Shashank Keshavmurthy

Climate change impacts on coral reefs: Synergies with local effects, possibilities for acclimation, and management implications

Most reviews concerning the impact of climate change on coral reefs discuss independent effects of warming or ocean acidification. However, the interactions between these, and between these and direct local stressors are less well addressed. This review underlines that coral bleaching, acidification, and diseases are expected to interact synergistically, and will negatively influence survival, growth, reproduction, larval development, settlement, and post-settlement development of corals. Interactions with local stress factors such as pollution, sedimentation, and overfishing are further expected to compound effects of climate change. Reduced coral cover and species composition following coral bleaching events affect coral reef fish community structure, with variable outcomes depending on their habitat dependence and trophic specialisation. Ocean acidification itself impacts fish mainly indirectly through disruption of predation- and habitat-associated behavior changes. Zooxanthellate octocorals on reefs are often overlooked but are substantial occupiers of space; these also are highly susceptible to bleaching but because they tend to be more heterotrophic, climate change impacts mainly manifest in terms of changes in species composition and population structure. Non-calcifying macroalgae are expected to respond positively to ocean acidification and promote microbe-induced coral mortality via the release of dissolved compounds, thus intensifying phase-shifts from coral to macroalgal domination. Adaptation of corals to these consequences of CO2 rise through increased tolerance of corals and successful mutualistic associations between corals and zooxanthellae is likely to be insufficient to match the rate and frequency of the projected changes. Impacts are interactive and magnified, and because there is a limited capacity for corals to adapt to climate change, global targets of carbon emission reductions are insufficient for coral reefs, so lower targets should be pursued. Alleviation of most local stress factors such as nutrient discharges, sedimentation, and overfishing is also imperative if sufficient overall resilience of reefs to climate change is to be achieved.

Development of gene expression markers of acute heat-light stress in reef-building corals of the genus Porites.

Coral reefs are declining worldwide due to increased incidence of climate-induced coral bleaching, which will have widespread biodiversity and economic impacts. A simple method to measure the sub-bleaching level of heat-light stress experienced by corals would greatly inform reef management practices by making it possible to assess the distribution of bleaching risks among individual reef sites. Gene expression analysis based on quantitative PCR (qPCR) can be used as a diagnostic tool to determine coral condition in situ. We evaluated the expression of 13 candidate genes during heat-light stress in a common Caribbean coral Porites astreoides, and observed strong and consistent changes in gene expression in two independent experiments. Furthermore, we found that the apparent return to baseline expression levels during a recovery phase was rapid, despite visible signs of colony bleaching. We show that the response to acute heat-light stress in P. astreoides can be monitored by measuring the difference in expression of only two genes: Hsp16 and actin. We demonstrate that this assay discriminates between corals sampled from two field sites experiencing different temperatures. We also show that the assay is applicable to an Indo-Pacific congener, P. lobata, and therefore could potentially be used to diagnose acute heat-light stress on coral reefs worldwide.

DNA barcoding reveals the coral “laboratory-rat”, Stylophora pistillata encompasses multiple identities

Stylophora pistillata is a widely used coral “lab-rat” species with highly variable morphology and a broad biogeographic range (Red Sea to western central Pacific). Here we show, by analysing Cytochorme Oxidase I sequences, from 241 samples across this range, that this taxon in fact comprises four deeply divergent clades corresponding to the Pacific-Western Australia, Chagos-Madagascar-South Africa, Gulf of Aden-Zanzibar-Madagascar, and Red Sea-Persian/Arabian Gulf-Kenya. On the basis of the fossil record of Stylophora, these four clades diverged from one another 51.5-29.6 Mya, i.e., long before the closure of the Tethyan connection between the tropical Indo-West Pacific and Atlantic in the early Miocene (16–24 Mya) and should be recognised as four distinct species. These findings have implications for comparative ecological and/or physiological studies carried out using Stylophora pistillata as a model species, and highlight the fact that phenotypic plasticity, thought to be common in scleractinian corals, can mask significant genetic variation.

Symbiont communities and host genetic structure of the brain coral Platygyra verweyi, at the outlet of a nuclear power plant and adjacent areas

In the context of rising seawater temperatures associated with climate change,  the issue of whether coral holobionts deal with this challenge by shuffling their associations with stress‐ and/or heat‐tolerant Symbiodinium, by generating heat‐resistant host genotypes, or both is important for coral survival. In this study, the composition of communities of the endosymbiont Symbiodinium and the population genetics of the coral host Platygyra verweyi were examined in a reef impacted by hot‐water discharged from the outlet of a nuclear power plant in operation in Kenting, Southern Taiwan since 1984. The water at this site is 2.0–3.0 °C warmer than adjacent reefs in summer, which have an average seawater temperature of 29.0 °C. The data were compared with those for the same species at other sites within 12 km of the outlet site. Platygyra verwyei was associated with one or both of Symbiodinium types C3 (heat sensitive) and D1a (heat tolerant) at all sites with the latter being the dominant at the nuclear power plant outlet. The proportion of C3 in populations increased gradually with increasing distance from the hot‐water discharge. Genetic analysis of the Platygyra verweyi host using mitochondrial and nuclear markers showed no genetic differentiation among sites. Changes in the composition of Symbiodinium types associated with P. verweyi among closely located sites in Kenting suggested that this coral might have acclimatized to the constant thermal stress by selective association with heat‐tolerant Symbiodinium types, whereas the role of the host in adaptation was inconclusive.

Molecular Evidence Shows Low Species Diversity of Coral-Associated Hydroids in Acropora Corals

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.

Coverage, diversity, and functionality of a high-latitude coral community (Tatsukushi, Shikoku Island, Japan).

Background Seawater temperature is the main factor restricting shallow-water zooxanthellate coral reefs to low latitudes. As temperatures increase, coral species and perhaps reefs may move into higher-latitude waters, increasing the chances of coral reef ecosystems surviving despite global warming. However, there is a growing need to understand the structure of these high-latitude coral communities in order to analyze their future dynamics and to detect any potential changes. Methodology/Principal Findings The high-latitude (32.75°N) community surveyed was located at Tatsukushi, Shikoku Island, Japan. Coral cover was 60±2% and was composed of 73 scleractinian species partitioned into 7 functional groups. Although only 6% of species belonged to the ‘plate-like’ functional group, it was the major contributor to species coverage. This was explained by the dominance of plate-like species such as Acropora hyacinthus and A. solitaryensis. Comparison with historical data suggests a relatively recent colonization/development of A. hyacinthus in this region and a potential increase in coral diversity over the last century. Low coverage of macroalgae (2% of the benthic cover) contrasted with the low abundance of herbivorous fishes, but may be reasonably explained by the high density of sea urchins (12.9±3.3 individuals m−2). Conclusions/Significance The structure and composition of this benthic community are relatively remarkable for a site where winter temperature can durably fall below the accepted limit for coral reef development. Despite limited functionalities and functional redundancy, the current benthic structure might provide a base upon which a reef could eventually develop, as characterized by opportunistic and pioneer frame-building species. In addition to increasing seawater temperatures, on-going management actions and sea urchin density might also explain the observed state of this community. A focus on such ‘marginal’ communities should be a priority, as they can provide important insights into how tropical corals might cope with environmental changes.

Can resistant coral-Symbiodinium associations enable coral communities to survive climate change? A study of a site exposed to long-term hot water input

Climate change has led to a decline in the health of corals and coral reefs around the world. Studies have shown that, while some corals can cope with natural and anthropogenic stressors either through resistance mechanisms of coral hosts or through sustainable relationships with Symbiodinium clades or types, many coral species cannot. Here, we show that the corals present in a reef in southern Taiwan, and exposed to long-term elevated seawater temperatures due to the presence of a nuclear power plant outlet (NPP OL), are unique in terms of species and associated Symbiodinium types. At shallow depths (<3 m), eleven coral genera elsewhere in Kenting predominantly found with Symbiodinium types C1 and C3 (stress sensitive) were instead hosting Symbiodinium type D1a (stress tolerant) or a mixture of Symbiodinium type C1/C3/C21a/C15 and Symbiodinium type D1a. Of the 16 coral genera that dominate the local reefs, two that are apparently unable to associate with Symbiodinium type D1a are not present at NPP OL at depths of <3 m. Two other genera present at NPP OL and other locations host a specific type of Symbiodinium type C15. These data imply that coral assemblages may have the capacity to maintain their presence at the generic level against long-term disturbances such as elevated seawater temperatures by acclimatization through successful association with a stress-tolerant Symbiodinium over time. However, at the community level it comes at the cost of some coral genera being lost, suggesting that species unable to associate with a stress-tolerant Symbiodinium are likely to become extinct locally and unfavorable shifts in coral communities are likely to occur under the impact of climate change.

Diversity and Distribution of Symbiodinium Associated with Seven Common Coral Species in the Chagos Archipelago, Central Indian Ocean

The Chagos Archipelago designated as a no-take marine protected area in 2010, lying about 500 km south of the Maldives in the Indian Ocean, has a high conservation priority, particularly because of its fast recovery from the ocean-wide massive coral mortality following the 1998 coral bleaching event. The aims of this study were to examine Symbiodinium diversity and distribution associated with scleractinian corals in five atolls of the Chagos Archipelago, spread over 10,000 km 2. Symbiodinium clade diversity in 262 samples of seven common coral species, Acropora muricata, Isopora palifera, Pocillopora damicornis, P. verrucosa, P. eydouxi, Seriatopora hystrix, and Stylophora pistillata were determined using PCR-SSCP of the ribosomal internal transcribed spacer 1 (ITS1), PCR-DDGE of ITS2, and phylogenetic analyses. The results indicated that Symbiodinium in clade C were the dominant symbiont group in the seven coral species. Our analysis revealed types of Symbiodinium clade C specific to coral species. Types C1 and C3 (with C3z and C3i variants) were dominant in Acroporidae and C1 and C1c were the dominant types in Pocilloporidae. We also found 2 novel ITS2 types in S. hystrix and 1 novel ITS2 type of Symbiodinium in A. muricata. Some colonies of A. muricata and I. palifera were also associated with Symbiodinium A1. These results suggest that corals in the Chagos Archipelago host different assemblages of Symbiodinium types then their conspecifics from other locations in the Indian Ocean; and that future research will show whether these patterns in Symbiodinium genotypes may be due to local adaptation to specific conditions in the Chagos.

Genetic evidence of peripheral isolation and low diversity in marginal populations of the Acropora hyacinthus complex

Zooxanthellate corals are found throughout the tropics, but also extend into subtropical and marginal locations due to the presence of warm ocean currents. The population history of corals in marginal locations is of great interest in relation to changing global climatic conditions, as species edge zones might play an important role in evolutionary innovation. Here, we examine the genetic structure of a widely distributed coral species complex, Acroporahyacinthus, from tropical to high subtropical regions along the Kuroshio Current in Taiwan and Japan. Population genetic analysis of 307 specimens from 18 locations (7 reefal and 11 marginal) identified at least four genetic lineages within the A. hyacinthus complex: HyaA, HyaB, HyaC (dominating reefal locations) and HyaD dominating marginal locations in mainland Japan and Taiwan, except the upper Penghu Islands, which were dominated by HyaC. Crossing experiments suggested semi-incompatibility and hybridization between HyaC and D from reefal locations, implying that the existence of hybridization partners enhances diversification and genetic diversity. An incomplete barrier between the HyaC and HyaD dominations was found along the two straits in the Ryukyu Islands, where Kuroshio Current flows constantly. Despite geographical distance, the genetic composition of populations in mainland Japan was comparable to that in mainland Taiwan, which may reflect a region-specific connectivity around the northern limit of A. hyacinthus in the Pacific. In contrast, populations in the Ryukyu Islands were not significantly different from those of Palau and the Great Barrier Reef. While the precise taxonomic nature of the lineages found around the Kuroshio Current remains to be elucidated, these results indicate that, despite the presence of four lineages in the Kuroshio triangle, low genetic diversity populations of the two main lines might be isolating and differentiating in the marginal region.

Population dynamics of a high-latitude coral Alveopora japonica Eguchi from Jeju Island, off the southern coast of Korea

Although coral reefs are facing severe challenges from a variety of natural and anthropogenic stresses, there is anecdotal evidence that the high-latitude coral species Alveopora japonica Eguchi, 1968, has increased its population over the past two decades around Jeju Island, off the southern coast of Korea. The present study provides the first ecological data on this species. Alveopora japonica is opportunistically occupying the empty space left vacant following the recent kelp-forest decline. Colony abundance, age- and size-frequency distributions, lifespan, growth rates and biological characteristics such as surface area, weight and volume of two A. japonica populations in Jeju Island were investigated. Alveopora japonica around Jeju Island is characterised by a mean colony size of 30cm2, a slow growth rate (4.8mm year–1), and a short lifespan of 12–13 years, as determined by X-radiographic measurements. Alveopora japonica presented a dense population of 120 colonies m–2 on average. Population-age and -size structures at both sites reflected a healthy status and indicated a local stability, with a stationary size structure allowing population maintenance over time. The present study provided data to develop population-dynamics models to predict the potential outcomes of A. japonica populations to alternative management scenarios in Jeju Island.