Baseline dynamics of Symbiodiniaceae genera and photochemical efficiency in corals from reefs with different thermal histories.

Ocean warming and marine heatwaves induced by climate change are impacting coral reefs globally, leading to coral bleaching and mortality. Yet, coral resistance and resilience to warming are not uniform across reef sites and corals can show inter- and intraspecific variability. To understand changes in coral health and to elucidate mechanisms of coral thermal tolerance, baseline data on the dynamics of coral holobiont performance under non-stressed conditions are needed. We monitored the seasonal dynamics of algal symbionts (family Symbiodiniaceae) hosted by corals from a chronically warmed and thermally variable reef compared to a thermally stable reef in southern Taiwan over 15 months. We assessed the genera and photochemical efficiency of Symbiodiniaceae in three coral species: Acropora nana, Pocillopora acuta, and Porites lutea. Both Durusdinium and Cladocopium were present in all coral species at both reef sites across all seasons, but general trends in their detection (based on qPCR cycle) varied between sites and among species. Photochemical efficiency (i.e., maximum quantum yield; Fv/Fm) was relatively similar between reef sites but differed consistently among species; no clear evidence of seasonal trends in Fv/Fm was found. Quantifying natural Symbiodiniaceae dynamics can help facilitate a more comprehensive interpretation of thermal tolerance response as well as plasticity potential of the coral holobiont.

Dominance of the scleractinian coral Alveopora japonica in the barren subtidal hard bottom of high-latitude Jeju Island off the south coast of Korea assessed by high-resolution underwater images.

Coastal benthic communities in temperate regions have been influenced by climate change, including increasing sea-surface temperature. Nevertheless, scleractinian coral Alveopora japonica Eguchi, 1968, is thriving in shallow subtidal hard bottoms around Jeju Island, off the southern coast of Korea. The presence of this corals has negatively impacted subtidal kelp populations in Jeju Island. However, there is no study to document how the presence or absence of this coral relates to other benthic communities. This study investigated the benthos in three shallow subtidal sites (Shinheung (SH), Bukchon (BC), and Seongsan (SS)) in northern Jeju using underwater photography. Macro-benthic organisms appearing on a 1 × 20 m line transect installed at depths of 5, 10, and 15 m at each site were analyzed. Results showed that of the three sites investigated, A. japonica colonies were most abundant at BC, accounting for 45.9% and 72.8% of the total transect area at 10 m and 15 m, respectively. At SS, A. japonica occupied 15.3% of the total area at 15 m and less than 1% at 5 m and 10 m. The same at SH accounted for 10% of the total area at 5 m, and less than 1% at 10 m and 15 m. Dead and bleached colonies accounted for 1.2-11.5% and 1.8-5.7%, respectively, at 5, 10, and 15 m at three sites. At SS, canopy-forming brown algae Ecklonia cava and Sargassum spp. accounted for 20.2 and 24.3% of the total transect area, respectively, at 5 m depth. In contrast, the percent cover of E. cava and Sargassum spp. at SH and BC ranged from 0.1 to 1.8%, respectively. Moreover, non-geniculate coralline algae dominated the subtidal substrate at SH, ranging between 60.2 and 69% at 15 and 10 m. The low cover of A. japonica in SS (at 5 m) coincided with a high percent cover of canopy-forming brown algae. However, canopy-forming brown algae were rare at all depths at SH and BC and were dominated instead by coralline algae and the scleractinian corals. This study, by utilizing a non-destructive method, provides a baseline qualitative and quantitative information for understanding the site and depth-dependent distribution of A. japonica and algal populations, which is important to understand climate change related changes in benthic communities in Jeju and elsewhere.

Learning from the past is not enough to survive present and future bleaching threshold temperatures.

In the past decade, the frequency of mass coral bleaching events has increased due to seawater temperature anomalies persisting for longer periods. Coral survival from temperature anomalies has been based on how each species in each location responds to stress, which is unique to individual species and may be due to the way stressful experiences accumulate through time in the form of ecological and physiological memory. A deeper understanding of ecological and physiological memory in corals is necessary to understand their survival strategies into the future. Laboratory experiments can help us simulate seawater temperatures experienced by corals in the past and compare their responses to those of the present and future. In this study, we sampled corals with different life history traits from one location perturbed by seawater temperature incursions (variable site) and from a second, relatively undisturbed location (stable site). We sampled across two seasons to observe the responses to bleaching threshold temperatures in the past (1998-29 °C), present (2018-31 °C), and future (2050-33 °C). Corals were healthy at 29 °C and 31 °C, but a fast-growing, temperature-susceptible coral species experienced high mortality at 33 °C compared to a slow-growing, temperature-resistant coral species. Moreover, corals from the variable site and during the spring season fared better under temperature stress. The results of this study provide insight into the possible role of life-history traits on coral's response to seasons and locations in terms of memory to long-term and short-term thermal anomalies and climate change.

Population genetics and demography of the coral-killing cyanobacteriosponge, Terpios hoshinota, in the Indo-West Pacific.

The first occurrence of the cyanobacteriosponge Terpios hoshinota was reported from coral reefs in Guam in 1973, but was only formally described in 1993. Since then, the invasive behavior of this encrusting, coral-killing sponge has been observed in many coral reefs in the West Pacific. From 2015, its occurrence has expanded westward to the Indian Ocean. Although many studies have investigated the morphology, ecology, and symbiotic cyanobacteria of this sponge, little is known of its population genetics and demography. In this study, a mitochondrial cytochrome oxidase I (COI) fragment and nuclear ribosomal internal transcribed spacer 2 (ITS2) were sequenced to reveal the genetic variation of T. hoshinota collected from 11 marine ecoregions throughout the Indo-West Pacific. Both of the statistical parsimony networks based on the COI and nuclear ITS2 were dominated by a common haplotype. Pairwise F ST and Isolation-by-distance by Mantel test of ITS2 showed moderate gene flow existed among most populations in the marine ecoregions of West Pacific, Coral Triangle, and Eastern Indian Ocean, but with a restricted gene flow between these regions and Maldives in the Central Indian Ocean. Demographic analyses of most T. hoshinota populations were consistent with the mutation-drift equilibrium, except for the Sulawesi Sea and Maldives, which showed bottlenecks following recent expansion. Our results suggest that while long-range dispersal might explain the capability of T. hoshinota to spread in the IWP, stable population demography might account for the long-term persistence of T. hoshinota outbreaks on local reefs.

Physiological plasticity of corals to temperature stress in marginal coral communities.

Adaptation and/or acclimatization through various mechanisms have been suggested to help some tropical coral species to overcome temperature-induced bleaching that is intensifying with climate change; however, while much research has been done on the physiological responses of tropical and subtropical corals to stress, little is known about these responses in corals in marginal environments-e.g., high-latitude and non-reefal communities. In this study, we examined the thermal-tolerant physiology of the flowerpot coral, Alveopora japonica, endemic to the high-latitude Jeju Island (33.39°N), South Korea and Oulastrea crispata and Coelastrea aspera from the subtropical non-reefal coral community on the Penghu Islands (23.34°N), Taiwan. Analysis of physiological parameters; photochemical efficiency, Chlorophyll pigment, Symbiodiniaceae cell number and host soluble proteins - showed that A. japonica can survive through a wide range of temperature stresses (10-32 °C) over a period of 8 days without showing signs of bleaching. In addition, corals O. crispata and C. aspera withstood temperature stresses of up to 33 °C and repeated temperature fluctuations without bleaching. Our results indicate that, under large seasonal variations and asymmetrical daily fluctuations in temperature, corals currently living in marginal environments could have thermal plasticity, allowing them to survive in the future climate change scenarios. This study reiterates the importance of studying the eco-physiology of corals that are generally ignored because of their neutral or positive responses to stress.

Demographic census confirms a stable population of the critically-endangered caryophyllid coral Polycyathus chaishanensis (Scleractinia; Caryophyllidae) in the Datan Algal Reef, Taiwan.

Polycyathus chaishanensis is a symbiotic caryophyllid coral described from a single population in a tidal pool off Chaishan, Kaohsiung, Taiwan. Due to its rarity, P. chaishanensis was declared a critically-endangered species under the Taiwan Wildlife Protection Act. In May 2017, a P. chaishanensis colony was discovered in the intertidal area of the Datan Algal Reef, Taoyuan, Taiwan. To determine whether this is a stable population in the algal reef, a demographic census-including data on occurrence, distribution, and colony size-was carried out in the algal reef in southern Taoyuan. Intertidal censuses and sediment collections were conducted at five different sections-Baiyu, Datan G1, Datan G2, Yongxing, and Yongan algal reefs-during the monthly spring low tide from July 2018 to January 2019. In total, 84 colonies-23 in Datan G1 and 61 in Datan G2-were recorded from a tidal range of - 160 to - 250 cm, according to the Taiwan Vertical Datum 2001 compiled by the Central Weather Bureau. No P. chaishanensis was found in Baiyu, Yongxing, or Yongan. The P. chaishanensis colony sizes ranged from 2.55 to 81.5 cm in diameter, with the larger P. chaishanensis present in the lower intertidal zone. Sediment was extremely high, with monthly site averages ranging from 3,818.26 to 29,166.88 mg cm-2 day-1, and there was a significant difference between sites and months, both of which affected the distribution of P. chaishanensis in the algal reef. Our study confirms the existence of a second population of P. chaishanensis in Taiwan, highlighting the importance of the Datan Algal Reef for the survival and protection of this critically-endangered caryophyllid coral and why it is so urgent that the reef should be conserved.

Specificity trumps flexibility-location-based stable associations between Symbiodiniaceae genera and Platygyra verweyi (Scleractinia; Merulinidae).

This study monitored symbiont communities bi-monthly in native coral cores used in a reciprocal transplantation of the coral Platygyra verweyi over two years (2014-2016) and samples of mother colonies from three locations with variable thermal regimes; our results show that associating with multiple Symbiodiniaceae genera (Cladocopium spp. and Durusdinium spp.) is not a prerequisite for symbiont shuffling. Platygyra verweyi associates with certain Symbiodiniaceae genera based on location. Results of quantitative real-time PCR indicated small-scale temporal changes in Symbiodiniaceae genera compositions from 2014 to 2016; however, these changes were not enough to invoke shuffling or switching, despite degree heating weeks exceeding 6 °C-weeks in 2014 and 4 °C-weeks in 2015, which usually resulted in substantial coral bleaching. Microsatellite analysis of the P. verweyi host showed no genetic differences among the study locations. Our results suggest that P. verweyi undergoes long-term acclimatization and/or adaptation based on microgeographic and local environmental conditionsby altering its combinations of associated Symbiodiniaceae. Results also suggest that shuffling might not be as common a phenomenon as it has been given credit for; corals thrive through specific associations, and many corals could still be vulnerable to climate change-induced stress, despite being promiscuous or able to associate with rare and background Symbiodiniaceae genera.

Leptoria phrygia in Southern Taiwan shuffles and switches symbionts to resist thermal-induced bleaching.

Symbiodiniaceae communities in some corals often shuffle or switch after severe bleaching events, one of the major threats to coral survival in a world with climate change. In this study we reciprocally transplanted five Leptoria phrygia colonies between two sites with significantly different temperature regimes and monitored them for 12 months. Our ITS2 amplicon deep sequencing demonstrated that L. phrygia acclimatized to maintain a strong and stable association with Durusdinium D17, D. trenchii, and D. glynnii, but also remained flexible and formed a short-term association with different Cladocopium. Most interestingly, two colonies shuffled between Durusdinium and Cladocopium without the occurrence of bleaching; one colony even switched its dominant Cladocopium after generic shuffling. Both dominant Cladocopium were originally rare with relative abundances as low as 0.024%. This is the first record of adult corals switching dominant symbiont without bleaching.

The coral Platygyra verweyi exhibits local adaptation to long-term thermal stress through host-specific physiological and enzymatic response.

Climate change threatens coral survival by causing coral bleaching, which occurs when the coral's symbiotic relationship with algal symbionts (Symbiodiniaceae) breaks down. Studies on thermal adaptation focus on symbionts because they are accessible both in vitro and in hospite. However, there is little known about the physiological and biochemical response of adult corals (without Symbiodiniaceae) to thermal stress. Here we show acclimatization and/or adaptation potential of menthol-bleached aposymbiotic coral Platygyra verweyi in terms of respiration breakdown temperature (RBT) and malate dehydrogenase (MDH) enzyme activity in samples collected from two reef sites with contrasting temperature regimes: a site near a nuclear power plant outlet (NPP-OL, with long-term temperature perturbation) and Wanlitong (WLT) in southern Taiwan. Aposymbiotic P. verweyi from the NPP-OL site had a 3.1 °C higher threshold RBT than those from WLT. In addition, MDH activity in P. verweyi from NPP-OL showed higher thermal resistance than those from WLT by higher optimum temperatures and the activation energy required for inactivating the enzyme by heat. The MDH from NPP-OL also had two times higher residual activity than that from WLT after incubation at 50 °C for 1 h. The results of RBT and thermal properties of MDH in P. verweyi demonstrate potential physiological and enzymatic response to a long-term and regular thermal stress, independent of their Symbiodiniaceae partner.

Temporal variation and photochemical efficiency of species in Symbiodinaceae associated with coral Leptoria phrygia (Scleractinia; Merulinidae) exposed to contrasting temperature regimes.

The Symbiodinaceae are paradoxical in that they play a fundamental role in the success of scleractinian corals, but also in their dismissal when under stress. In the past decades, the discovery of the endosymbiont's genetic and functional diversity has led people to hope that some coral species can survive bleaching events by associating with a stress-resistant symbiont that can become dominant when seawater temperatures increase. The variety of individual responses encouraged us to scrutinize each species individually to gauge its resilience to future changes. Here, we analyse the temporal variation in the Symbiodinaceae community associated with Leptoria phrygia, a common scleractinian coral from the Indo-Pacific. Coral colonies were sampled from two distant reef sites located in southern Taiwan that differ in temperature regimes, exemplifying a 'variable site' (VS) and a 'steady site' (SS). We investigated changes in the relative abundance of the dominant symbiont and its physiology every 3-4 months from 2016-2017. At VS, 11 of the 12 colonies were dominated by the stress-resistant Durusdinium spp. (>90% dominance) and only one colony exhibited co-dominance between Durusdinium spp. and Cladocopium spp. Every colony displayed high photochemical efficiency across all sampling periods, while showing temporal differences in symbiont density and chlorophyll a concentration. At SS, seven colonies out of 13 were dominated by Cladocopium spp., five presented co-dominance between Durusdinium spp./Cladocopium spp. and only one was dominated by Durusdinium spp. Colonies showed temporal differences in photochemical efficiency and chlorophyll a concentration during the study period. Our results suggest that VS colonies responded physiologically better to high temperature variability by associating with Durusdinium spp., while in SS there is still inter-colonial variability, a feature that might be advantageous for coping with different environmental changes.

Transcriptomic response in Acropora muricata under acute temperature stress follows preconditioned seasonal temperature fluctuations.

OBJECTIVE: Global climate change has resulted in the decline of health and condition of various coral reefs worldwide. Here, we describe expression profiles of Acropora muricata collected during opposing seasons in Otsuki, Kochi, Japan to define the capacity of corals to cope with changing environmental conditions. Coral communities in Otsuki experience large temperature fluctuations between the winter (~ 16 °C) and summer (~ 27 °C). RESULTS: Coral nubbins that were collected in the summer showed no change in photochemical efficiency when exposed to thermal or cold stress, while winter samples showed a decrease in photochemical health when subjected to thermal stress. Under cold stress, corals that were collected in the summer showed an up-regulation of actin-related protein and serine/threonine protein kinase, while corals collected during the winter did not show any cellular stress. On the other hand, under thermal stress, the most notable change was the up-regulation of phosphoenolpyruvate carboxykinase in corals that were collected during the winter season. Our observations in the differential genes expressed under temperature-derived stress suggest that A. muricata from Kochi may maintain physiological resilience due to the frequently encountered environmental stress, and this may play a role in the coral's thermal tolerance.

Development of Novel Polymorphic Microsatellite Markers in Catch Bowl Coral, Isopora palifera (Scleractinia; Acroporidae) Using Next-generation Sequencing.

Sung-Yin Yang, Wai-Ling Fong, Wenhua Savanna Chow, Chia-Min Hsu, Chia-Ling Carynn Chan, Shashank Keshavmurthy, and Chaolun Allen Chen (2018) Catch bowl coral, Isopora palifera, is a shallow- water scleractinian species distributed in the Indo-West Pacific region, and has been studied for its reproduction, symbiont diversity, and population genetics. In order to develop microsatellite markers to reveal the genetic connectivity of I. palifera in the Kenting reefs, southern Taiwan, we applied a stepwise approach including Illumina sequencing, primer screening, and validation. DNA sequences of each 6,363,035 read pairs were assembled with high coverage and sequencing depth, and 1,173,835 potential SSRs were identified. A set of 60,986 primers were designed and tested, and six novel microsatellite markers with three type motifs, including 3 di- and 3 tetra- repeats, were successfully isolated. The ranges in number of alleles per locus and observed and expected heterozygosities were 3-5, 0.444-0.538, and 0.375-0.565, respectively. Application of these loci to the genetic diversity of an I. palifera population that experienced bleaching events in the Kenting reef between 1998 and 2015 showed a signature admixture of three clusters without temporal variation. These loci are useful for studying population genetics in the genus Isopora. Our results suggest that next-generation sequencing technology is convenient and cost-effective and can be utilized to isolate microsatellites in other reef-building corals.

Repeated and Prolonged Temperature Anomalies Negate Symbiodiniaceae Genera Shuffling in the Coral Platygyra verweyi (Scleractinia; Merulinidae).

Kuo-Wei Kao, Shashank Keshavmurthy, Cing-Hsin Tsao, Jih-Terng Wang, and Chaolun Allen Chen (2018) With climate change, global average sea surface temperatures are expected to increase by 1.0-3.7°C by the end of this century. Even a 1.0°C increase in seawater temperature from local long-term summer maxima lasting for weeks to months results in bleaching and/or mortality in reef-building corals. Studies on coral resistance mechanisms have proposed a correlation between shuffling of different Symbiodiniaceae genera (changing the dominant Symbiodiniaceae genera) and putative thermal tolerance in corals. Although it was suggested that some corals can increase their tolerance by 1.0-1.5°C through shuffling to thermally tolerant Durusdinium trenchii (formerly D1a), the effects of accumulated thermal stress due to prolonged high temperatures on the survival of corals that have shuffled have not been investigated. We show herein that prolonged exposure to high temperature (> 10.43-degree heating weeks) can drastically reduce coral survival rate even after it has shuffled to stress-tolerant Symbiodiniaceae genera. Our study suggests that there is a limit to the capacity of for shuffling, and hence is likely to lose its efficacy in the future as repeated and prolonged thermal stress events become more frequent and pronounced.

Dynamics of coral-associated bacterial communities acclimated to temperature stress based on recent thermal history.

Seasonal variation in temperature fluctuations may provide corals and their algal symbionts varying abilities to acclimate to changing temperatures. We hypothesized that different temperature ranges between seasons may promote temperature-tolerance of corals, which would increase stability of a bacterial community following thermal stress. Acropora muricata coral colonies were collected in summer and winter (water temperatures were 23.4-30.2 and 12.1-23.1 °C, respectively) from the Penghu Archipelago in Taiwan, then exposed to 6 temperature treatments (10-33 °C). Changes in coral-associated bacteria were determined after 12, 24, and 48 h. Based on 16S rRNA gene amplicons and Illumina sequencing, bacterial communities differed between seasons and treatments altered the dominant bacteria. Cold stress caused slower shifts in the bacterial community in winter than in summer, whereas a more rapid shift occurred under heat stress in both seasons. Results supported our hypothesis that bacterial community composition of corals in winter are more stable in cold temperatures but changed rapidly in hot temperatures, with opposite results for the bacterial communities in summer. We infer that the thermal tolerance ranges of coral-associated bacteria, with a stable community composition, are associated with their short-term (3 mo) seawater thermal history. Therefore, seasonal acclimation may increase tolerance of coral-associated bacteria to temperature fluctuations.

Diverse responses of Symbiodinium types to menthol and DCMU treatment.

To understand the mechanism of photosynthetic inhibition and generation of reactive oxygen species (ROS) in Symbiodinium types under stress, chemicals such as dichlorophenyl dimethylurea (DCMU) are widely used. Moreover, DCMU and recently menthol were used to generate aposymbiotic cnidarian hosts. While the effects of DCMU on Symbiodinium cells have been extensively studied, no studies have shown the mechanism behind menthol-induced coral bleaching. Moreover, no study has compared the effects of DCMU and menthol treatments on photosystem II (PSII) activity and generation of ROS in different Symbiodinium types. In this study, we utilized five freshly isolated Symbiodinium types (S. minutum (B1), S. goreaui (C1), C3, C15, and S. trenchii (D1a)) to compare the effects of DCMU and menthol treatments. Symbiodinium cells were exposed to DCMU and menthol at different concentrations for 4 h. Results showed that values of the 50% inhibitory concentration (IC50) for PSII inhibition were 0.72∼1.96 mM for menthol-treated cells compared to 29∼74 pM for DCMU-treated cells. Diverse responses of Symbiodinium types were displayed in terms of PSII tolerance to menthol (S. minutum > S. trenchii = C15 > C3 = S. goreaui), and also in the response curves. In contrast, responses were not so diverse when the different types were treated with DCMU. Three of five menthol-treated Symbiodinium types showed instant and significant ROS generation when PSII activity was inhibited, compared to no ROS being generated in DCMU-treated Symbiodinium types. Both results indicated that menthol inhibited Symbiodinium PSII activity through Symbiodinium type-dependent mechanisms, which were also distinct from those with DCMU treatment. This study further confirmed that photosynthetic functions Symbiodinium have diverse responses to stress even within the same clade.

Symbiodinium spp. associated with scleractinian corals from Dongsha Atoll (Pratas), Taiwan, in the South China Sea.

Dongsha Atoll (also known as Pratas) in Taiwan is the northernmost atoll in the South China Sea and a designated marine national park since 2007. The marine park's scope of protection covers the bio-resources of its waters in addition to uplands, so it is important to have data logging information and analyses of marine flora and fauna, including their physiology, ecology, and genetics. As part of this effort, we investigated Symbiodinium associations in scleractinian corals from Dongsha Atoll through surveys carried out at two depth ranges (shallow, 1-5 m; and deep, 10-15 m) in 2009 and during a bleaching event in 2010. Symbiodinium composition was assessed using restriction fragment length polymorphism (RFLP) of 28S nuclear large subunit ribosomal DNA (nlsrDNA). Our results showed that the 796 coral samples from seven families and 20 genera collected in 2009 and 132 coral samples from seven families and 12 genera collected in 2010 were associated with Symbiodinium C, D and C+D. Occurrence of clade D in shallow water (24.5%) was higher compared to deep (14.9%). Due to a bleaching event in 2010, up to 80% of coral species associated with Symbiodinium C underwent moderate to severe bleaching. Using the fine resolution technique of denaturing gradient gel electrophoresis (DGGE) of internal transcribed spacer 2 (ITS2) in 175 randomly selected coral samples, from 2009 and 2010, eight Symbiodinium C types and two Symbiodinium D types were detected. This study is the first baseline survey on Symbiodinium associations in the corals of Dongsha Atoll in the South China Sea, and it shows the dominance of Symbiodinium clade C in the population.

Doors are closing on early development in corals facing climate change.

Marine invertebrates are particularly vulnerable to climatic anomalies in early life history stages because of the time spent in the water column. Studies have focused on the effect of seawater temperature on fertilization, development, and larval stages in corals; however, none of them show comparative results along an environmental gradient. In this study, we show that temperatures in the range of 15-33 °C have strong effects on fertilization rates and embryonic stages of two coral species, Acropora muricata in the subtropical environment and Acropora hyacinthus in subtropical and temperate environments. Deformations after the first cleavage stages were observed at low (15 °C) and high (33 °C) temperatures. Development was delayed by 6-7 h in the slightly non-optimal temperature of 20 °C. We found significant differences in fertilization rates and responses of embryos from different latitudes, with temperate corals being more sensitive to extremely hot temperatures and vice versa. We hypothesize that the coral development is restricted to a narrow temperature range and deviation outside this window could inhibit a species' continuance and ecological success. Thus, it would have significant negative effects on adult populations and communities, playing a role in future of coral reef survival.

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.

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.

Critical research needs for identifying future changes in Gulf coral reef ecosystems.

Expert opinion was assessed to identify current knowledge gaps in determining future changes in Arabian/Persian Gulf (thereafter 'Gulf') coral reefs. Thirty-one participants submitted 71 research questions that were peer-assessed in terms of scientific importance (i.e., filled a knowledge gap and was a research priority) and efficiency in resource use (i.e., was highly feasible and ecologically broad). Ten research questions, in six major research areas, were highly important for both understanding Gulf coral reef ecosystems and also an efficient use of limited research resources. These questions mirrored global evaluations of the importance of understanding and evaluating biodiversity, determining the potential impacts of climate change, the role of anthropogenic impacts in structuring coral reef communities, and economically evaluating coral reef communities. These questions provide guidance for future research on coral reef ecosystems within the Gulf, and enhance the potential for assessment and management of future changes in this globally significant region.