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Review

Thermal Stress and Resilience of Corals in a Climate-Changing World

by
Rodrigo Carballo-Bolaños
1,2,3,
Derek Soto
1,2,3 and
Chaolun Allen Chen
1,2,3,4,5,*
1
Biodiversity Program, Taiwan International Graduate Program, Academia Sinica and National Taiwan Normal University, Taipei 11529, Taiwan
2
Biodiversity Research Center, Academia Sinica, Taipei 11529, Taiwan
3
Department of Life Science, National Taiwan Normal University, Taipei 10610, Taiwan
4
Department of Life Science, Tunghai University, Taichung 40704, Taiwan
5
Institute of Oceanography, National Taiwan University, Taipei 10617, Taiwan
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2020, 8(1), 15; https://doi.org/10.3390/jmse8010015
Submission received: 5 December 2019 / Revised: 13 December 2019 / Accepted: 20 December 2019 / Published: 24 December 2019
(This article belongs to the Special Issue Coral Reef Resilience)
Browse Figure
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Abstract

:
Coral reef ecosystems are under the direct threat of increasing atmospheric greenhouse gases, which increase seawater temperatures in the oceans and lead to bleaching events. Global bleaching events are becoming more frequent and stronger, and understanding how corals can tolerate and survive high-temperature stress should be accorded paramount priority. Here, we review evidence of the different mechanisms that corals employ to mitigate thermal stress, which include association with thermally tolerant endosymbionts, acclimatisation, and adaptation processes. These differences highlight the physiological diversity and complexity of symbiotic organisms, such as scleractinian corals, where each species (coral host and microbial endosymbionts) responds differently to thermal stress. We conclude by offering some insights into the future of coral reefs and examining the strategies scientists are leveraging to ensure the survival of this valuable ecosystem. Without a reduction in greenhouse gas emissions and a divergence from our societal dependence on fossil fuels, natural mechanisms possessed by corals might be insufficient towards ensuring the ecological functioning of coral reef ecosystems.

1. Introduction

Since the last century, scleractinian coral reef ecosystems have undergone a decrease in biodiversity and ecological functioning [1,2,3,4,5], formerly attributed to the direct and indirect effects of overfishing [6,7], pollution from agriculture, sewage runoff, and land development [8,9,10]. Currently, along with the exponential increase of the human population [11] and our societal dependence on carbon fossil fuels, these local threats have been compounded by the impacts of global climate change in the oceans [12,13,14]. The impact of increasing greenhouse gases in the atmosphere is leading to a global increase in seawater temperatures that has caused mass bleaching events [12,14,15,16,17]. These global bleaching events are becoming more frequent (1998, 2010 and 2014–17) and severe [14,16,18,19,20,21,22], leaving coral reefs vulnerable and unable to recover. The 2014–2017 mass bleaching event, which lasted 36 months and spanned four calendar years, was the longest-lasting, most widespread, and probably most damaging event on record [21,22,23,24,25,26,27,28,29], and stands out as unique by spanning all phases of the El Niño-Southern Oscillation cycle of 2017, being the warmest non-El Niño year ever recorded [21,30].
Coral bleaching is defined as the loss of colour, due to the partial or total loss of Symbiodiniaceae dinoflagellates and/or the reduction of their photosynthetic pigments, that exposes the white calcium carbonate of the coral skeleton (Figure 1A) [31,32]. Bleaching is a generalized stress response to environmental perturbations such as aerial exposure, sedimentation, eutrophication, exposure to heavy metals, high UV radiation, and extreme changes in salinity and temperature [17,31,33,34], however, at large scales is triggered by high seawater temperatures (exceeding normal summer maxima) in combination with high solar radiation [12,15,17,31,32,33,35]. Scleractinian corals possess molecular protective mechanisms, such as heat shock proteins and antioxidant enzymes to resist thermal stress [17,33,36], or mycosporine amino acids (MAA) and fluorescent pigments to resist light stress (Figure 1B) [17,33,37,38]. The cellular mechanism of bleaching starts with the photoinhibition process within the photosynthetic apparatus of the endosymbionts, which results in the build-up of free electrons that react to form reactive oxygen species (ROS) [39,40]. The proliferation of harmful ROS leads to the degradation, exocytosis, or apoptosis of symbiont cells by the coral host [39], in order to avoid cellular damage [36]. If the duration of the thermal stress extends beyond their physiological ability to recover, corals cannot survive without their main symbiotic partners [15,31,35]. Even though the molecular process of bleaching is similar across coral species, variations in the mechanism to resist and survive thermal stress exist (Figure 1B,C) [17,32,35].
Resilience is the capacity of a coral colony or an entire coral reef ecosystem to absorb, resist, and recover from perturbations [41,42,43]. The resilience of corals to thermal stress is contingent on the mean long-term annual maximum temperature of the region they live in [17]. Much research has been done in the past decades to understand if the resilience of corals to thermal stress might be an adaptation and/or acclimatisation process (reviewed in [17,44,45]). Here, we review current research that focuses on the capabilities of coral species to adapt and/or acclimatise to thermal events, in order to understand what the future of this irreplaceable ecosystem will be. We have included only scientific studies which have clearly identified the different general strategies to survive thermal stress, as presented in this review.

2. Mechanisms of Resilience to Thermal Stress

2.1. Thermally Tolerant Endosymbionts

By associating with stress-resistant symbionts, some coral species are able to acquire increased thermal tolerance. Within the Symbiodiniaceae, species like Durusdinium spp. (previously clade D) [46,47,48], Cladocopium C15 [49], and C. thermophilum C3 [50,51] are resistant to thermal stress. Dinoflagellates in the genus Durusdinium are extremophiles inhabiting environments of thermal stress, high temperature fluctuations, sedimentation and high-latitudinal marginal reefs [52,53,54,55,56,57,58,59,60,61,62]. In recent decades, Durusdinium spp. have generated interest because they proliferate in bleached corals [53,60,63,64,65], protecting against thermal stress by providing 1–1.5 °C of thermal tolerance [46]. Durusdinium spp. maintain high photochemical efficiency when exposed to high temperatures compared to symbionts from other genera (Breviolum or Cladocopium) [48,66,67] and are able to fix more carbon and assimilate more nitrogen [68]. Furthermore, D. trenchii has been found to provide tolerance to cold stress too [69,70].
When exposed to thermal stress, some species of coral are capable of shifting the relative abundance of their dominant symbionts. Background symbionts, which can represent <10% of the overall Symbiodiniaceae community [60,71], become dominant, conferring thermal tolerance to the holobiont. Even though many coral species are able to associate with a heterogeneous community of Symbiodiniaceae [72,73], others do not change their dominant symbiont even when bleaching [74], showing a long-term symbiotic adaptation between coral host and dominant symbiont [75,76,77,78].

2.2. Acclimatisation (Phenotypic Plasticity)

Phenotypic plasticity refers to dissimilar phenotypes that can be generated from a single genotype in response to different environmental conditions [79]. These phenotypic changes are reversible and dependent on the boundaries of each organism’s genotype [17]. In this context, acclimatisation refers to the phenotypic changes of corals in their natural environment, while acclimation denotes short-term phenotypic changes under manipulative experimental conditions in the laboratory. Reciprocal transplantation experiments (RTE) are a well-known method to quantify acclimatisation mechanisms by measuring differences in physiological parameters in specimens transplanted across environmentally distinct sites, locations or regions. For example, a RTE of Porites lobata between a fore reef (impacted by high wave action, oceanic swells and storms) and back reef (sheltered) in American Samoa, showed phenotypic plasticity in mean annual skeletal extension rates, bulk densities, and calcification rates after only six months, with all variables in transplanted corals approximating values of corals originally from the site [80]. In another study, Sawall et al. [81] found optimal calcification rates at 28–29 °C throughout all populations of Pocillopora verrucosa with evident differences in temperature fluctuations between the northern (21–27 °C) and southern (28–33 °C) parts of the Red Sea, supporting high phenotypic plasticity due to low genetic divergence between north and south coral host populations.

2.3. Thermal Stress Acclimatisation

Multiple studies have identified a direct link between thermal preconditioning and bleaching susceptibility (Table 1) [82,83,84,85,86,87,88,89,90,91]. After exposing corals to short-term thermal preconditioning experiments, only preconditioned corals did not bleach during a heat-stress experiment (Table 1) [82,83], despite maintaining their Symbiodiniaceae and the bacterial community [82]. Moreover, other studies have compared coral responses of the first major mass bleaching event in 1998 with subsequent stronger bleaching events [89,91]. Maynard et al. [91] surveyed the same sites in 1998 and after a more severe bleaching event in 2002, which featured exposure to twice as many degree heating weeks (DHW) and 15% higher solar irradiance, corals acclimatised, and exhibited less bleaching than in 1998. In a similar study, Guest et al. [89] demonstrated how coral bleaching was less severe after the 2010 large-scale bleaching event in Southeast Asia in locations that previously showed high bleaching in 1998 (Singapore and Malaysia), and had greater historical temperature variability and lower rates of warming. Meanwhile, corals in Indonesia were unaffected by bleaching in 1998, but showed high mortality in 2010. Consequently, corals acclimatised to previous thermal stress events, but also those living in sites with highly variable temperatures presented higher tolerance [89].
Brown et al. [90] demonstrated ‘long-term environmental memory’ during the bleaching event in 2010. In 2000, coral colonies were rotated 180° in a manipulative experiment [96]. During the bleaching event of 2010, the sides of colonies exposed to high solar radiation before rotation in the 2000 experiment, retained four times as many symbionts than the sides exposed to low solar radiation, despite experiencing higher radiation for 10 years [90]. These experiments provide evidence that long-term acclimatisation to local conditions enhances thermal tolerance during bleaching events (Table 1). Coles et al. [87] showed evidence of acclimatisation to increasing seawater temperatures by replicating a bleaching experiment from 1970 at the same location in 2010. Because sea-surface temperature (SST) has steadily increased 1.13 °C over the last four decades, the authors experimentally increased 2.2 °C of ambient temperatures. Corals in 2017 showed higher calcification rates, delayed bleaching, and mortality compared to corals in 1970 (Table 1) [87]. Unfortunately, despite increased temperature tolerance in local corals, Hawaii suffered high coral mortality (34%) during the 2014–2017 global bleaching event, showing that high-temperature acclimatisation processes may not be occurring quickly enough to mitigate the projected length and intensity of future bleaching events [87].

2.4. Acclimatisation to High Temperature Variability

A series of backreef pools exhibiting tidal temperature variability on the island of Ofu, American Samoa, present a unique environment to study physiological differences between conspecific corals at small-spatial scales [97]. Using genetically identical coral fragments in a heat-stress experiment from both pools, Oliver and Palumbi [67] provided evidence of increased thermal tolerance when corals have acclimatised to high temperature variability (Table 1). Corals from the highly variable (HV) pool showed lower mortality and higher photochemical efficiency, while those from the moderately variable (MV) pool suffered increased mortality and lower photochemical efficiency related to symbiont species. Corals associated with Durusdinium spp. exhibited an intermediate decline in photochemical efficiency, while those associated with Cladocopium spp. showed the highest decline [67]. Palumbi et al. [92] performed reciprocal transplantations of corals between HV and MV pools and subjected those corals to a heat stress experiment to test for acclimatisation responses to thermal stress (Table 1). Corals acquired heat sensitivity based on the pool they were transplanted to: MV pool corals acquired heat resistance when moved to HV pool, but not to the same extent of HV conspecifics, while HV to MV transplantees experienced reduced chlorophyll a retention, similar to the levels of native corals [92]. Mayfield et al. [93] performed a thermal stress experiment with corals from a site in Taiwan exhibiting high daily temperature fluctuations and found that, under HV conditions, physiological parameters behaved similarly to those in control corals, suggesting that individuals living under HV temperatures can acclimate to high temperatures that would cause bleaching and mortality in unacclimated corals from other regions (Table 1) [93].
Some studies have compiled data of past bleaching events, in an effort to link patterns of bleaching susceptibility within sites under high temperature variability, in a worldwide context [94,95]. Sites characterized by a high-frequency pattern of temperature variability experienced higher thermal stress during both bleaching events, with extensive bleaching reported during 1998. However, in 2005–2006, these sites experienced reduced bleaching compared to sites under low frequency patterns, due to the acclimatisation of corals to thermal stress after the 1998 bleaching event and selective adaptation of resilient corals that survived the bleaching event [94]. Safaie et al. [95] explored this concept further by collecting in situ data with remotely sensed datasets from different reef locations around the globe, along with spatiotemporally coincident quantitative coral bleaching observations. Corals regularly exposed to temperature fluctuations on daily or tidal timescales became acclimatised to thermal stress and resistant to bleaching events. More importantly, these patterns of high-frequency temperature variability to bleaching occur in many reefs worldwide [95].

2.5. Molecular Mechanisms for Acclimatisation

Most studies involving transcriptomic analyses and thermal stress have shown differential gene expression under high temperature stress compared to controls (Table 2) [98,99,100,101,102,103]. Corals exposed to experimental thermal stress presented an upregulation of genes involved in oxidative stress responses [98,99] and carbon metabolism [98]. A comparison of differences in gene expression in corals preconditioned to thermal stress showed seventy differentially expressed genes between non-preconditioned corals and controls, 42 between preconditioned corals and controls, and nine genes between non-preconditioned and preconditioned corals (Table 2) [102].
To understand the genomic basis of thermal resilience in corals, Barshis et al. [103] compared transcriptome-wide gene expression among thermally resilient and thermally sensitive conspecifics (Table 2). Sixty genes were up-regulated in thermally sensitive corals, while resilient corals already presented up-regulated genes under ambient conditions. These “frontloaded” genes facilitate a faster reaction to thermal stress at the protein level [103]. In a similar study, using reciprocally transplanted corals from HV and MV pools, transcriptome-wide gene expression analyses showed differential expression in 74 genes related to heat acclimation between genetically identical corals from both pools (Table 2) [93]. In a related study performed at the same sites, Ruiz-Jones and Palumbi [104] monitored the transcriptomic response of corals in the HV pool with a strong tidal cycle (high temperatures over 17 days). Their results bolstered the conclusions of Barshis et al. [103], showing that genes up-regulated during the hottest days, were enriched for “unfolded protein response”, an ancient eukaryotic cellular response to endoplasmic reticulum stress, which corals use as the first line of defence against thermal stress [104].

2.6. Adaptation

Adaptation, strictly defined, refers to changes in the genetic composition of a population that are passed onto the next generation through natural selection [17,44,105]. The major concern regarding global climate change is that the current rate of environmental changes will outpace the evolutionary capabilities of corals to adapt [12,14,16,19,106]. Recent evidence has shown that, in addition to phenotypic plasticity and acclimatisation, other adaptive responses in corals, such as trans-generational plasticity [107], epigenetics [108,109], and somatic mutations [110] might contribute to resilience under thermal stress. Moreover, the fast rate of asexual reproduction within the Symbiodiniaceae (days to weeks in hospite) [111] in combination with large population sizes within corals (~1–5 × 106 cells cm−2) [112] provide the potential for mutations to develop that might enable corals to resist thermal stress [110].
Few studies have examined adaptation to local thermal history in Symbiodiniaceae dinoflagellates [113,114]. Howells et al. [113] demonstrated adaptive capacity in the symbiont C. goreaui (formerly type C1) in corals from two sites in the GBR with dissimilar thermal histories. Corals hosting C. goreaui from the cooler site presented photodamage and bleaching, while those from the hotter site exhibited no signs of stress and greater growth [113]. Chakravarti et al. [114] tested adaptation to thermal tolerance of C. goreaui through experimental evolution. Dinoflagellates were cultured in vitro at elevated temperature of 31 °C for ~80 generations (2.5 y), while wild-types were reared at 27 °C ambient temperature, then both cultures were tested at both temperatures. To measure physiological responses in hospite, both types (thermally selected and wild types) were inoculated into aposymbiotic recruits of three coral species and were exposed to both temperatures similar to in vitro experiments [114]. Symbionts reared in vitro performed better in photophysiology and growth at both temperatures, and showed lower levels of extracellular ROS. In contrast, wild-type symbionts were unable to photosynthesise or grow at high temperatures, and produced 17 times more extracellular ROS [114]. The differences were less obvious in hospite than in vitro. Cultures of corals inoculated with the thermally tolerant symbionts showed no difference in growth between 27 and 31 °C, while those inoculated with wild-types showed a negative growth trend at 31 °C, confirming an adaptation to thermal stress in C. goreaui after many generations living under high temperature [114].
Dixon et al. [115] revealed genetic data from the coral host that forms the heritable basis of temperature tolerance by performing a cross-fertilization experiment with coral colonies from two thermally divergent locations in GBR. The authors measured heat tolerance using the survivorship rate of larvae exposed to high temperatures and found that parents from the warmer location conferred significantly higher thermo-tolerance to their offspring, up to 10 fold increase in odds of survival, in comparison to parents from the cooler location. Dixon et al. [115] also identified “tolerance-associated genes” (TAGs), whose expression before stress predicted high survivorship rates in larvae under thermal stress, dissimilar from frontloaded genes [103]. When TAG expression was compared with parental colonies after three days of heat stress, they were negatively correlated with long-term heat stress response similar to the larval response, indicating that the larval heat tolerance results from the absence of pre-existing stress and not from prior up-regulation of heat stress genes through frontloading [115].
Krueger et al. [116] presented evidence that Stylophora pistillata underwent selection for heat tolerance in the Red Sea, after spending 47 days at 1–2 °C above their long-term summer maximum and showed an increase in primary productivity. Fine et al. [117] demonstrated how different corals species showed no signs of stress after exposure to 33 °C for four weeks and proposed that corals that colonised the Gulf of Aqaba after the last ice age had to cross exceedingly warm waters (>32 °C in the summer) at the entrance of the Red Sea, maintaining this adaptation to heat tolerance until the present day.

2.7. Heterotrophy

Heterotrophic carbon can become a significant energy source for some coral species when phototrophic carbon is unavailable, such as during a bleaching event (Table 1) [118]. Some studies have shown how heterotrophy replenished energy reserves in corals exposed to high temperatures [119] and during the recovery phase [120]. Similarly, Borell and Bischof [121] showed higher photochemical efficiency in fed corals compared to unfed corals after a mild thermal stress experiment. Also, Borell et al. [122] demonstrated how heterotrophy sustained photosynthetic activity and energy reserves in thermally stressed corals.
In a study which developed an energy-budget model linking coral bleaching and mortality risk, authors concluded that the time between the start of severe bleaching and the beginning of mortality is influenced by the amount of lipid stores corals have before the bleaching event and their capacity to acquire energy through heterotrophy [123]. With a stable isotope 13C pulse-chase labelling experiment, Hughes et al. [124] demonstrated that, after exposure to high temperatures, coral hosts incorporated heterotrophic labelled carbon for storage and to stimulate endosymbiont recovery. Even after recovery from bleaching, 75% of carbon in newly acquired lipids was sourced heterotrophically [125], and corals continued assimilating heterotrophic carbon for up to 11 months after the bleaching experiment [126].
Nonetheless, the capacity for heterotrophic plasticity is compromised after two consecutive bleaching events [127]. Researchers experimentally bleached corals for 2.5 weeks, transferred corals to the field for recovery, and then repeated the bleaching experiment after one year. After the first thermal stress experiment, zooplankton and dissolved organic carbon (DOC) allowed the metabolic demand of bleached corals to be met; however, neither form of heterotrophic carbon was able to contribute to the energy budget of both species after the second bleaching experiment, suggesting that the capacity for heterotrophic plasticity is compromised under annual bleaching events [127] and corals need to depend on their energy reserves and/or symbiont association to survive repeated bleaching [128].

3. Perspectives for the Future

Because the loss of corals around the world would be a devastating consequence of human influence on earth, strategies to mitigate the damage and improve coral’s thermal tolerance are currently being taken into consideration. For example, assisted colonization, migration and/or gene flow contemplate the movement of colonies or larvae of the same species living at different latitudes. ‘Warm-adapted’ corals can be transplanted to high latitude areas, where conspecifics living in colder environments, are vulnerable to thermal stress [129,130,131]. Assisted evolution has the potential to increase thermal stress tolerance in corals through various approaches: preconditioning acclimatisation (see Section: ‘Thermal stress acclimatisation’) and trans-generational acclimatisation, changes in microbial communities [132], selective breeding [133], mutagenesis [134], and the use of “CRISPR/Cas9” genome editing technology [135]. The use of ‘strong corals’ naturally adapted to high temperature extremes, such as corals originating from the Persian Gulf or Red Sea, as possible seedlings to repopulate areas where corals have disappeared [117,136,137,138] is also being considered. Unfortunately, none of these measures seem to be able to keep pace with the current rate of climate change, with the time between recurrent bleaching events becoming increasingly too short to allow complete recovery of coral reef ecosystems [139]. Despite recent advances in research methods and technology, such as transcriptomics [140], financial and logistical limitations to implement these actions remain [141], especially at large scales [130], and it takes many years to safely deploy new technology after social and political scrutiny [142].
Other conservation measures under consideration include designing better marine protected areas (MPAs) [143] or networks of MPAs [144,145,146], taking into consideration larval dispersal, connectivity and distribution patterns in areas with thermally tolerant corals [147] and including ‘refugia’ in areas where coral reefs have proven to be resilient to climate change [21,43,148,149]. This might help avoid the “protection paradox” in MPAs, in which vulnerable species are protected from local pressures, like fishing; yet while these species recover, they might be more sensitive to global pressures, like bleaching events [144]. Nevertheless, well-protected reefs within MPAs are not shielded from thermal stress [150,151]. After the last bleaching event, this was confirmed for MPAs [152], and for remote and isolated reefs with almost no direct human pressures [23,24,27,153,154,155].
The integration of assisted evolution [131,134] into coral reef restoration programs [156,157] to increase the resilience of already degraded ecosystems [41] is one strategy that has proven to be successful. Morikawa and Palumbi [158] used naturally thermal-tolerant corals from American Samoa to show that resilient corals can survive multiple bleaching events, providing the first proof that ecosystem engineering for conservation might be a resilience restoration tool of great importance in our climate changed future [158].
Evidence from reciprocally transplanted coral clones between sites with different thermal histories shows how individual coral colonies can shift their thermal threshold and thermal tolerance [93,159,160]. It is clear that many coral species are acclimatising and adapting to rapid changes in climate and their mechanisms differ among species and localities [67,82,83,89,90,113,115,161]. However, under current greenhouse gas emission projections, coral reefs worldwide are likely to change into new configurations with new assemblages of species [19,149,162,163,164,165]. These changes are happening fast, the GBR being the best example. After the 2014–2017 mass bleaching event, even the most ‘pristine’ areas in the northern GBR saw high mortality regardless of reefs’ individual management status, proving that current management toolsets are insufficient to protect coral reef ecosystems from climate change [20,152]. The Paris Agreement was a first step to tackle the climate crisis, but no major industrialized country is meeting its pledges to control and reduce their greenhouse gas emissions [166]. It is imperative that societies completely change our dependence on fossil fuels, therefore addressing the root causes of climate change.

Author Contributions

Conceptualization, R.C.-B. and C.A.C.; methodology, R.C.-B.; software, R.C.-B.; validation, R.C.-B. and D.S.; formal analysis, R.C.-B.; investigation, R.C.-B.; resources, C.A.C.; data curation, R.C.-B.; writing—original draft preparation, R.C.-B. and D.S.; writing—review and editing, R.C.-B., D.S. and C.A.C.; visualization, R.C.-B.; supervision, C.A.C.; project administration, C.A.C.; funding acquisition, C.A.C. All authors have read and agreed to the published version of the manuscript

Funding

This research was funded by Academia Sinica for Life Science Research (no. 4010) and Ministry of Science and Technology, Taiwan (MOST 101-2621-B-001-005-MY3) to C.A.C.

Acknowledgments

Many thanks to LK Chou and D Huang for their invitation to contribute to the special issue of “Coral Reef Resilience”. We also thank three anonymous reviewers for helping improve this manuscript. R.C.-B. and D.S. are the receipts of PhD fellowship from Taiwan International Graduate Program (TIGP)-Biodiversity in the Academia Sinica. This review is supported by funds from Academia Sinica and Ministry of Science and Technology, Taiwan to C.A.C.

Conflicts of Interest

The authors declare no conflict of interest and the funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

References

  1. Wilkinson, C. Status of Coral Reefs of the World: 2000; Australian Institute of Marine Science: Townsville, Australia, 2000.
  2. Gardner, T.A.; Côté, I.M.; Gill, J.A.; Grant, A.; Watkinson, A.R. Long-term region-wide declines in Caribbean corals. Science 2003, 301, 958–960. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Pandolfi, J.M.; Bradbury, R.H.; Sala, E.; Hughes, T.P.; Bjorndal, K.A.; Cooke, R.G.; McArdle, D.; McClenachan, L.; Newman, M.J.H.; Paredes, G.; et al. Global trajectories of the long-term decline of coral reef ecosystems. Science 2003, 301, 955–958. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. De’ath, G.; Fabricius, K.E.; Sweatman, H.; Puotinen, M. The 27–year decline of coral cover on the Great Barrier Reef and its causes. Proc. Natl. Acad. Sci. USA 2012, 109, 17995–17999. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  5. Bruno, J.F.; Selig, E.R. Regional decline of coral cover in the Indo-Pacific: Timing, extent, and subregional comparisons. PLoS ONE 2007, 2, e711. [Google Scholar] [CrossRef] [Green Version]
  6. Jackson, J.B.; Kirby, M.X.; Berger, W.H.; Bjorndal, K.A.; Botsford, L.W.; Bourque, B.J.; Bradbury, R.H.; Cooke, R.; Erlandson, J.; Estes, J.A.; et al. Historical overfishing and the recent collapse of coastal ecosystems. Science 2001, 293, 629–637. [Google Scholar] [CrossRef] [Green Version]
  7. Valentine, J.F.; Heck, K.L. Perspective review of the impacts of overfishing on coral reef food web linkages. Coral Reefs 2005, 24, 209–213. [Google Scholar] [CrossRef]
  8. Dubinsky, Z.; Stambler, N. Marine pollution and coral reefs. Glob. Chang. Biol. 1996, 2, 511–526. [Google Scholar] [CrossRef]
  9. McCulloch, M.; Fallon, S.; Wyndham, T.; Hendy, E.; Lough, J.; Barnes, D. Coral record of increased sediment flux to the inner Great Barrier Reef since European settlement. Nature 2003, 421, 727. [Google Scholar] [CrossRef]
  10. Fabricius, K.E. Effects of terrestrial runoff on the ecology of corals and coral reefs: Review and synthesis. Mar. Pollut. Bull. 2005, 50, 125–146. [Google Scholar] [CrossRef]
  11. Cohen, J.E. Population growth and earth’s human carrying capacity. Science 1995, 269, 341–346. [Google Scholar] [CrossRef] [Green Version]
  12. Hughes, T.P.; Baird, A.H.; Bellwood, D.R.; Card, M.; Connolly, S.R.; Folke, C.; Grosberg, R.; Hoegh-Guldberg, O.; Jackson, J.B.C.; Kleypas, J.; et al. Climate change, human impacts, and the resilience of coral reefs. Science 2003, 301, 929–933. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. D’Angelo, C.; Wiedenmann, J. Impacts of nutrient enrichment on coral reefs: New perspectives and implications for coastal management and reef survival. Curr. Opin. Environ. Sustain. 2014, 7, 82–93. [Google Scholar] [CrossRef] [Green Version]
  14. Hoegh-Guldberg, O.; Mumby, P.J.; Hooten, A.J.; Steneck, R.S.; Greenfield, P.; Gomez, E.; Harvell, C.D.; Sale, P.F.; Edwards, A.J.; Caldeira, K.; et al. Coral reefs under rapid climate change and ocean acidification. Science 2007, 318, 1737–1742. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Fitt, W.K.; Brown, B.E.; Warner, M.E.; Dunne, R.P. Coral bleaching: Interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 2001, 20, 51–65. [Google Scholar] [CrossRef]
  16. Hoegh-Guldberg, O. Climate change, coral bleaching and the future of the world’s coral reefs. Mar. Freshw. Res. 1999, 50, 839–866. [Google Scholar] [CrossRef] [Green Version]
  17. Coles, S.L.; Brown, B.E. Coral bleaching—Capacity for acclimatization and adaptation. Adv. Mar. Biol. 2003, 46, 183–223. [Google Scholar] [CrossRef]
  18. Heron, S.F.; Maynard, J.A.; Van Hooidonk, R.; Eakin, C.M. Warming trends and bleaching stress of the world’s coral reefs 1985–2012. Sci. Rep. 2016, 6, 38402. [Google Scholar] [CrossRef] [Green Version]
  19. Hughes, T.P.; Barnes, M.L.; Bellwood, D.R.; Cinner, J.E.; Cumming, G.S.; Jackson, J.B.; Kleypas, J.; van der Leemput, I.A.; Lough, J.M.; Morrison, T.H.; et al. Coral reefs in the Anthropocene. Nature 2017, 546, 82. [Google Scholar] [CrossRef]
  20. Hughes, T.P.; Kerry, J.T.; Álvarez-Noriega, M.; Álvarez-Romero, J.G.; Anderson, K.D.; Baird, A.H.; Babcock, R.C.; Beger, M.; Bellwood, D.R.; Berkelmans, R.; et al. Global warming and recurrent mass bleaching of corals. Nature 2017, 543, 373–377. [Google Scholar] [CrossRef]
  21. Eakin, C.M.; Sweatman, H.P.A.; Brainard, R.E. The 2014–2017 global-scale coral bleaching event: Insights and impacts. Coral Reefs 2019, 38, 539–545. [Google Scholar] [CrossRef] [Green Version]
  22. Skirving, W.J.; Heron, S.F.; Marsh, B.L.; Liu, G.; De La Cour, J.L.; Geiger, E.F.; Eakin, C.M. The relentless march of mass coral bleaching: A global perspective of changing heat stress. Coral Reefs 2019, 38, 547–557. [Google Scholar] [CrossRef] [Green Version]
  23. Harrison, H.B.; Álvarez-Noriega, M.; Baird, A.H.; Heron, S.F.; MacDonald, C.; Hughes, T.P. Back-to-back coral bleaching events on isolated atolls in the Coral Sea. Coral Reefs 2019, 38, 713–719. [Google Scholar] [CrossRef]
  24. Head, C.E.I.; Bayley, D.T.I.; Rowlands, G.; Roche, R.C.; Tickler, D.M.; Rogers, A.D.; Koldewey, H.; Turner, J.R.; Andradi-Brown, D.A. Coral bleaching impacts from back-to-back 2015–2016 thermal anomalies in the remote central Indian Ocean. Coral Reefs 2019, 38, 605–618. [Google Scholar] [CrossRef] [Green Version]
  25. Raymundo, L.J.; Burdick, D.; Hoot, W.C.; Miller, R.M.; Brown, V.; Reynolds, T.; Gault, J.; Idechong, J.; Fifer, J.; Williams, A. Successive bleaching events cause mass coral mortality in Guam, Micronesia. Coral Reefs 2019, 38, 677–700. [Google Scholar] [CrossRef]
  26. Burt, J.A.; Paparella, F.; Al-Mansoori, N.; Al-Mansoori, A.; Al-Jailani, H. Causes and consequences of the 2017 coral bleaching event in the southern Persian/Arabian Gulf. Coral Reefs 2019, 38, 567–589. [Google Scholar] [CrossRef]
  27. Vargas-Ángel, B.; Huntington, B.; Brainard, R.E.; Venegas, R.; Oliver, T.; Barkley, H.; Cohen, A. El Niño-associated catastrophic coral mortality at Jarvis Island, central Equatorial Pacific. Coral Reefs 2019, 38, 731–741. [Google Scholar] [CrossRef]
  28. Frade, P.R.; Bongaerts, P.; Englebert, N.; Rogers, A.; Gonzalez-Rivero, M.; Hoegh-Guldberg, O. Deep reefs of the Great Barrier Reef offer limited thermal refuge during mass coral bleaching. Nat. Commun. 2018, 9, 3447. [Google Scholar] [CrossRef] [Green Version]
  29. Ku’ulei, S.R.; Bahr, K.D.; Jokiel, P.L.; Donà, A.R. Patterns of bleaching and mortality following widespread warming events in 2014 and 2015 at the Hanauma Bay Nature Preserve, Hawaii. Peer J. 2017, 5, e3355. [Google Scholar]
  30. Hartfield, G.; Blunden, J.; Arndt, D.S. State of the climate in 2017. Bull. Am. Meteorol. Soc. 2018, 99, S1–S310. [Google Scholar] [CrossRef]
  31. Glynn, P. Coral reef bleaching: Ecological perspectives. Coral Reefs 1993, 12, 1–17. [Google Scholar] [CrossRef]
  32. Douglas, A.E. Coral bleaching—how and why? Mar. Pollut. Bull. 2003, 46, 385–392. [Google Scholar] [CrossRef]
  33. Brown, B.E. Coral bleaching: Causes and consequences. Coral Reefs 1997, 16, S129–S138. [Google Scholar] [CrossRef]
  34. Obura, D.O. Reef corals bleach to resist stress. Mar. Pollut. Bull. 2009, 58, 206–212. [Google Scholar] [CrossRef] [PubMed]
  35. Jokiel, P.L. Temperature stress and coral bleaching. In Coral Health and Disease; Springer: Berlin, Germany, 2004; pp. 401–425. [Google Scholar]
  36. Lesser, M.P. Oxidative stress in marine environments: Biochemistry and physiological ecology. Annu. Rev. Physiol. 2006, 68, 253–278. [Google Scholar] [CrossRef] [Green Version]
  37. Shick, J.M.; Dunlap, W.C. Mycosporine-like amino acids and related gadusols: Biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annu. Rev. Physiol. 2002, 64, 223–262. [Google Scholar] [CrossRef] [Green Version]
  38. Salih, A.; Larkum, A.; Cox, G.; Kühl, M.; Hoegh-Guldberg, O. Fluorescent pigments in corals are photoprotective. Nature 2000, 408, 850–853. [Google Scholar] [CrossRef]
  39. Weis, V.M. Cellular mechanisms of cnidarian bleaching: Stress causes the collapse of symbiosis. J. Exp. Biol. 2008, 211, 3059–3066. [Google Scholar] [CrossRef] [Green Version]
  40. Tchernov, D.; Gorbunov, M.Y.; de Vargas, C.; Yadav, S.N.; Milligan, A.J.; Häggblom, M.; Falkowski, P.G. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc. Natl. Acad. Sci. USA 2004, 101, 13521–13535. [Google Scholar] [CrossRef] [Green Version]
  41. Darling, E.S.; Côté, I.M. Seeking resilience in marine ecosystems. Science 2018, 359, 986–987. [Google Scholar] [CrossRef]
  42. Bellwood, D.R.; Hughes, T.P.; Folke, C.; Nyström, M. Confronting the coral reef crisis. Nature 2004, 429, 827–833. [Google Scholar] [CrossRef]
  43. Roche, R.C.; Williams, G.J.; Turner, J.R. Towards developing a mechanistic understanding of coral reef resilience to thermal stress across multiple scales. Curr. Clim. Chang. Rep. 2018, 4, 51–64. [Google Scholar] [CrossRef] [Green Version]
  44. Edmunds, P.J.; Gates, R.D. Acclimatization in tropical reef corals. Mar. Ecol. Prog. Ser. 2008, 361, 307–310. [Google Scholar] [CrossRef]
  45. Brown, B.E.; Cossins, A.R. The potential for temperature acclimatisation of reef corals in the face of climate change. In Coral Reefs: An Ecosystem in Transition; Springer: Berlin, Germany, 2011; pp. 421–433. [Google Scholar]
  46. Berkelmans, R.; van Oppen, M.J.H. The role of zooxanthellae in the thermal tolerance of corals: A ‘nugget of hope’ for coral reefs in an era of climate change. Proc. R. Soc. B Biol. Sci. 2006, 273, 2305–2312. [Google Scholar] [CrossRef] [PubMed]
  47. Stat, M.; Gates, R.D. Clade D Symbiodinium in scleractinian corals: A “nugget” of hope, a selfish opportunist, an ominous sign, or all of the above? J. Mar. Biol. 2011, 2011. [Google Scholar] [CrossRef] [Green Version]
  48. Rowan, R. Thermal adaptation in reef coral symbionts. Nature 2004, 430, 742. [Google Scholar] [CrossRef] [PubMed]
  49. Levas, S.J.; Grottoli, A.G.; Hughes, A.; Osburn, C.L.; Matsui, Y. Physiological and biogeochemical traits of bleaching and recovery in the mounding species of coral Porites lobata: Implications for resilience in mounding corals. PLoS ONE 2013, 8, e63267. [Google Scholar] [CrossRef] [Green Version]
  50. Hume, B.C.C.; Voolstra, C.R.; Arif, C.; D’Angelo, C.; Burt, J.A.; Eyal, G.; Loya, J.; Wiedenmann, J. Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change. Proc. Natl. Acad. Sci. USA 2016, 113, 4416–4421. [Google Scholar] [CrossRef] [Green Version]
  51. Hume, B.C.; D’Angelo, C.; Smith, E.G.; Stevens, J.R.; Burt, J.; Wiedenmann, J. Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world’s hottest sea, the Persian/Arabian Gulf. Sci. Rep. 2015, 5, 8562. [Google Scholar] [CrossRef] [Green Version]
  52. Chen, C.A.; Wang, J.-T.; Fang, L.-S.; Yang, Y.-W. Fluctuating algal symbiont communities in Acropora palifera (Scleractinia: Acroporidae) in Taiwan. Mar. Ecol. Prog. Ser. 2005, 295, 113–121. [Google Scholar] [CrossRef]
  53. Hsu, C.-M.; Keshavmurthy, S.; Dennis, V.; Kuo, C.-Y.; Wang, J.-T.; Meng, P.-J.; Chen, C.A. Temporal and spatial variations of symbiont communities in catch bowl coral, Isopora palifera (Scleractinia; Acroporidae), at reefs in Kenting National Park, Taiwan. Zool. Stud. 2012, 51, 1343–1353. [Google Scholar]
  54. LaJeunesse, T.C.; Pettay, D.T.; Sampayo, E.M.; Phongsuwan, N.; Brown, B.; Obura, D.O.; Hoegh-Guldberg, O.; Fitt, W.K. Long-standing environmental conditions, geographic isolation and host-symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J. Biogeogr. 2010, 37, 785–800. [Google Scholar] [CrossRef]
  55. Lien, Y.-T.; Nakano, Y.; Plathong, S.; Fukami, H.; Wang, J.-T.; Chen, C.A. Occurrence of the putatively heat-tolerant Symbiodinium phylotype D in high-latitudinal outlying coral communities. Coral Reefs 2007, 26, 35–44. [Google Scholar] [CrossRef]
  56. Wham, D.C.; Ning, G.; LaJeunesse, T.C. Symbiodinium glynnii sp. nov., a species of stress-tolerant symbiotic dinoflagellates from pocilloporid and montiporid corals in the Pacific Ocean. Phycologia 2017, 56, 396–409. [Google Scholar] [CrossRef]
  57. LaJeunesse, T.C.; Parkinson, J.E.; Gabrielson, P.W.; Jeong, H.J.; Reimer, J.D.; Voolstra, C.R.; Santos, S.R. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 2018, 28, 2570–2580. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  58. Carballo-Bolaños, R.; Denis, V.; Huang, Y.-Y.; Keshavmurthy, S.; Chen, C.A. Temporal variation and photochemical efficiency of species in Symbiodiniaceae associated with coral Leptoria phrygia (Scleractinia; Merulinidae) exposed to contrasting temperature regimes. PLoS ONE 2019, 14, e0218801. [Google Scholar] [CrossRef] [PubMed]
  59. Chen, C.A.; Lam, K.K.; Nakano, Y.; Tsai, W.-S. A stable association of the stress-tolerant zooxanthellae, Symbiodinium clade D, with the low-temperature-tolerant coral, Oulastrea crispata (Scleractinia: Faviidae) in subtropical non-reefal coral communities. Zool. Stud. 2003, 42, 540–550. [Google Scholar]
  60. Kao, K.-W.; Keshavmurthy, S.; Tsao, C.-H.; Wang, J.-T.; Chen, C.A. Repeated and prolonged temperature anomalies negate Symbiodiniaceae genera shuffling in the coral Platygyra verweyi (Scleractinia; Merulinidae). Zool. Stud. 2018, 57, 1–14. [Google Scholar]
  61. Keshavmurthy, S.; Hsu, C.-M.; Kuo, C.-Y.; Meng, P.-J.; Wang, J.-T.; Chen, C.A. Symbiont communities and host genetic structure of the brain coral Platygyra verweyi, at the outlet of a nuclear power plant and adjacent areas. Mol. Ecol. 2012, 21, 4393–4407. [Google Scholar] [CrossRef]
  62. Keshavmurthy, S.; Meng, P.-J.; Wang, J.-T.; Kuo, C.-Y.; Yang, S.-Y.; Hsu, C.-M.; Gan, C.-H.; Dai, C.-F.; Chen, C.A. Can resistant coral-Symbiodinium associations enable coral communities to survive climate change? A study of a site exposed to long-term hot water input. Peer J. 2014, 2, e327. [Google Scholar] [CrossRef] [Green Version]
  63. Lajeunesse, T.C.; Smith, R.T.; Finney, J.; Oxenford, H. Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral ‘bleaching’ event. Proc. R. Soc. B Biol. Sci. 2009, 276, 4139–4148. [Google Scholar] [CrossRef]
  64. Silverstein, R.N.; Cunning, R.; Baker, A.C. Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Glob. Chang. Biol. 2015, 21, 236–249. [Google Scholar] [CrossRef] [PubMed]
  65. Jones, A.M.; Berkelmans, R.; van Oppen, M.J.H.; Mieog, J.C.; Sinclair, W. A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: Field evidence of acclimatization. Proc. R. Soc. B Biol. Sci. 2008, 275, 1359–1365. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  66. Cunning, R.; Silverstein, R.N.; Baker, A.C. Symbiont shuffling linked to differential photochemical dynamics of Symbiodinium in three Caribbean reef corals. Coral Reefs 2017, 1–8. [Google Scholar] [CrossRef]
  67. Oliver, T.A.; Palumbi, S.R. Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 2011, 30, 429–440. [Google Scholar] [CrossRef]
  68. Baker, D.M.; Andras, J.P.; Jordán-Garza, A.G.; Fogel, M.L. Nitrate competition in a coral symbiosis varies with temperature among Symbiodinium clades. ISME J. 2013, 7, 1248–1251. [Google Scholar] [CrossRef]
  69. Silverstein, R.N.; Cunning, R.; Baker, A.C. Tenacious D: Symbiodinium in clade D remain in reef corals at both high and low temperature extremes despite impairment. J. Exp. Biol. 2017, 220, 1192–1196. [Google Scholar] [CrossRef] [Green Version]
  70. LaJeunesse, T.C.; Smith, R.; Walther, M.; Pinzón, J.; Pettay, D.T.; McGinley, M.; Aschaffenburg, M.; Medina-Rosas, P.; Cupul-Magaña, A.L.; López Pérez, A.; et al. Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance. Proc. R. Soc. B Biol. Sci. 2010, 277, 2925–2934. [Google Scholar] [CrossRef] [Green Version]
  71. Mieog, J.C.; van Oppen, M.J.; Cantin, N.E.; Stam, W.T.; Olsen, J.L. Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across the Great Barrier Reef: Implications for symbiont shuffling. Coral Reefs 2007, 26, 449–457. [Google Scholar] [CrossRef] [Green Version]
  72. Silverstein, R.N.; Correa, A.M.S.; Baker, A.C. Specificity is rarely absolute in coral−algal symbiosis: Implications for coral response to climate change. Proc. R. Soc. B Biol. Sci. 2012, 279, 2609–2618. [Google Scholar] [CrossRef] [Green Version]
  73. Baker, A.C. Flexibility and specificity in coral-agal symbiosis: Diversity, ecology, and biogeogrpahy of Symbiodinium. Annu. Rev. Ecol. Evol. Syst. 2003, 34, 661–689. [Google Scholar] [CrossRef] [Green Version]
  74. Goulet, T.L. Most corals may not change their symbionts. Mar. Ecol. Prog. Ser. 2006, 321, 1–7. [Google Scholar] [CrossRef] [Green Version]
  75. Thornhill, D.J.; Xiang, Y.; Fitt, W.K.; Santos, S.R. Reef endemism, host specificity and temporal stability in populations of symbiotic dinoflagellates from two ecologically dominant Caribbean corals. PLoS ONE 2009, 4, e6262. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  76. Stat, M.; Loh, W.K.W.; LaJeunesse, T.C.; Hoegh-Guldberg, O.; Carter, D.A. Stability of coral-endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef. Coral Reefs 2009, 28, 709–713. [Google Scholar] [CrossRef]
  77. Thornhill, D.J.; Fitt, W.K.; Schmidt, G.W. Highly stable symbioses among western Atlantic brooding corals. Coral Reefs 2006, 25, 515–519. [Google Scholar] [CrossRef]
  78. Thornhill, D.J.; Lajeunesse, T.C.; Kemp, D.W.; Fitt, W.K.; Schmidt, G.W. Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar. Biol. 2006, 148, 711–722. [Google Scholar] [CrossRef]
  79. Pigliucci, M.; Murren, C.J.; Schlichting, C.D. Phenotypic plasticity and evolution by genetic assimilation. J. Exp. Biol. 2006, 209, 2362–2367. [Google Scholar] [CrossRef] [Green Version]
  80. Smith, L.W.; Barshis, D.; Birkeland, C. Phenotypic plasticity for skeletal growth, density, and calification of Porites lobata in response to habitat type. Coral Reefs 2007, 26, 559–567. [Google Scholar] [CrossRef]
  81. Sawall, Y.; Al-Sofyani, A.; Hohn, S.; Banguera-Hinestroza, E.; Voolstra, C.R.; Wahl, M. Extensive phenotypic plasticity of a Red Sea coral over a strong latitudinal temperature gradient suggests limited acclimatization potential to warming. Sci. Rep. 2015, 5, 8940. [Google Scholar] [CrossRef] [Green Version]
  82. Bellantuono, A.J.; Hoegh-Guldberg, O.; Rodriguez-Lanetty, M. Resistance to thermal stress in corals without changes in symbiont composition. Proc. R. Soc. B Biol. Sci. 2012, 279, 1100–1107. [Google Scholar] [CrossRef] [Green Version]
  83. Middlebrook, R.; Hoegh-Guldberg, O.; Leggat, W. The effect of thermal history on the susceptibility of reef-building corals to thermal stress. J. Exp. Biol. 2008, 211, 1050–1056. [Google Scholar] [CrossRef] [Green Version]
  84. Hawkins, T.D.; Warner, M.E. Warm preconditioning protects against acute heat-induced respiratory dysfunction and delays bleaching in a symbiotic sea anemone. J. Exp. Biol. 2017, 220, 969–983. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  85. Putnam, H.M.; Gates, R.D. Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions. J. Exp. Biol. 2015, 218, 2365–2372. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  86. Fisch, J.; Drury, C.; Towle, E.K.; Winter, R.N.; Miller, M.W. Physiological and reproductive repercussions of consecutive summer bleaching events of the threatened Caribbean coral Orbicella faveolata. Coral Reefs 2019, 38, 863–876. [Google Scholar] [CrossRef]
  87. Coles, S.L.; Bahr, K.D.; Rodgers, K.u.S.; May, S.L.; McGowan, A.E.; Tsang, A.; Bumgarner, J.; Han, J.H. Evidence of acclimatization or adaptation in Hawaiian corals to higher ocean temperatures. Peer J. 2018, 6, e5347. [Google Scholar] [CrossRef] [PubMed]
  88. Hughes, T.P.; Kerry, J.T.; Connolly, S.R.; Baird, A.H.; Eakin, C.M.; Heron, S.F.; Hoey, A.S.; Hoogenboom, M.O.; Jacobson, M.; Liu, G.; et al. Ecological memory modifies the cumulative impact of recurrent climate extremes. Nat. Clim. Chang. 2019, 9, 40–43. [Google Scholar] [CrossRef]
  89. Guest, J.R.; Baird, A.H.; Maynard, J.A.; Muttaqin, E.; Edwards, A.J.; Campbell, S.J.; Yewdall, K.; Affendi, Y.A.; Chou, L.M. Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS ONE 2012, 7, e33353. [Google Scholar] [CrossRef]
  90. Brown, B.E.; Dunne, R.P.; Edwards, A.J.; Sweet, M.J.; Phongsuwan, N. Decadal environmental ‘memory’ in a reef coral? Mar. Biol. 2015, 162, 479–483. [Google Scholar] [CrossRef] [Green Version]
  91. Maynard, J.A.; Anthony, K.R.N.; Marshall, P.A.; Masiri, I. Major bleaching events can lead to increased thermal tolerance in corals. Mar. Biol. 2008, 155, 173–182. [Google Scholar] [CrossRef]
  92. Palumbi, S.R.; Barshis, D.J.; Traylor-Knowles, N.; Bay, R.A. Mechanisms of reef coral resistance to future climate change. Science 2014, 344, 895–898. [Google Scholar] [CrossRef]
  93. Mayfield, A.B.; Fan, T.-Y.; Chen, C.-S. Physiological acclimation to elevated temperature in a reef-building coral from an upwelling environment. Coral Reefs 2013, 32, 909–921. [Google Scholar] [CrossRef]
  94. Thompson, D.M.; Van Woesik, R. Corals escape bleaching in regions that recently and historically experienced frequent thermal stress. Proc. R. Soc. B Biol. Sci. 2009, 276, 2893–2901. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  95. Safaie, A.; Silbiger, N.J.; McClanahan, T.R.; Pawlak, G.; Barshis, D.J.; Hench, J.L.; Rogers, J.S.; Williams, G.J.; Davis, K.A. High frequency temperature variability reduces the risk of coral bleaching. Nat. Commun. 2018, 9, 1671. [Google Scholar] [CrossRef] [PubMed]
  96. Brown, B.; Dunne, R.; Warner, M.; Ambarsari, I.; Fitt, W.; Gibb, S.; Cummings, D.G. Damage and recovery of Photosystem II during a manipulative field experiment on solar bleaching in the coral Goniastrea aspera. Mar. Ecol. Prog. Ser. 2000, 195, 117–124. [Google Scholar] [CrossRef]
  97. Thomas, L.; Rose, N.H.; Bay, R.A.; López, E.H.; Morikawa, M.K.; Ruiz-Jones, L.; Palumbi, S.R. Mechanisms of thermal tolerance in reef-building corals across a fine-grained environmental mosaic: Lessons from Ofu, American Samoa. Front. Mar. Sci. 2018, 4. [Google Scholar] [CrossRef] [Green Version]
  98. Leggat, W.; Seneca, F.; Wasmund, K.; Ukani, L.; Yellowlees, D.; Ainsworth, T.D. Differential responses of the coral host and their algal symbiont to thermal stress. PLoS ONE 2011, 6, e26687. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  99. Császár, N.; Seneca, F.; Van Oppen, M. Variation in antioxidant gene expression in the scleractinian coral Acropora millepora under laboratory thermal stress. Mar. Ecol. Prog. Ser. 2009, 392, 93–102. [Google Scholar] [CrossRef] [Green Version]
  100. DeSalvo, M.K.; Sunagawa, S.; Voolstra, C.R.; Medina, M. Transcriptomic responses to heat stress and bleaching in the elkhorn coral Acropora palmata. Mar. Ecol. Prog. Ser. 2010, 402, 97–113. [Google Scholar] [CrossRef] [Green Version]
  101. Seneca, F.O.; Palumbi, S.R. The role of transcriptome resilience in resistance of corals to bleaching. Mol. Ecol. 2015, 24, 1467–1484. [Google Scholar] [CrossRef]
  102. Bellantuono, A.J.; Granados-Cifuentes, C.; Miller, D.J.; Hoegh-Guldberg, O.; Rodriguez-Lanetty, M. Coral thermal tolerance: Tuning gene expression to resist thermal stress. PLoS ONE 2012, 7, e50685. [Google Scholar] [CrossRef] [Green Version]
  103. Barshis, D.J.; Ladner, J.T.; Oliver, T.A.; Seneca, F.O.; Traylor-Knowles, N.; Palumbi, S.R. Genomic basis for coral resilience to climate change. Proc. Natl. Acad. Sci. USA 2013, 110, 1387–1392. [Google Scholar] [CrossRef] [Green Version]
  104. Ruiz-Jones, L.J.; Palumbi, S.R. Tidal heat pulses on a reef trigger a fine-tuned transcriptional response in corals to maintain homeostasis. Sci. Adv. 2017, 3, e1601298. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  105. Brown, B.E. Adaptations of reef corals to physical environmental stress. Adv. Mar. Biol. 1997, 31, 222–299. [Google Scholar]
  106. Hoegh-Guldberg, O. The adaptation of coral reefs to climate change: Is the Red Queen being outpaced? Sci. Mar. 2012, 76, 403–408. [Google Scholar] [CrossRef] [Green Version]
  107. Torda, G.; Donelson, J.M.; Aranda, M.; Barshis, D.J.; Bay, L.; Berumen, M.L.; Bourne, D.G.; Cantin, N.; Foret, S.; Matz, M.; et al. Rapid adaptive responses to climate change in corals. Nat. Clim. Chang. 2017, 7, 627. [Google Scholar] [CrossRef]
  108. Eirin-Lopez, J.M.; Putnam, H.M. Marine environmental epigenetics. Annu. Rev. Mar. Sci. 2019, 11, 335–368. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  109. Durante, M.K.; Baums, I.B.; Williams, D.E.; Vohsen, S.; Kemp, D.W. What drives phenotypic divergence among coral clonemates of Acropora palmata? Mol. Ecol. 2019, 28. [Google Scholar] [CrossRef] [Green Version]
  110. Van Oppen, M.J.H.; Souter, P.; Howells, E.J.; Heyward, A.; Berkelmans, R. Novel genetic diversity through somatic mutations: Fuel for adaptation of reef corals? Diversity 2011, 3, 405–423. [Google Scholar] [CrossRef] [Green Version]
  111. Wilkerson, F.; Kobayashi, D.; Muscatine, L. Mitotic index and size of symbiotic algae in Caribbean reef corals. Coral Reefs 1988, 7, 29–36. [Google Scholar] [CrossRef]
  112. Fitt, W.K.; McFarland, F.K.; Warner, M.E.; Chilcoat, G.C. Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol. Oceanogr. 2000, 45, 677–685. [Google Scholar] [CrossRef] [Green Version]
  113. Howells, E.J.; Beltrán, V.H.; Larsen, N.W.; Bay, L.K.; Willis, B.L.; van Oppen, M.J.H. Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat. Clim. Chang. 2012, 2, 116–120. [Google Scholar] [CrossRef]
  114. Chakravarti, L.J.; Beltran, V.H.; van Oppen, M.J. Rapid thermal adaptation in photosymbionts of reef-building corals. Glob. Chang. Biol. 2017, 23, 4675–4688. [Google Scholar] [CrossRef] [PubMed]
  115. Dixon, G.B.; Davies, S.W.; Aglyamova, G.V.; Meyer, E.; Bay, L.K.; Matz, M.V. Genomic determinants of coral heat tolerance across latitudes. Science 2015, 348, 1460–1462. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  116. Krueger, T.; Horwitz, N.; Bodin, J.; Giovani, M.-E.; Escrig, S.; Meibom, A.; Fine, M. Common reef-building coral in the northern Red Sea resistant to elevated temperature and acidification. R. Soc. Open Sci. 2017, 4, 170038. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  117. Fine, M.; Gildor, H.; Genin, A. A coral reef refuge in the Red Sea. Glob. Chang. Biol. 2013, 19, 3640–3647. [Google Scholar] [CrossRef] [PubMed]
  118. Houlbrèque, F.; Ferrierriers, C. Heterotrophy in tropical scleractinian corals. Biol. Rev. 2009, 84, 1–17. [Google Scholar] [CrossRef] [PubMed]
  119. Grottoli, A.G.; Rodrigues, L.J.; Palardy, J.E. Heterotrophic plasticity and resilience in bleached corals. Nature 2006, 440, 1186–1189. [Google Scholar] [CrossRef]
  120. Rodrigues, L.J.; Grottoli, A.G. Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol. Oceanogr. 2007, 52, 1874–1882. [Google Scholar] [CrossRef]
  121. Borell, E.M.; Bischof, K. Feeding sustains photosythetic quantum yield of a scleractinian coral during thermal stress. Oecologia 2008, 157, 593–601. [Google Scholar] [CrossRef]
  122. Borell, E.M.; Yuliantri, A.R.; Bischof, K.; Richter, C. The effect of heterotrophy on photosynthesis and tissue composition of two scleractinian corals under elevated temperature. J. Exp. Mar. Biol. Ecol. 2008, 364, 116–123. [Google Scholar] [CrossRef]
  123. Anthony, K.; Hoogenboom, M.O.; Maynard, J.A.; Grottoli, A.G.; Middlebrook, R. Energetics approach to predicting mortality risk from environmental stress: A case study of coral bleaching. Funct. Ecol. 2009, 23, 539–550. [Google Scholar] [CrossRef]
  124. Hughes, A.; Grottoli, A.; Pease, T.; Matsui, Y. Acquisition and assimilation of carbon in non-bleached and bleached corals. Mar. Ecol. Prog. Ser. 2010, 420, 91–101. [Google Scholar] [CrossRef]
  125. Baumann, J.; Grottoli, A.G.; Hughes, A.D.; Matsui, Y. Photoautotrophic and heterotrophic carbon in bleached and non-bleached coral lipid acquisition and storage. J. Exp. Mar. Biol. Ecol. 2014, 461, 469–478. [Google Scholar] [CrossRef]
  126. Hughes, A.D.; Grottoli, A.G. Heterotrophic compensation: A possible mechanism for resilience of coral reefs to global warming or a sign of prolonged stress? PLoS ONE 2013, 8, e81172. [Google Scholar] [CrossRef] [PubMed]
  127. Levas, S.; Grottoli, A.G.; Schoepf, V.; Aschaffenburg, M.; Baumann, J.; Bauer, J.E.; Warner, M.E. Can heterotrophic uptake of dissolved organic carbon and zooplankton mitigate carbon budget deficits in annually bleached corals? Coral Reefs 2016, 35, 495–506. [Google Scholar] [CrossRef]
  128. Grottoli, A.G.; Warner, M.E.; Levas, S.J.; Aschaffenburg, M.D.; Schoepf, V.; McGinley, M.; Baumann, J.; Matsui, Y. The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Glob. Chang. Biol. 2014, 20, 3823–3833. [Google Scholar] [CrossRef]
  129. Van Oppen, M.J.H.; Puill-Stephan, E.; Lundgren, P.; De’ath, G.; Bay, L.K. First-generation fitness consequences of interpopulational hybridisation in a Great Barrier Reef coral and its implications for assisted migration management. Coral Reefs 2014, 33, 607–611. [Google Scholar] [CrossRef]
  130. Hoegh-Guldberg, O.; Hughes, L.; Mclntyre, S.; Lindenmayer, D.B.; Parmesan, C.; Possingham, H.P.; Thomas, C.D. Assisted colonization and rapid climate change. Science 2008, 321, 345–346. [Google Scholar] [CrossRef]
  131. Anthony, K.; Bay, L.K.; Costanza, R.; Firn, J.; Gunn, J.; Harrison, P.; Heyward, A.; Lundgren, P.; Mead, D.; Moore, T.; et al. New interventions are needed to save coral reefs. Nat. Ecol. Evol. 2017, 1, 1420. [Google Scholar] [CrossRef]
  132. Webster, N.S.; Reusch, T.B.H. Microbial contributions to the persistence of coral reefs. ISME J. 2017, 11, 2167. [Google Scholar] [CrossRef]
  133. Chan, W.Y.; Peplow, L.M.; Menéndez, P.; Hoffmann, A.A.; van Oppen, M.J.H. Interspecific hybridization may provide novel opportunities for coral reef restoration. Front. Mar. Sci. 2018, 5. [Google Scholar] [CrossRef] [Green Version]
  134. Van Oppen, M.J.; Oliver, J.K.; Putnam, H.M.; Gates, R.D. Building coral reef resilience through assisted evolution. Proc. Natl. Acad. Sci. USA 2015, 112, 2307–2313. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  135. Levin, R.A.; Voolstra, C.R.; Agrawal, S.; Steinberg, P.D.; Suggett, D.J.; van Oppen, M.J.H. Engineering strategies to decode and enhance the genomes of coral symbionts. Front. Microbiol. 2017, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  136. Spalding, M.D.; Brown, B.E. Warm-water coral reefs and climate change. Science 2015, 350, 769–771. [Google Scholar] [CrossRef] [PubMed]
  137. Coles, S.L.; Riegl, B.M. Thermal tolerances of reef corals in the Gulf: A review of the potential for increasing coral survival and adaptation to climate change through assisted translocation. Mar. Pollut. Bull. 2013, 72, 323–332. [Google Scholar] [CrossRef]
  138. Riegl, B.M.; Purkis, S.J.; Al-Cibahy, A.S.; Abdel-Moati, M.A.; Hoegh-Guldberg, O. Present limits to heat-adaptability in corals and population-level responses to climate extremes. PLoS ONE 2011, 6, e24802. [Google Scholar] [CrossRef]
  139. Hughes, T.P.; Anderson, K.D.; Connolly, S.R.; Heron, S.F.; Kerry, J.T.; Lough, J.M.; Baird, A.H.; Baum, J.K.; Berumen, M.L.; Bridge, T.C.; et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 2018, 359, 80–83. [Google Scholar] [CrossRef] [Green Version]
  140. Cziesielski, M.J.; Schmidt-Roach, S.; Aranda, M. The past, present, and future of coral heat stress studies. Ecol. Evol. 2019, 9, 10055–10066. [Google Scholar] [CrossRef]
  141. Bayraktarov, E.; Saunders, M.I.; Abdullah, S.; Mills, M.; Beher, J.; Possingham, H.P.; Mumby, P.J.; Lovelock, C.E. The cost and feasibility of marine coastal restoration. Ecol. Appl. 2016, 26, 1055–1074. [Google Scholar] [CrossRef]
  142. Kaebnick, G.E.; Heitman, E.; Collins, J.P.; Delborne, J.A.; Landis, W.G.; Sawyer, K.; Taneyhill, L.A.; Winickoff, D.E. Precaution and governance of emerging technologies. Science 2016, 354, 710–711. [Google Scholar] [CrossRef] [Green Version]
  143. Edgar, G.J.; Stuart-Smith, R.D.; Willis, T.J.; Kininmonth, S.; Baker, S.C.; Banks, S.; Barret, N.S.; Becerro, M.A.; Bernard, A.T.F.; Berkhout, J.; et al. Global conservation outcomes depend on marine protected areas with five key features. Nature 2014, 506, 216. [Google Scholar] [CrossRef] [Green Version]
  144. Bates, A.E.; Cooke, R.S.C.; Duncan, M.I.; Edgar, G.J.; Bruno, J.F.; Benedetti-Cecchi, L.; Côté, I.M.; Lefcheck, J.S.; Costello, M.J.; Barrett, N.; et al. Climate resilience in marine protected areas and the ‘Protection Paradox’. Biol. Conserv. 2019, 236, 305–314. [Google Scholar] [CrossRef]
  145. Grorud-Colvert, K.; Claudet, J.; Tissot, B.N.; Caselle, J.E.; Carr, M.H.; Day, J.C.; Friedlander, A.M.; Lester, S.E.; De Loma, T.L.; Malone, D.; et al. Marine protected area networks: Assessing whether the whole is greater than the sum of its parts. PLoS ONE 2014, 9, e102298. [Google Scholar] [CrossRef] [PubMed]
  146. Bellwood, D.R.; Pratchett, M.S.; Morrison, T.H.; Gurney, G.G.; Hughes, T.P.; Álvarez-Romero, J.G.; Day, J.C.; Grantham, R.; Grech, A.; Hoey, A.S.; et al. Coral reef conservation in the Anthropocene: Confronting spatial mismatches and prioritizing functions. Biol. Conserv. 2019, 236, 604–615. [Google Scholar] [CrossRef]
  147. Mumby, P.J.; Elliott, I.A.; Eakin, C.M.; Skirving, W.; Paris, C.B.; Edwards, H.J.; Enríquez, S.; Iglesias-Prieto, R.; Cherubin, L.M.; Stevens, J.R. Reserve design for uncertain responses of coral reefs to climate change. Ecol. Lett. 2011, 14, 132–140. [Google Scholar] [CrossRef] [PubMed]
  148. Beyer, H.L.; Kennedy, E.V.; Beger, M.; Chen, C.A.; Cinner, J.E.; Darling, E.S.; Eakin, C.M.; Gates, R.D.; Heron, S.F.; Knowlton, N.; et al. Risk-sensitive planning for conserving coral reefs under rapid climate change. Conserv. Lett. 2018, 11, e12587. [Google Scholar] [CrossRef]
  149. Hoegh-Guldberg, O.; Kennedy, E.V.; Beyer, H.L.; McClennen, C.; Possingham, H.P. Securing a long-term future for coral reefs. Trends Ecol. Evol. 2018, 33, 936–944. [Google Scholar] [CrossRef] [Green Version]
  150. Selig, E.R.; Casey, K.S.; Bruno, J.F. Temperature-driven coral decline: The role of marine protected areas. Glob. Chang. Biol. 2012, 18, 1561–1570. [Google Scholar] [CrossRef]
  151. Bruno, J.F.; Côté, I.M.; Toth, L.T. Climate change, coral loss, and the curious case of the parrotfish paradigm: Why don’t marine protected areas improve reef resilience? Annu. Rev. Mar. Sci. 2019, 11, 307–334. [Google Scholar] [CrossRef] [Green Version]
  152. Hughes, T.P.; Kerry, J.T.; Baird, A.H.; Connolly, S.R.; Dietzel, A.; Eakin, C.M.; Heron, S.F.; Hoey, A.S.; Hoogenboom, M.O.; Liu, G.; et al. Global warming transforms coral reef assemblages. Nature 2018, 556, 492. [Google Scholar] [CrossRef]
  153. Sheppard, C.; Sheppard, A.; Mogg, A.; Bayley, D.; Dempsey, A.C.; Roche, R.; Turner, J.; Purkis, S. Coral bleaching and mortality in the Chagos Archipelago. Atoll Res. Bull. 2017, 613, 1–26. [Google Scholar] [CrossRef]
  154. Barkley, H.C.; Cohen, A.L.; Mollica, N.R.; Brainard, R.E.; Rivera, H.E.; DeCarlo, T.M.; Lohmann, G.P.; Drenkard, E.J.; Alpert, A.E.; Young, C.W.; et al. Repeat bleaching of a central Pacific coral reef over the past six decades (1960–2016). Commun. Biol. 2018, 1, 177. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  155. Fox, M.D.; Carter, A.L.; Edwards, C.B.; Takeshita, Y.; Johnson, M.D.; Petrovic, V.; Amir, C.G.; Sala, E.; Sandin, S.A.; Smith, J.E. Limited coral mortality following acute thermal stress and widespread bleaching on Palmyra Atoll, central Pacific. Coral Reefs 2019, 38, 701–712. [Google Scholar] [CrossRef]
  156. Van Oppen, M.J.; Gates, R.D.; Blackall, L.L.; Cantin, N.; Chakravarti, L.J.; Chan, W.Y.; Cormick, C.; Crean, A.; Damjanovic, K.; Epstein, H.; et al. Shifting paradigms in restoration of the world’s coral reefs. Glob. Chang. Biol. 2017, 23, 3437–3448. [Google Scholar] [CrossRef] [PubMed]
  157. Rinkevich, B. The active reef restoration toolbox is a vehicle for coral resilience and adaptation in a changing world. J. Mar. Sci. Eng. 2019, 7, 201. [Google Scholar] [CrossRef] [Green Version]
  158. Morikawa, M.K.; Palumbi, S.R. Using naturally occurring climate resilient corals to construct bleaching-resistant nurseries. Proc. Natl. Acad. Sci. USA 2019, 116, 10586–10591. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  159. Kenkel, C.D.; Matz, M.V. Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nat. Ecol. Evol. 2017, 1, 0014. [Google Scholar] [CrossRef] [PubMed]
  160. Bay, R.A.; Palumbi, S.R. Transcriptome predictors of coral survival and growth in a highly variable environment. Ecol. Evol. 2017, 7, 4794–4803. [Google Scholar] [CrossRef]
  161. Bay, R.A.; Rose, N.H.; Logan, C.A.; Palumbi, S.R. Genomic models predict successful coral adaptation if future ocean warming rates are reduced. Sci. Adv. 2017, 3, e1701413. [Google Scholar] [CrossRef] [Green Version]
  162. Frieler, K.; Meinshausen, M.; Golly, A.; Mengel, M.; Lebek, K.; Donner, S.D.; Hoegh-Guldberg, O. Limiting global warming to 2 °C is unlikely to save most coral reefs. Nat. Clim. Chang. 2012, 3, 165. [Google Scholar] [CrossRef]
  163. Van Hooidonk, R.; Maynard, J.; Tamelander, J.; Gove, J.; Ahmadia, G.; Raymundo, L.; Williams, G.; Heron, S.F.; Planes, S. Local-scale projections of coral reef futures and implications of the Paris Agreement. Sci. Rep. 2016, 6, 39666. [Google Scholar] [CrossRef]
  164. Pachauri, R.K.; Allen, M.R.; Barros, V.R.; Broome, J.; Cramer, W.; Christ, R.; Church, J.A.; Clarke, L.; Dahe, Q.; Dasgupta, P.; et al. Climate change 2014: Synthesis report. In Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change; Ipcc: Geneva, Switzerland, 2014. [Google Scholar]
  165. Graham, N.A.; Bellwood, D.R.; Cinner, J.E.; Hughes, T.P.; Norström, A.V.; Nyström, M. Managing resilience to reverse phase shifts in coral reefs. Front. Ecol. Environ. 2013, 11, 541–548. [Google Scholar] [CrossRef]
  166. Spash, C.L. This changes nothing: The Paris Agreement to ignore reality. Globalizations 2016, 13, 928–933. [Google Scholar] [CrossRef]
Jmse 08 00015 g001 550
Figure 1. (A) Onset of a bleaching process in a colony of Acropora spp., in Kenting, Taiwan 2015 (Photo: J. Wei); (B) Bleaching event showing colonies with fluorescent pigments as a protective mechanism (a) and already bleached colonies (b), in Okinawa, Japan 2016 (Photo: S.-Y. Yang); (C) Intra-specific: between Montipora spp. colonies (a) and between Isopora palifera colonies (b), inter-specific: between Montipora spp. and I. palifera colonies (c) and intra-colony: within Leptoria phrygia colony (d) responses to thermal stress in Kenting, Taiwan 2016 (Photo: R. Carballo-Bolaños).
Figure 1. (A) Onset of a bleaching process in a colony of Acropora spp., in Kenting, Taiwan 2015 (Photo: J. Wei); (B) Bleaching event showing colonies with fluorescent pigments as a protective mechanism (a) and already bleached colonies (b), in Okinawa, Japan 2016 (Photo: S.-Y. Yang); (C) Intra-specific: between Montipora spp. colonies (a) and between Isopora palifera colonies (b), inter-specific: between Montipora spp. and I. palifera colonies (c) and intra-colony: within Leptoria phrygia colony (d) responses to thermal stress in Kenting, Taiwan 2016 (Photo: R. Carballo-Bolaños).
Jmse 08 00015 g001
Table
Table 1. Studies performed to test acclimatisation to thermal stress and high temperature variability at different locations around the world.
Table 1. Studies performed to test acclimatisation to thermal stress and high temperature variability at different locations around the world.
StudyTemp/DHWDurationLocationSpeciesMain ResultsRef.
Precondition + HSE28 °C (precond.)10 dGBR, AustraliaAcropora milleporaNo bleaching in pre-conditioned corals[82]
31 °C (HSE)8 d
Precondition + HSE31 °C (precond.)2 dGBR, AustraliaAcropora asperaNo bleaching in pre-conditioned corals[83]
34 °C (HSE)6 d
Comparison 1998/2002 BEDHW = 2002 > 1998Bleaching surveyGBR, AustraliaAcropora spp., Pocillopora spp., Porites spp.Less mortality in 2002[91]
Comparison 1998/2010 BEDHW = Malaysia + Singapore > IndonesiaBleaching surveyIndonesia, Malaysia, SingaporeAcropora spp., Pocillopora spp.,Low bleaching in Malaysia and Singapore[89]
Survey 2010 BE-Bleaching surveyThailandCoelastrea asperaLess bleaching in high irradiance colony sides (decadal environmental ‘memory’)[90]
Comparison 1970/2017 HSE31.4 °C 31 dHawaii, USAMontipora capitata, Pocillopora damicornis, Lobactis scutariaHigher calcification, delayed bleaching and mortality in 2017 [87]
HSE (HV and MV)31.5 °C5 dAmerican SamoaAcropora hyacinthusMortality and photochemical efficiency decline: HV+Durusdinium < MV+Durusdinium < MV+Cladocopium [67]
HSE from RT (HV and MV)34 °C3 hAmerican SamoaAcropora hyacinthusAcclimatised: MV to HV increased heat resistance; HV to MV reduced chl a retention; Different expression of 74 genes[92]
HSE (HV and LV)30 °C270 dTaiwanPocillopora damicornis,Acclimatised: HV = control in all parameters[93]
Comparison 1998/2005-06 BE (HV - LV)-Bleaching surveyEgypt, Madagascar, Seychelles, Australia, Guam, Kiribati, Cook IslandsMultiple speciesLess bleaching in HV sites[94]
Comparison multiple BEs (HV - LV)-Bleaching surveyWestern Indian Ocean, Pacific Ocean, Caribbean Sea, GBR, Red Sea Multiple speciesLess bleaching in HV sites[95]
HSE = Heat Stress Experiment, HV = Highly Variable, MV = Moderately Variable, LV = Low Variable, RT = Reciprocal Transplantation, BE = Bleaching Event, DHW = Degree Heating Weeks, d = days, h = hours, GBR = Great Barrier Reef.
Table
Table 2. Thermal stress studies looking at differences in gene expression.
Table 2. Thermal stress studies looking at differences in gene expression.
StudyMethodGenes/MoleculesResponseLocationSpeciesMain ResultsRef.
HSE – gene expressionqPCRHSP70, MnSOD, ferritin, Zn2+-metalloproteaseOxidative stress responseGBR, AustraliaAcropora milleporaUp-regulation in heat-stressed[99]
HSE – gene expressionqPCRHSP90, HSP70Oxidative stress response GBR, AustraliaAcropora aspera10.5-fold up-regulation in heat-stressed coral host genes[98]
Glyceraldehyde-3-phosphate dehydrogenase, α-ketoglutarate dehydrogenase, glycogen synthase, glycogen phosphorylaseCarbon metabolism
Short-term precondition—gene expressioncDNA micro-arrayLectins, heme-binding proteins, transcription factor AP-1, NF-kB inhibitor, thymosin, phosphate carrier protein, ferritinOxidative stress responseGBR, AustraliaAcropora asperaDifferent expression: 70 genes (non-preconditioned/control), 42 genes (preconditioned/control), 9 genes (preconditioned/non-preconditioned)[102]
HSE—transcriptome wide gene expression (Thermally resilient vs. sensitive)RNA-Seq HSP70, HSP23/HSPB1, HSP16.2, CSMD1, Cu-Zn SODOxidative stress response American SamoaAcropora hyacinthusUp-regulation in thermal sensitive: 60 genes = “Frontloaded” in thermal resistant [103]
TNFRs, TRAFs, NF-κB/Nfkb1, JNK/MAPK8Apoptosis/immune response
HSE—transcriptome wide gene expression
(RT HV – MV)		RNA-Seq HSPs, Chaperonin proteins, CYPsOxidative stress responseAmerican SamoaAcropora hyacinthusDifferent expression: 71 contigs based on pool of origin (HV/MV), 74 contigs based on pool transplanted [93]
TNFRs, TRAFs,Apoptosis/immune response
HSE = Heat Stress Experiment, HV = Highly Variable, MV = Moderately Variable, RT = Reciprocal Transplantation, qPCR = quantitative Polymerase Chain Reaction, HSP = Heat Stress Protein, SOD = Superoxide Dismutase, TNFR = Tumor Necrosis Factor Receptor, TRAF = Tumor Receptor Associated Family, GBR = Great Barrier Reef.

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Carballo-Bolaños, R.; Soto, D.; Chen, C.A. Thermal Stress and Resilience of Corals in a Climate-Changing World. J. Mar. Sci. Eng. 2020, 8, 15. https://doi.org/10.3390/jmse8010015

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Carballo-Bolaños R, Soto D, Chen CA. Thermal Stress and Resilience of Corals in a Climate-Changing World. Journal of Marine Science and Engineering. 2020; 8(1):15. https://doi.org/10.3390/jmse8010015

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Carballo-Bolaños, Rodrigo, Derek Soto, and Chaolun Allen Chen. 2020. "Thermal Stress and Resilience of Corals in a Climate-Changing World" Journal of Marine Science and Engineering 8, no. 1: 15. https://doi.org/10.3390/jmse8010015

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