symbiont lineages. This study provides thus evidence that closely related symbionts are ecologically distinct and fulfil their own niche within the ecosystem provided by the host and external environment.
The diversity of symbiotic dinoflagellates (Symbiodinium) in pocilloporid corals originating from various reef habitats surrounding Heron Island, southern Great Barrier Reef, was examined by targeting ribosomal, mitochondrial, and chloroplast genes using six methods that analyse for sequence differences. The ability of each of 13 genetic analyses to characterize eight ecologically distinct Symbiodinium spp. was dependent on the level of conservation of the gene region targeted and the technique used. Other than differences in resolution, phylogenetic reconstructions using nuclear and organelle gene sequences were complementary and when combined produced a well-resolved phylogeny. Analysis of the ribosomal internal transcribed spacers using denaturing gradient gel electrophoresis fingerprinting in combination with sequencing of dominant bands provided a precise method for rapidly resolving and characterizing symbionts into ecologically and evolutionarily distinct units of diversity. Single-stranded conformation polymorphisms of the nuclear ribosomal large subunit (D1/D2 domain) identified the same number of ecologically distinct Symbiodinium spp., but profiles were less distinctive. The repetitive sequencing of bacterially cloned ITS2 polymerase chain reaction amplifications generated numerous sequence variants that clustered together according to the symbiont under analysis. The phylogenetic relationships between these clusters show how intragenomic variation in the ribosomal array diverges among closely related eukaryotic genomes. The strong correlation between phylogenetically independent lineages with different ecological and physiological attributes establishes a clear basis for assigning species designations to members of the genus Symbiodinium.
Reef-building corals are renowned for their brilliant colours yet the biochemical basis for the pigmentation of corals is unknown. Here, we show that these colours are due to a family of GFP-like proteins that¯uoresce under ultraviolet (UV) or visible light. Pigments from ten coral species were almost identical to pocilloporin (Dove et al. 1995) being dimers or trimers with approximately 28-kDa subunits. Degenerative primers made to common N-terminal sequences yielded a complete sequence from reef-building coral cDNA, which had 19.6% amino acid identity with green¯uo-rescent protein (GFP). Molecular modelling revealed a`b-can' structure, like GFP, with 11 b-strands and a completely solvent-inaccessible¯uorophore composed of the modi®ed residues Gln-61, Tyr-62 and Gly-63. The molecular properties of pocilloporins indicate a range of functions from the conversion of high-intensity UV radiation into photosynthetically active radiation (PAR) that can be regulated by the dino¯agellate peridininchlorophyll-protein (PCP) complex, to the shielding of the Soret and Q x bands of chlorophyll a and c from scattered high-intensity light. These properties of pocilloporin support its potential role in protecting the photosynthetic machinery of the symbiotic dino¯agel-lates of corals under high light conditions and in enhancing the availability of photosynthetic light under shade conditions.
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