Papers on coral response to global warming

This is a list of papers on coral response to global warming and the ocean acidification. The list is not complete, and will most likely be updated in the future in order to make it more thorough and more representative.

UPDATE (March 22, 2016): Some dead links corrected, re-formatting, and Gleason & Wellington (1993), Glynn (1996), Fischer & Jones (2012), Barshis et al. (2013), Logan et al. (2014), Yara et al. (2014), Palumbi et al. (2014), Grottoli et al. (2014), Kwiatkowski et al. (2015), and Chow et al. (2016) added.

Quantifying the degree of coral bleaching using digital photographic technique – Chow et al. (2016)
Abstract: A simple, non-destructive and objective method is developed and evaluated to quantify bleaching or colour change in coral in terms of its percent whiteness. Digital photos of coral colony were taken with a photoquadrat marked with black and white bands around a metal frame to serve as colour references. Photos taken were then converted to a black and white grey-scale and intensities of the coral colour were determined with reference to this grey-scale using computer image analytical technique. A completely bleached coral gave an estimated percent whiteness that is close to 100%, an estimate that agrees well with the visual image of a bleached coral. The percent whiteness estimates were found not to be significantly affected by different levels of irradiance and turbidites under simulated conditions. Colour change in seven common Hong Kong coral species were further evaluated in situ and shown to exhibit an increasing trend of percent whiteness from January (winter) to April 2012 (spring), reflecting an increasing degree of bleaching. Using Goniopora lobata as an experimental species, estimated percent whiteness was shown to be negatively correlated with its zooxanthellae density and chlorophyll a concentration. This suggests that this method could allow repeated monitoring of individual coral colony over time to detect subtle variations in its colour as a general assessment of its health. Furthermore, reference percent whiteness of different coral species can be standardized for comparison of colour change over time to identify the critical level of percent whiteness that is associated with bleaching. Thus, this method should prove to be an easy and objective tool for rapid field assessment of coral health.
Citation: M.H. Chow, Ryan H.L. Tsang, Eric K.Y. Lam, P. Ang Jr., Journal of Experimental Marine Biology and Ecology, Volume 479, June 2016, Pages 60–68, doi:10.1016/j.jembe.2016.03.003.

Coral bleaching under unconventional scenarios of climate warming and ocean acidification – Kwiatkowski et al. (2015)
Abstract: Elevated sea surface temperatures have been shown to cause mass coral bleaching. Widespread bleaching, affecting >90% of global coral reefs and causing coral degradation, has been projected to occur by 2050 under all climate forcing pathways adopted by the IPCC for use within the Fifth Assessment Report. These pathways include an extremely ambitious pathway aimed to limit global mean temperature rise to 2 °C (ref. 6; Representative Concentration Pathway 2.6—RCP2.6), which assumes full participation in emissions reductions by all countries, and even the possibility of negative emissions. The conclusions drawn from this body of work, which applied widely used algorithms to estimate coral bleaching, are that we must either accept that the loss of a large percentage of the world’s coral reefs is inevitable, or consider technological solutions to buy those reefs time until atmospheric CO2 concentrations can be reduced. Here we analyse the potential for geoengineering, through stratospheric aerosol-based solar radiation management (SRM), to reduce the extent of global coral bleaching relative to ambitious climate mitigation. Exploring the common criticism of geoengineering—that ocean acidification and its impacts will continue unabated—we focus on the sensitivity of results to the aragonite saturation state dependence of bleaching. We do not, however, address the additional detrimental impacts of ocean acidification on processes such as coral calcification that will further determine the benefit to corals of any SRM-based scenario. Despite the sensitivity of thermal bleaching thresholds to ocean acidification being uncertain, stabilizing radiative forcing at 2020 levels through SRM reduces the risk of global bleaching relative to RCP2.6 under all acidification–bleaching relationships analysed.
Citation: Lester Kwiatkowski, Peter Cox, Paul R. Halloran, Peter J. Mumby, Andy J. Wiltshire, Nature Climate Change 5, 777–781 (2015) doi:10.1038/nclimate2655. [full text]

The cumulative impact of annual coral bleaching can turn some coral species winners into losers – Grottoli et al. (2014)
Abstract: Mass coral bleaching events caused by elevated seawater temperatures result in extensive coral loss throughout the tropics, and are projected to increase in frequency and severity. If bleaching becomes an annual event later in this century, more than 90% of coral reefs worldwide may be at risk of long-term degradation. While corals can recover from single isolated bleaching and can acclimate to recurring bleaching events that are separated by multiple years, it is currently unknown if and how they will survive and possibly acclimatize to annual coral bleaching. Here, we demonstrate for the first time that annual coral bleaching can dramatically alter thermal tolerance in Caribbean corals. We found that high coral energy reserves and changes in the dominant algal endosymbiont type (Symbiodinium spp.) facilitated rapid acclimation in Porites divaricata, whereas low energy reserves and a lack of algal phenotypic plasticity significantly increased susceptibility in Porites astreoides to bleaching the following year. Phenotypic plasticity in the dominant endosymbiont type of Orbicella faveolata did not prevent repeat bleaching, but may have facilitated rapid recovery. Thus, coral holobiont response to an isolated single bleaching event is not an accurate predictor of its response to bleaching the following year. Rather, the cumulative impact of annual coral bleaching can turn some coral species ‘winners’ into ‘losers’, and can also facilitate acclimation and turn some coral species ‘losers’ into ‘winners’. Overall, these findings indicate that cumulative impact of annual coral bleaching could result in some species becoming increasingly susceptible to bleaching and face a long-term decline, while phenotypically plastic coral species will acclimatize and persist. Thus, annual coral bleaching and recovery could contribute to the selective loss of coral diversity as well as the overall decline of coral reefs in the Caribbean.
Citation: Grottoli, A. G., Warner, M. E., Levas, S. J., Aschaffenburg, M. D., Schoepf, V., McGinley, M., Baumann, J. and Matsui, Y. (2014), The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Glob Change Biol, 20: 3823–3833. doi:10.1111/gcb.12658. [full text]

Mechanisms of reef coral resistance to future climate change – Palumbi et al. (2014)
Abstract: Reef corals are highly sensitive to heat, yet populations resistant to climate change have recently been identified. To determine the mechanisms of temperature tolerance, we reciprocally transplanted corals between reef sites experiencing distinct temperature regimes and tested subsequent physiological and gene expression profiles. Local acclimatization and fixed effects, such as adaptation, contributed about equally to heat tolerance and are reflected in patterns of gene expression. In less than 2 years, acclimatization achieves the same heat tolerance that we would expect from strong natural selection over many generations for these long-lived organisms. Our results show both short-term acclimatory and longer-term adaptive acquisition of climate resistance. Adding these adaptive abilities to ecosystem models is likely to slow predictions of demise for coral reef ecosystems.
Citation: Stephen R. Palumbi, Daniel J. Barshis, Nikki Traylor-Knowles, Rachael A. Bay, Science 23 May 2014: Vol. 344, Issue 6186, pp. 895-898, DOI: 10.1126/science.1251336. [full text]

Projected coral bleaching in response to future sea surface temperature rises and the uncertainties among climate models – Yara et al. (2014)
Abstract: We quantitatively evaluated the effects of rising sea surface temperature (SST) on coral bleaching and the uncertainties resulting from differences in global warming projections. To do so, we used monthly SSTs in the twenty-first century obtained from 23 climate models under the A1B scenario (from the Special Report on Emissions Scenarios) and SST-based indices for coral bleaching. All of the projections indicated that severe bleaching or death of corals will be common and severe in wide areas of the tropical and subtropical oceans by the middle of this century. However, decadal oscillation could modify the exact timing by around ±10 years. Such projections are important for conserving marine biodiversity and designing future strategies to avoid tropical and subtropical coral extinction. To obtain more reliable projections and reduce uncertainties, climate models should be improved by using higher spatiotemporal resolutions, and more realistic biological indices should be embedded into existing models.
Citation: Yumiko Yara, Masahiko Fujii, Hiroya Yamano, Yasuhiro Yamanaka, Hydrobiologia, July 2014, Volume 733, Issue 1, pp 19-29, DOI: 10.1007/s10750-014-1838-0. [full text]

Incorporating adaptive responses into future projections of coral bleaching – Logan et al. (2014)
Abstract: Climate warming threatens to increase mass coral bleaching events, and several studies have projected the demise of tropical coral reefs this century. However, recent evidence indicates corals may be able to respond to thermal stress though adaptive processes (e.g., genetic adaptation, acclimatization, and symbiont shuffling). How these mechanisms might influence warming-induced bleaching remains largely unknown. This study compared how different adaptive processes could affect coral bleaching projections. We used the latest bias-corrected global sea surface temperature (SST) output from the NOAA/GFDL Earth System Model 2 (ESM2M) for the preindustrial period through 2100 to project coral bleaching trajectories. Initial results showed that, in the absence of adaptive processes, application of a preindustrial climatology to the NOAA Coral Reef Watch bleaching prediction method overpredicts the present-day bleaching frequency. This suggests that corals may have already responded adaptively to some warming over the industrial period. We then modified the prediction method so that the bleaching threshold either permanently increased in response to thermal history (e.g., simulating directional genetic selection) or temporarily increased for 2–10 years in response to a bleaching event (e.g., simulating symbiont shuffling). A bleaching threshold that changes relative to the preceding 60 years of thermal history reduced the frequency of mass bleaching events by 20–80% compared with the ‘no adaptive response’ prediction model by 2100, depending on the emissions scenario. When both types of adaptive responses were applied, up to 14% more reef cells avoided high-frequency bleaching by 2100. However, temporary increases in bleaching thresholds alone only delayed the occurrence of high-frequency bleaching by ca. 10 years in all but the lowest emissions scenario. Future research should test the rate and limit of different adaptive responses for coral species across latitudes and ocean basins to determine if and how much corals can respond to increasing thermal stress.
Citation: Logan, C. A., Dunne, J. P., Eakin, C. M. and Donner, S. D. (2014), Incorporating adaptive responses into future projections of coral bleaching. Glob Change Biol, 20: 125–139. doi:10.1111/gcb.12390. [full text]

Genomic basis for coral resilience to climate change – Barshis et al. (2013)
Abstract: Recent advances in DNA-sequencing technologies now allow for in-depth characterization of the genomic stress responses of many organisms beyond model taxa. They are especially appropriate for organisms such as reef-building corals, for which dramatic declines in abundance are expected to worsen as anthropogenic climate change intensifies. Different corals differ substantially in physiological resilience to environmental stress, but the molecular mechanisms behind enhanced coral resilience remain unclear. Here, we compare transcriptome-wide gene expression (via RNA-Seq using Illumina sequencing) among conspecific thermally sensitive and thermally resilient corals to identify the molecular pathways contributing to coral resilience. Under simulated bleaching stress, sensitive and resilient corals change expression of hundreds of genes, but the resilient corals had higher expression under control conditions across 60 of these genes. These “frontloaded” transcripts were less up-regulated in resilient corals during heat stress and included thermal tolerance genes such as heat shock proteins and antioxidant enzymes, as well as a broad array of genes involved in apoptosis regulation, tumor suppression, innate immune response, and cell adhesion. We propose that constitutive frontloading enables an individual to maintain physiological resilience during frequently encountered environmental stress, an idea that has strong parallels in model systems such as yeast. Our study provides broad insight into the fundamental cellular processes responsible for enhanced stress tolerances that may enable some organisms to better persist into the future in an era of global climate change.
Citation: Daniel J. Barshis, Jason T. Ladner, Thomas A. Oliver, François O. Seneca, Nikki Traylor-Knowles, Stephen R. Palumbi, PNAS, 110, 4, 1387–1392, doi: 10.1073/pnas.1210224110. [full text]

Atmospheric dimethysulphide production from corals in the Great Barrier Reef and links to solar radiation, climate and coral bleaching – Fischer & Jones (2012)
Abstract: Coral zooxanthellae contain high concentrations of dimethylsulphoniopropionate (DMSP), the precursor of dimethylsulphide (DMS), an aerosol substance that could affect cloud cover, solar radiation and ocean temperatures. Acropora intermedia a dominant staghorn coral in the Indo-Pacific region, contain some of the highest concentrations of DMSP reported in the literature but no studies have shown that corals produce atmospheric DMS in situ and thus could potentially participate in sea surface temperature (SST) regulation over reefs; or how production varies during coral bleaching. We show that A. intermedia from the Great Barrier Reef (GBR) produces significant amounts of atmospheric DMS, in chamber experiments, indicating that coral reefs in this region could contribute to an “ocean thermostat” similar to that described for the western Pacific warm pool, where significantly fewer coral reefs have bleached during the last 25 years because of a cloud-SST feedback. However, when Acropora intermedia was stressed with higher light levels and seawater temperatures DMSP production, an indicator of zooxanthellae expulsion, increased markedly in the chamber, whilst atmospheric DMS emissions almost completely shut down. These results suggest that during increased light levels and seawater temperatures in the GBR coral shut-down atmospheric DMS aerosol production, potentially increasing solar radiation levels over reefs and exacerbating coral bleaching.
Citation: Esther Fischer, Graham Jones, Biogeochemistry, September 2012, Volume 110, Issue 1, pp 31-46, DOI: 10.1007/s10533-012-9719-y.

Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures – Yamano et al. (2011)
Abstract: Rising temperatures caused by climatic warming may cause poleward range shifts and/or expansions in species distribution. Tropical reef corals (hereafter corals) are some of the world’s most important species, being not only primary producers, but also habitat-forming species, and thus fundamental ecosystem modification is expected according to changes in their distribution. Although most studies of climate change effects on corals have focused on temperature-induced coral bleaching in tropical areas, poleward range shifts and/or expansions may also occur in temperate areas. We show the first large-scale evidence of the poleward range expansion of modern corals, based on 80 years of national records from the temperate areas of Japan, where century-long measurements of in situ sea-surface temperatures have shown statistically significant rises. Four major coral species categories, including two key species for reef formation in tropical areas, showed poleward range expansions since the 1930s, whereas no species demonstrated southward range shrinkage or local extinction. The speed of these expansions reached up to 14 km/year, which is far greater than that for other species. Our results, in combination with recent findings suggesting range expansions of tropical coral-reef associated organisms, strongly suggest that rapid, fundamental modifications of temperate coastal ecosystems could be in progress.
Citation: Yamano, H., K. Sugihara, and K. Nomura (2011), Geophys. Res. Lett., 38, L04601, doi:10.1029/2010GL046474. [full text]

Modeling regional coral reef responses to global warming and changes in ocean chemistry: Caribbean case study – Buddemeier et al. (2011)
Abstract: Climatic change threatens the future of coral reefs in the Caribbean and the important ecosystem services they provide. We used a simulation model [Combo (“COral Mortality and Bleaching Output”)] to estimate future coral cover in the part of the eastern Caribbean impacted by a massive coral bleaching event in 2005. Combo calculates impacts of future climate change on coral reefs by combining impacts from long-term changes in average sea surface temperature (SST) and ocean acidification with impacts from episodic high temperature mortality (bleaching) events. We used mortality and heat dose data from the 2005 bleaching event to select historic temperature datasets, to use as a baseline for running Combo under different future climate scenarios and sets of assumptions. Results suggest a bleak future for coral reefs in the eastern Caribbean. For three different emissions scenarios from the Intergovernmental Panel on Climate Change (IPCC; B1, A1B, and A1FI), coral cover on most Caribbean reefs is projected to drop below 5% by the year 2035, if future mortality rates are equivalent to some of those observed in the 2005 event (50%). For a scenario where corals gain an additional 1–1.5°C of heat tolerance through a shift in the algae that live in the coral tissue, coral cover above 5% is prolonged until 2065. Additional impacts such as storms or anthropogenic damage could result in declines in coral cover even faster than those projected here. These results suggest the need to identify and preserve the locations that are likely to have a higher resiliency to bleaching to save as many remnant populations of corals as possible in the face of projected wide-spread coral loss.
Citation: R. W. Buddemeier, Diana R. Lane and J. A. Martinich, Climatic Change, DOI: 10.1007/s10584-011-0022-z. [full text]

Coral reefs may start dissolving when atmospheric CO₂ doubles – Silverman et al. (2009)
Abstract: Calcification rates in stony corals are expected to decline significantly in the near future due to ocean acidification. In this study we provide a global estimate of the decline in calcification of coral reefs as a result of increase in sea surface temperature and partial pressure of CO₂. This estimate, unlike previously reported estimates, is based on an empirical rate law developed from field observations for gross community calcification as a function of aragonite degree of saturation (Ω_arag), sea surface temperature and live coral cover. Calcification rates were calculated for more than 9,000 reef locations using model values of Ω_arag and sea surface temperature at different levels of atmospheric CO₂. The maps we produced show that by the time atmospheric partial pressure of CO₂ will reach 560 ppm all coral reefs will cease to grow and start to dissolve.
Citation: Silverman, J., B. Lazar, L. Cao, K. Caldeira, and J. Erez (2009), Geophys. Res. Lett., 36, L05606, doi:10.1029/2008GL036282. [full text]

Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook – Baker et al. (2008)
Abstract: Since the early 1980s, episodes of coral reef bleaching and mortality, due primarily to climate-induced ocean warming, have occurred almost annually in one or more of the world’s tropical or subtropical seas. Bleaching is episodic, with the most severe events typically accompanying coupled ocean–atmosphere phenomena, such as the El Niño-Southern Oscillation (ENSO), which result in sustained regional elevations of ocean temperature. Using this extended dataset (25+ years), we review the short- and long-term ecological impacts of coral bleaching on reef ecosystems, and quantitatively synthesize recovery data worldwide. Bleaching episodes have resulted in catastrophic loss of coral cover in some locations, and have changed coral community structure in many others, with a potentially critical influence on the maintenance of biodiversity in the marine tropics. Bleaching has also set the stage for other declines in reef health, such as increases in coral diseases, the breakdown of reef framework by bioeroders, and the loss of critical habitat for associated reef fishes and other biota. Secondary ecological effects, such as the concentration of predators on remnant surviving coral populations, have also accelerated the pace of decline in some areas. Although bleaching severity and recovery have been variable across all spatial scales, some reefs have experienced relatively rapid recovery from severe bleaching impacts. There has been a significant overall recovery of coral cover in the Indian Ocean, where many reefs were devastated by a single large bleaching event in 1998. In contrast, coral cover on western Atlantic reefs has generally continued to decline in response to multiple smaller bleaching events and a diverse set of chronic secondary stressors. No clear trends are apparent in the eastern Pacific, the central-southern-western Pacific or the Arabian Gulf, where some reefs are recovering and others are not. The majority of survivors and new recruits on regenerating and recovering coral reefs have originated from broadcast spawning taxa with a potential for asexual growth, relatively long distance dispersal, successful settlement, rapid growth and a capacity for framework construction. Whether or not affected reefs can continue to function as before will depend on: (1) how much coral cover is lost, and which species are locally extirpated; (2) the ability of remnant and recovering coral communities to adapt or acclimatize to higher temperatures and other climatic factors such as reductions in aragonite saturation state; (3) the changing balance between reef accumulation and bioerosion; and (4) our ability to maintain ecosystem resilience by restoring healthy levels of herbivory, macroalgal cover, and coral recruitment. Bleaching disturbances are likely to become a chronic stress in many reef areas in the coming decades, and coral communities, if they cannot recover quickly enough, are likely to be reduced to their most hardy or adaptable constituents. Some degraded reefs may already be approaching this ecological asymptote, although to date there have not been any global extinctions of individual coral species as a result of bleaching events. Since human populations inhabiting tropical coastal areas derive great value from coral reefs, the degradation of these ecosystems as a result of coral bleaching and its associated impacts is of considerable societal, as well as biological concern. Coral reef conservation strategies now recognize climate change as a principal threat, and are engaged in efforts to allocate conservation activity according to geographic-, taxonomic-, and habitat-specific priorities to maximize coral reef survival. Efforts to forecast and monitor bleaching, involving both remote sensed observations and coupled ocean–atmosphere climate models, are also underway. In addition to these efforts, attempts to minimize and mitigate bleaching impacts on reefs are immediately required. If significant reductions in greenhouse gas emissions can be achieved within the next two to three decades, maximizing coral survivorship during this time may be critical to ensuring healthy reefs can recover in the long term.
Citation: Andrew C. Baker, Peter W. Glynn, and Bernhard Riegl, Estuarine, Coastal and Shelf Science, Volume 80, Issue 4, 10 December 2008, Pages 435-471, doi:10.1016/j.ecss.2008.09.003. [full text]

Coral Reefs Under Rapid Climate Change and Ocean Acidification – Hoegh-Guldberg et al. (2007)
Abstract: Atmospheric carbon dioxide concentration is expected to exceed 500 parts per million and global temperatures to rise by at least 2°C by 2050 to 2100, values that significantly exceed those of at least the past 420,000 years during which most extant marine organisms evolved. Under conditions expected in the 21st century, global warming and ocean acidification will compromise carbonate accretion, with corals becoming increasingly rare on reef systems. The result will be less diverse reef communities and carbonate reef structures that fail to be maintained. Climate change also exacerbates local stresses from declining water quality and overexploitation of key species, driving reefs increasingly toward the tipping point for functional collapse. This review presents future scenarios for coral reefs that predict increasingly serious consequences for reef-associated fisheries, tourism, coastal protection, and people. As the International Year of the Reef 2008 begins, scaled-up management intervention and decisive action on global emissions are required if the loss of coral-dominated ecosystems is to be avoided.
Citation: O. Hoegh-Guldberg, P. J. Mumby, A. J. Hooten, R. S. Steneck, P. Greenfield, E. Gomez, C. D. Harvell, P. F. Sale, A. J. Edwards, K. Caldeira, N. Knowlton, C. M. Eakin, R. Iglesias-Prieto, N. Muthiga, R. H. Bradbury, A. Dubi and M. E. Hatziolos, Science 14 December 2007: Vol. 318 no. 5857 pp. 1737-1742, DOI: 10.1126/science.1152509. [full text]

Effects of climate and seawater temperature variation on coral bleaching and mortality – McClanahan et al. (2007)
Abstract: Coral bleaching due to thermal and environmental stress threatens coral reefs and possibly people who rely on their resources. Here we explore patterns of coral bleaching and mortality in East Africa in 1998 and 2005 in a region where the equatorial current and the island effect of Madagascar interact to create different thermal and physicochemical environments. A variety of temperature statistics were calculated, and their relationships with the degree-heating months (DHM), a good predictor of coral bleaching, determined. Changes in coral cover were analyzed from 29 sites that span >1000 km of coastline from Kenya to the Comoros Islands. Temperature patterns are influenced by the island effect, and there are three main temperature environments based on the rise in temperature over 52 years, measures of temperature variation, and DHM. Offshore sites north of Madagascar that included the Comoros had low temperature rises, low DHM, high standard deviations (SD), and the lowest relative coral mortality. Coastal sites in Kenya had moderate temperature rises, the lowest temperature SD, high DHM, and the highest relative coral mortality. Coastal sites in the south had the highest temperature rises, moderate SD and DHM, and low relative coral mortality. Consequently, the rate of temperature rise was less important than background variation, as reflected by SD and kurtosis measures of sea surface water temperature (SST), in predicting coral survival across 1998. Coral bleaching responses to a warm-water anomaly in 2005 were also negatively related to temperature variation, but positively correlated with the speed of water flow. Separating these effects is difficult; however, both factors will be associated with current environments on the opposite sides of reefs and islands. Reefs in current shadows may represent refugia where corals acclimate and adapt to environmental variation, which better prepares them for rising temperature and anomalies, even though these sites are likely to experience the fastest rates of temperature rise. We suggest that these sites are a conservation priority and should be targeted for management and further ecological research in order to understand acclimation, adaptation, and resilience to climate change.
Citation: McClanahan, Timothy R., Mebrahtu Ateweberhan, Christopher A. Muhando, Joseph Maina, and Mohammed S. Mohammed. 2007, Ecological Monographs 77:503–525, doi:10.1890/06-1182.1. [full text]

The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change – Berkelmans & van Oppen (2006)
Abstract: The ability of coral reefs to survive the projected increases in temperature due to global warming will depend largely on the ability of corals to adapt or acclimatize to increased temperature extremes over the next few decades. Many coral species are highly sensitive to temperature stress and the number of stress (bleaching) episodes has increased in recent decades. We investigated the acclimatization potential of Acropora millepora, a common and widespread Indo-Pacific hard coral species, through transplantation and experimental manipulation. We show that adult corals, at least in some circumstances, are capable of acquiring increased thermal tolerance and that the increased tolerance is a direct result of a change in the symbiont type dominating their tissues from Symbiodinium type C to D. Our data suggest that the change in symbiont type in our experiment was due to a shuffling of existing types already present in coral tissues, not through exogenous uptake from the environment. The level of increased tolerance gained by the corals changing their dominant symbiont type to D (the most thermally resistant type known) is around 1–1.5 °C. This is the first study to show that thermal acclimatization is causally related to symbiont type and provides new insight into the ecological advantage of corals harbouring mixed algal populations. While this increase is of huge ecological significance for many coral species, in the absence of other mechanisms of thermal acclimatization/adaptation, it may not be sufficient to survive climate change under predicted sea surface temperature scenarios over the next 100 years. However, it may be enough to ‘buy time’ while greenhouse reduction measures are put in place.
Citation: Ray Berkelmans and Madeleine J.H van Oppen, Proc. R. Soc. B 22 September 2006 vol. 273 no. 1599 2305-2312, doi: 10.1098/rspb.2006.3567. [full text]

Global assessment of coral bleaching and required rates of adaptation under climate change – Donner et al. (2005)
Abstract: Elevated ocean temperatures can cause coral bleaching, the loss of colour from reef-building corals because of a breakdown of the symbiosis with the dinoflagellate Symbiodinium. Recent studies have warned that global climate change could increase the frequency of coral bleaching and threaten the long-term viability of coral reefs. These assertions are based on projecting the coarse output from atmosphere–ocean general circulation models (GCMs) to the local conditions around representative coral reefs. Here, we conduct the first comprehensive global assessment of coral bleaching under climate change by adapting the NOAA Coral Reef Watch bleaching prediction method to the output of a low- and high-climate sensitivity GCM. First, we develop and test algorithms for predicting mass coral bleaching with GCM-resolution sea surface temperatures for thousands of coral reefs, using a global coral reef map and 1985–2002 bleaching prediction data. We then use the algorithms to determine the frequency of coral bleaching and required thermal adaptation by corals and their endosymbionts under two different emissions scenarios. The results indicate that bleaching could become an annual or biannual event for the vast majority of the world’s coral reefs in the next 30–50 years without an increase in thermal tolerance of 0.2–1.0°C per decade. The geographic variability in required thermal adaptation found in each model and emissions scenario suggests that coral reefs in some regions, like Micronesia and western Polynesia, may be particularly vulnerable to climate change. Advances in modelling and monitoring will refine the forecast for individual reefs, but this assessment concludes that the global prognosis is unlikely to change without an accelerated effort to stabilize atmospheric greenhouse gas concentrations.
Citation: Simon D. Donner, William J. Skirving, Christopher M. Little, Michael Oppenheimer, Ove Hoegh-Guldberg, Global Change Biology, Volume 11, Issue 12, pages 2251–2265, December 2005. [full text]

Coral reefs: Corals’ adaptive response to climate change – Baker et al. (2004)
Abstract: The long-term response of coral reefs to climate change depends on the ability of reef-building coral symbioses to adapt or acclimatize to warmer temperatures, but there has been no direct evidence that such a response can occur. Here we show that corals containing unusual algal symbionts that are thermally tolerant and commonly associated with high-temperature environments are much more abundant on reefs that have been severely affected by recent climate change. This adaptive shift in symbiont communities indicates that these devastated reefs could be more resistant to future thermal stress, resulting in significantly longer extinction times for surviving corals than had been previously assumed.
Citation: Andrew C. Baker, Craig J. Starger, Tim R. McClanahan & Peter W. Glynn, Nature 430, 741 (12 August 2004) | doi:10.1038/430741a. [full text]

Coral reef calcification and climate change: The effect of ocean warming – McNeil et al. (2004)
Abstract: Coral reefs are constructed of calcium carbonate (CaCO₃). Deposition of CaCO₃ (calcification) by corals and other reef organisms is controlled by the saturation state of CaCO₃ in seawater (Ω) and sea surface temperature (SST). Previous studies have neglected the effects of ocean warming in predicting future coral reef calcification rates. In this study we take into account both these effects by combining empirical relationships between coral calcification rate and Ω and SST with output from a climate model to predict changes in coral reef calcification rates. Our analysis suggests that annual average coral reef calcification rate will increase with future ocean warming and eventually exceed pre-industrial rates by about 35% by 2100. Our results suggest that present coral reef calcification rates are equivalent to levels in the late 19th century and does not support previous suggestions of large and potentially catastrophic decreases in the future.
Citation: McNeil, B. I., R. J. Matear, and D. J. Barnes (2004), Geophys. Res. Lett., 31, L22309, doi:10.1029/2004GL021541. [full text, comment by Kleypas et al., reply by McNeil et al.]

Global Trajectories of the Long-Term Decline of Coral Reef Ecosystems – Pandolfi et al. (2003)
Abstract: Degradation of coral reef ecosystems began centuries ago, but there is no global summary of the magnitude of change. We compiled records, extending back thousands of years, of the status and trends of seven major guilds of carnivores, herbivores, and architectural species from 14 regions. Large animals declined before small animals and architectural species, and Atlantic reefs declined before reefs in the Red Sea and Australia, but the trajectories of decline were markedly similar worldwide. All reefs were substantially degraded long before outbreaks of coral disease and bleaching. Regardless of these new threats, reefs will not survive without immediate protection from human exploitation over large spatial scales.
Citation: John M. Pandolfi, Roger H. Bradbury, Enric Sala, Terence P. Hughes, Karen A. Bjorndal, Richard G. Cooke, Deborah McArdle, Loren McClenachan, Marah J. H. Newman, Gustavo Paredes, Robert R. Warner and Jeremy B. C. Jackson, Science 15 August 2003: Vol. 301 no. 5635 pp. 955-958, DOI: 10.1126/science.1085706.

Climate Change, Human Impacts, and the Resilience of Coral Reefs – Hughes et al. (2003)
Abstract: The diversity, frequency, and scale of human impacts on coral reefs are increasing to the extent that reefs are threatened globally. Projected increases in carbon dioxide and temperature over the next 50 years exceed the conditions under which coral reefs have flourished over the past half-million years. However, reefs will change rather than disappear entirely, with some species already showing far greater tolerance to climate change and coral bleaching than others. International integration of management strategies that support reef resilience need to be vigorously implemented, and complemented by strong policy decisions to reduce the rate of global warming.
Citation: T. P. Hughes, A. H. Baird, D. R. Bellwood, M. Card, S. R. Connolly, C. Folke, R. Grosberg, O. Hoegh-Guldberg, J. B. C. Jackson, J. Kleypas, J. M. Lough, P. Marshall, M. Nyström, S. R. Palumbi, J. M. Pandolfi, B. Rosen and J. Roughgarden, Science 15 August 2003: Vol. 301 no. 5635 pp. 929-933, DOI: 10.1126/science.1085046. [full text]

Microbial diseases of corals and global warming – Rosenberg & Haim (2002)
Abstract: Coral bleaching and other diseases of corals have increased dramatically during the last few decades. As outbreaks of these diseases are highly correlated with increased sea-water temperature, one of the consequences of global warming will probably be mass destruction of coral reefs. The causative agent(s) of a few of these diseases have been reported: bleaching of Oculina patagonica by Vibrio shiloi; black band disease by a microbial consortium; sea-fan disease (aspergillosis) by Aspergillus sydowii; and coral white plague possibly by Sphingomonas sp. In addition, we have recently discovered that Vibrio coralyticus is the aetiological agent for bleaching the coral Pocillopora damicornis in the Red Sea. In the case of coral bleaching by V. shiloi, the major effect of increasing temperature is the expression of virulence genes by the pathogen. At high summer sea-water temperatures, V. shiloi produces an adhesin that allows it to adhere to a β-galactoside-containing receptor in the coral mucus, penetrate into the coral epidermis, multiply intracellularly, differentiate into a viable-but-not-culturable (VBNC) state and produce toxins that inhibit photosynthesis and lyse the symbiotic zooxanthellae. In black band disease, sulphide is produced at the coral–microbial biofilm interface, which is probably responsible for tissue death. Reports of newly emerging coral diseases and the lack of epidemiological and biochemical information on the known diseases indicate that this will become a fertile area of research in the interface between microbial ecology and infectious disease.
Citation: Eugene Rosenberg, Yael Ben-Haim, Environmental Microbiology, Volume 4, Issue 6, pages 318–326, June 2002, DOI: 10.1046/j.1462-2920.2002.00302.x. [full text]

The future of coral reefs – Knowlton (2001)
Abstract: Coral reefs, with their millions of species, have changed profoundly because of the effects of people, and will continue to do so for the foreseeable future. Reefs are subject to many of the same processes that affect other human-dominated ecosystems, but some special features merit emphasis: (i) Many dominant reef builders spawn eggs and sperm into the water column, where fertilization occurs. They are thus particularly vulnerable to Allee effects, including potential extinction associated with chronic reproductive failure. (ii) The corals likely to be most resistant to the effects of habitat degradation are small, short-lived “weedy” corals that have limited dispersal capabilities at the larval stage. Habitat degradation, together with habitat fragmentation, will therefore lead to the establishment of genetically isolated clusters of inbreeding corals. (iii) Increases in average sea temperatures by as little as 1°C, a likely result of global climate change, can cause coral “bleaching” (the breakdown of coral–algal symbiosis), changes in symbiont communities, and coral death. (iv) The activities of people near reefs increase both fishing pressure and nutrient inputs. In general, these processes favor more rapidly growing competitors, often fleshy seaweeds, and may also result in explosions of predator populations. (v) Combinations of stress appear to be associated with threshold responses and ecological surprises, including devastating pathogen outbreaks. (vi) The fossil record suggests that corals as a group are more likely to suffer extinctions than some of the groups that associate with them, whose habitat requirements may be less stringent.
Citation: Nancy Knowlton, PNAS May 8, 2001 vol. 98 no. 10 5419-5425, doi: 10.1073/pnas.091092998. [full text]

Coral bleaching: the winners and the losers – Loya et al. (2001)
Abstract: Sea surface temperatures were warmer throughout 1998 at Sesoko Island, Japan, than in the 10 preceding years. Temperatures peaked at 2.8 °C above average, resulting in extensive coral bleaching and subsequent coral mortality. Using random quadrat surveys, we quantitatively documented the coral community structure one year before and one year after the bleaching event. The 1998 bleaching event reduced coral species richness by 61% and reduced coral cover by 85%. Colony morphology affected bleaching vulnerability and subsequent coral mortality. Finely branched corals were most susceptible, while massive and encrusting colonies survived. Most heavily impacted were the branched Acropora and pocilloporid corals, some of which showed local extinction. We suggest two hypotheses whose synergistic effect may partially explain observed mortality patterns (i.e. preferential survival of thick-tissued species, and shape-dependent differences in colony mass-transfer efficiency). A community-structural shift occurred on Okinawan reefs, resulting in an increase in the relative abundance of massive and encrusting coral species.
Citation: Loya, Sakai, Yamazato, Nakano, Sambali, Van Woesik, Ecology Letters, Volume 4, Issue 2, pages 122–131, March 2001, DOI: 10.1046/j.1461-0248.2001.00203.x.

Climate change, coral bleaching and the future of the world’s coral reefs – Hoegh-Guldberg (1999)
Abstract: Sea temperatures in many tropical regions have increased by almost 1°C over the past 100 years, and are currently increasing at ~1–2°C per century. Coral bleaching occurs when the thermal tolerance of corals and their photosynthetic symbionts (zooxanthellae) is exceeded. Mass coral bleaching has occurred in association with episodes of elevated sea temperatures over the past 20 years and involves the loss of the zooxanthellae following chronic photoinhibition. Mass bleaching has resulted in significant losses of live coral in many parts of the world. This paper considers the biochemical, physiological and ecological perspectives of coral bleaching. It also uses the outputs of four runs from three models of global climate change which simulate changes in sea temperature and hence how the frequency and intensity of bleaching events will change over the next 100 years. The results suggest that the thermal tolerances of reef-building corals are likely to be exceeded every year within the next few decades. Events as severe as the 1998 event, the worst on record, are likely to become commonplace within 20 years. Most information suggests that the capacity for acclimation by corals has already been exceeded, and that adaptation will be too slow to avert a decline in the quality of the world’s reefs. The rapidity of the changes that are predicted indicates a major problem for tropical marine ecosystems and suggests that unrestrained warming cannot occur without the loss and degradation of coral reefs on a global scale.
Citation: Ove Hoegh-Guldberg, Marine and Freshwater Research 50(8) 839 – 866, doi:10.1071/MF99078. [full text]

The Significance of Emerging Diseases in the Tropical Coral Reef Ecosystem – Hayes & Goreau (1998)
Abstract: Novel pathologies of coral reef organisms, especially reef frame building scleractinian corals, have escalated during the decade between 1987 and 1997. These emerging diseases have appeared with progressively greater frequency and over wider distribution, and have revealed more diversified characteristics than ever before. The causes of most of these infections are not yet confirmed, but they evidence a gradual decline in the vital status of the coral reef ecosystem. As specific causes are identified for these afflictions, terminology will shift from non-specific descriptions, such as “white band”, “white plague”, “white pox”, “yellow band” and “black band” diseases, to etiological and pathognomonic characterizations (e.g. aspergillosis and cyanobacteriosis). Stony corals are vulnerable to sedimentation, nutrient overloading, and chemical pollution from agricultural, urban, and domestic sources. They are incapable of relocation to other sites or of self-protection from cumulative effects of exposure to nitrates, phosphates, herbicides, pesticides, and raw sewage. In contrast to stresses attributed to warm water seasonal anomalies (e.g. coral reef bleaching), stresses imparted by pathogenic micro-organisms occur throughout the calendar year, fluctuate with changing temperature, and invariably result in tissue mortality. The coral has several mechanisms for defense. The epidermis, especially in tentacles of the coral polyp, contains nematocysts which are released in response to predators. The epidermal cells also possess cilia and a flagellary apparatus which are responsible for generating microcurrents in boundary water adjacent to the organism. These currents facilitate the entry of food into the coelenteron for digestion. Mesenterial filaments extend through the epidermis, sweep the surface of the colony, initiate digestion of food particles, and eventually return to the coelenteron. Both the epidermis and the gastrodermis contain mucocytes (or “immunocytes”) which release a mucous secretion. That mucous blanket physically insulates the tissue from particulates or soluble toxins, and may also be bacteriostatic because of immunoglobulin (IgA). The recent emergence of diseases in corals may be interpreted as the consequence of (1) changing coastal ocean water quality favoring the proliferation, attachment and colonization of microbes, and (2) reduced efficiency of the coral’s normal defenses. In order to appreciate these changes, research efforts to evaluate the microbial content of reef waters and to analyze the respective roles of mucus, cilia and flagella, and nematocysts of the corals are necessary. In this study, we have begun to detail the structural, physiological, chemical, and immunological attributes of the coral. Our analysis suggests that at least some of the emerging coral diseases may be explained by a decline in the capacity of coral colonies to mount effective protection against the increasing prevalence and varied invasive strategies of marine pathogens.
Citation: Raymond L. Hayes and Nora I. Goreau, Revista Biol Trop 46: 173–185. [full text is available in the abstract page]

Coral bleaching: causes and consequences – Brown (1997)
Abstract: It has been over 10 years since the phenomenon of extensive coral bleaching was first described. In most cases bleaching has been attributed to elevated temperature, but other instances involving high solar irradiance, and sometimes disease, have also been documented. It is timely, in view of our concern about worldwide reef condition, to review knowledge of physical and biological factors involved in bleaching, the mechanisms of zooxanthellae and pigment loss, and the ecological consequences for coral communities. Here we evaluate recently acquired data on temperature and irradiance-induced bleaching, including long-term data sets which suggest that repeated bleaching events may be the consequence of a steadily rising background sea temperature that will in the future expose corals to an increasingly hostile environment. Cellular mechanisms of bleaching involve a variety of processes that include the degeneration of zooxanthellae in situ, release of zooxanthellae from mesenterial filaments and release of algae within host cells which become detached from the endoderm. Photo-protective defences (particularly carotenoid pigments) in zooxanthellae are likely to play an important role in limiting the bleaching response which is probably elicited by a combination of elevated temperature and irradiance in the field. The ability of corals to respond adaptively to recurrent bleaching episodes is not known, but preliminary evidence suggests that phenotypic responses of both corals and zooxanthellae may be significant.
Citation: B. E. Brown, Coral Reefs, Volume 16, Supplement 1, S129-S138, DOI: 10.1007/s003380050249. [full text]

Tracking South Pacific Coral Reef Bleaching by Satellite and Field Observations – Goreau et al. (1997)
Abstract: South Pacific waters with anomalously high surface temperature were tracked by satellite to identify potential sites for field study of coral reef bleaching. Areas with warm season monthly anomalies exceeding +0.9 degrees C were verified to have coral bleaching by local observers, while other areas were not affected. Comparison of 15 environmental variables, measured at 19 field sites across the area affected in 1994, shows that bleaching correlates significantly only with anomalously high temperature. Live coral cover was inversely correlated with many human population density-dependent stresses, but these were not correlated to bleaching. Observations in the Indian and Atlantic Oceans also show that coral reefs worldwide are acclimated close to their upper temperature limits and probably unable to adapt rapidly to a +1 degree C anomalous warming during the warm season.
Citation: T. J. Goreau, R. L. Hayes, and A. E. Strong, Proceedings of the 8th International Coral Reef Symposium 2:1491-1494, 1997. [full text is available in the abstract page]

Coral reef bleaching: facts, hypotheses and implications – Glynn (1996)
Abstract: Coral reef bleaching, the temporary or permanent loss of photosynthetic microalgae (zooxanthellae) and/or their pigments by a variety of reef taxa, is a stress response usually associated with anthropogenic and natural disturbances. Degrees of bleaching, within and among coral colonies and across reef communities, are highly variable and difficult to quantify, thus complicating comparisons of different bleaching events. Small-scale bleaching events can often be correlated with specific disturbances (e.g. extreme low/high temperatures, low/high solar irradiance, subaerial exposure, sedimentation, freshwater dilution, contaminants, and diseases), whereas large scale (mass) bleaching occurs over 100s to 1000s of km2, which is more difficult to explain. Debilitating effects of bleaching include reduced/no skeletal growth and reproductive activity, and a lowered capacity to shed sediments, resist invasion of competing species and diseases. Severe and prolonged bleaching can cause partial to total colony death, resulting in diminished reef growth, the transformation of reef-building communities to alternate, non-reef building community types, bioerosion and ultimately the disappearance of reef structures. Present evidence suggests that the leading factors responsible for large-scale coral reef bleaching are elevated sea temperatures and high solar irradiance (especially ultraviolet wavelengths), which may frequently act jointly.
Citation: Glynn, P. W. (1996), Coral reef bleaching: facts, hypotheses and implications. Global Change Biology, 2: 495–509. doi:10.1111/j.1365-2486.1996.tb00063.x.

Coral bleaching relative to elevated seawater temperature in the Andaman Sea (Indian Ocean) over the last 50 years – Brown et al. (1996)
No abstract.
Citation: B. E. Brown, R. P. Dunne and H. Chansang, Coral Reefs, Volume 15, Number 3, 151-152, DOI: 10.1007/BF01145885.

Periodic mass-bleaching and elevated sea temperatures: bleaching of outer reef slope communities in Moorea, French Polynesia – Hoegh-Guldberg & Salvat (1995)
Abstract: Mass-bleaching events (in which corals and other symbiotic invertebrates lose their zooxanthellae) have been occurring every 3 to 4 yr since 1979. The last report of widespread mass-bleaching in the Pacific (which included bleaching around French Polynesia) was in February-April 1991. This paper reports on mass-bleaching along the outer reef slope of Moorea, French Polynesia, in April 1994. Mass-bleaching was extensive at all sites visited, with corals being bleached down to 25 m. Colour loss by corals was due to low areal densities of zooxanthellae and the percentage of live coral affected ranged between 39.6 (+/- 7.12, SEM) (NW sites) and 72.4 (+/- 7.11, SEM) (NE sites). Bleaching also varied as a function of depth and included a wide range of species. Acropora spp. showed the most severe bleaching (89.0 to 100% of all colonies completely bleached) and Porites spp. showed the least amount of bleaching (12.9 to 42.5% of all colonies partly bleached). Pocillopora spp. showed intermediate bleaching (73.9 to 92.1% of all colonies either partly or completely bleached). The results of this report indicate that current bleaching is on a scale equal to that of the 1991 bleaching event. Temperatures recorded hourly at 14 m off the outer reef slope from July 1991 to August 1994 (and those from satellite sea surface temperature readings) indicate unusually warm sea temperatures in March 1994, which were approximately 1.0*C higher than the highest temperatures recorded in 1992 and 1993, years in which bleaching on a massive scale did not occur. The appearance of warmer temperatures preceded the onset of bleaching by 2 to 3 wk, which strongly confirms the hypothesis that positive thermal anomalies are responsible for recent bleaching events in the Central and Western Pacific.
Citation: Hoegh-Guldberg O, Salvat B, MEPS 121:181-190 (1995), doi:10.3354/meps121181.

Catastrophes, Phase Shifts, and Large-Scale Degradation of a Caribbean Coral Reef – Hughes (1994)
Abstract: Many coral reefs have been degraded over the past two to three decades through a combination of human and natural disturbances. In Jamaica, the effects of overfishing, hurricane damage, and disease have combined to destroy most corals, whose abundance has declined from more than 50 percent in the late 1970s to less than 5 percent today. A dramatic phase shift has occurred, producing a system dominated by fleshy macroalgae (more than 90 percent cover). Immediate implementation of management procedures is necessary to avoid further catastrophic damage.
Citation: Terence P. Hughes, Science 9 September 1994: Vol. 265 no. 5178 pp. 1547-1551, DOI: 10.1126/science.265.5178.1547. [full text]

1994 coral bleaching event, Society Islands, French Polynesia – Fagerstom & Rougerie (1994)
Abstract: The progression of a temperature-induced bleaching event on the barrier reef at Passe d’Arue, Tahiti, during March–April 1994 was observed at approximately weekly intervals. The event consisted of selective exaggeration of polyp colours (Montipora verneuilli, Pocillopora verrucosa), fluorescence followed by bleaching (Acropora spp.), partial-complete bleaching (Fungia spp., Montastraea curta, anemones) and commencement of polyp death. Porites (massive spp.), P. (Synarea) rus and melobesoid algae were almost untouched by the event.
Citation: J.A. Fagerstrom and F. Rougerie, Marine Pollution Bulletin, Volume 29, Issues 1-3, 1994, Pages 34-35, doi:10.1016/0025-326X(94)90423-5. [full text]

Coral reef bleaching: ecological perspectives – Glynn (1993)
Abstract: Coral reef bleaching, the whitening of diverse invertebrate taxa, results from the loss of symbiotic zooxanthellae and/or a reduction in photosynthetic pigment concentrations in zooxanthellae residing within the gastrodermal tissues of host animals. Of particular concern are the consequences of bleaching of large numbers of reef-building scleractinian corals and hydrocorals. Published records of coral reef bleaching events from 1870 to the present suggest that the frequency (60 major events from 1979 to 1990), scale (co-occurrence in many coral reef regions and often over the bathymetric depth range of corals) and severity (>95% mortality in some areas) of recent bleaching disturbances are unprecedented in the scientific literature. The causes of small scale, isolated bleaching events can often be explained by particular stressors (e.g., temperature, salinity, light, sedimentation, aerial exposure and pollutants), but attempts to explain large scale bleaching events in terms of possible global change (e.g., greenhouse warming, increased UV radiation flux, deteriorating ecosystem health, or some combination of the above) have not been convincing. Attempts to relate the severity and extent of large scale coral reef bleaching events to particular causes have been hampered by a lack of (a) standardized methods to assess bleaching and (b) continuous, long-term data bases of environmental conditions over the periods of interest. An effort must be made to understand the impact of bleaching on the remainder of the reef community and the long-term effects on competition, predation, symbioses, bioerosion and substrate condition, all factors that can influence coral recruitment and reef recovery. If projected rates of sea warming are realized by mid to late AD 2000, i.e. a 2°C increase in high latitude coral seas, the upper thermal tolerance limits of many reef-building corals could be exceeded. Present evidence suggests that many corals would be unable to adapt physiologically or genetically to such marked and rapid temperature increases.
Citation: P. W. Glynn, Coral Reefs, Volume 12, Number 1, 1-17, DOI: 10.1007/BF00303779.

Effects of disturbance on coral communities: bleaching in Moorea, French Polynesia – Gleason (1993)
Abstract: This study examines patterns of susceptibility and short-term recovery of corals from bleaching. A mass coral bleaching event began in March, 1991 on reefs in Moorea, French Polynesia and affected corals on the shallow barrier reef and to >20 m depth on the outer forereef slope. There were significant differences in the effect of the bleaching among common coral genera, with Acropora, Montastrea, Montipora, and Pocillopora more affected than Porites, Pavona, leptastrea or Millepora. Individual colonies of the common species of Acropora and Pocillopora were marked and their fate assessed on a subsequent survey in August, 1991 to determine rates of recovery and mortality. Ninety-six percent of Acropora spp. showed some degree of bleaching compared to 76% of Pocillopora spp. From March to August mortality of bleached colonies of Pocillopora was 17%, 38% recovered completely, and many suffered some partial mortality of the tissue. In contrast, 63% of the Acropora spp. died, and about 10% recovered completely. Generally, those colonies with less than 50% of the colony area affected by the bleaching recovered at a higher rate than did those with more severe bleaching. Changes in community composition four months after the event began included a significant decrease only in crustose algae and an increase in cover of filamentous algae, much of which occupied plate-like and branching corals that had died in the bleaching event. Total coral cover and cover of susceptible coral genera had declined, but not significantly, after the event.
Citation: M. G. Gleason, Coral Reefs, Volume 12, Numbers 3-4, 193-201, DOI: 10.1007/BF00334479.

Ultraviolet radiation and coral bleaching – Gleason & Wellington (1993)
Abstract: EPISODES of coral bleaching resulting from dissociation of endosymbiotic algae (zooxanthellae) from host coral tissues have occurred with increasing frequency over the past decade on reefs throughout the tropics. These episodes have usually been attributed to increases in sea water temperatures, but the mass bleaching events that occurred throughout the Caribbean during 1987 and 1990 were not readily explained by temperature alone. An additional factor that may have contributed to these bleaching episodes is ultraviolet radiation in the 280–400-nm band. At many localities where bleaching occurred in 1987 and 1990, sea conditions were described as extremely calm with exceptionally clear water. In the absence of suspended organic and inorganic matter in the water column, higher than average intensities of ultraviolet radiation probably reached all depths within the photic zone for several consecutive months. Evidence for a possible link between ultraviolet radiation and coral bleaching has not been forthcoming2. Here we report results of a field experiment showing that, irrespective of high water temperatures, short-term (three weeks) increases in ultraviolet radiation of a magnitude possible under calm, clear water column conditions can readily induce bleaching in reef-building corals.
Citation: Daniel F. Gleason & Gerard M. Wellington, Nature 365, 836 – 838 (28 October 1993); doi:10.1038/365836a0.

An Assessment of Global Warming Stress on Caribbean Coral Reef Ecosystems – Atwood et al. (1992)
Abstract: There is evidence that stress on coral reef ecosystems in the Caribbean region is increasing. Recently numerous authors have stated that the major stress results from “abnormally high” seasonal sea surface temperatures (SST) and have implicated global warming as a cause, stating that recent episodes of coral bleaching result therefrom. However, an analysis of available SST data sets shows no discernible warming trend that could cause an increase in coral bleaching. Given the lack of long-term records synoptic with observations of coral ecosystem health, there is insufficient evidence available to label temperatures observed in coincidence with recent regional bleaching events as “abnormally” high.
Citation: Atwood, Donald K.; Hendee, James C.; Mendez, Antonio, Bulletin of Marine Science, Volume 51, Number 1, July 1992 , pp. 118-130(13).

Coral reef bleaching in the 1980s and possible connections with global warming – Glynn (1991)
Abstract: Scleractinian corals and their symbiotic dinoflagellate algae build massive, wave-resistant coral reefs that are pre-eminent in shallow tropical seas. This mutualism is especially sensitive to numerous environmental stresses, and has been disrupted frequently during the past decade. Increased seawater temperatures have been proposed as the most likely cause of coral reef bleaching, and it has been suggested that the recent large-scale disturbances are the first biological indication of global warming. This article describes recent bleaching events and their possible link with sea warming and other environmental stresses, and offers some speculation on the fate of coral reefs if the Earth enters a sustained period of warming.
Citation: Peter W. Glynn, Trends in Ecology & Evolution, Volume 6, Issue 6, June 1991, Pages 175-179, doi:10.1016/0169-5347(91)90208-F.

Damage and recovery of coral reefs affected by El Niño related seawater warming in the Thousand Islands, Indonesia – Brown & Suharsono (1990)
Abstract: Extensive coral bleaching occurred during sea-water warming (as a result of the 1982/3 El Niño Southern Oscillation event) in 1983 on the shallow reefs in the Java Sea. Mean seawater temperatures rose by 2–3° C over a six month period with values greater than 33° C being recorded between 1200–1500 h. As many as 80–90% of corals died on the reef flats at the study sites, with the major casualties being branching species in the genera Acropora and Pocillopora. Five years after the event the community structure of the study sites has recovered significantly, though coral cover is still 50% of its former level. Contrasting patterns of recovery at two selected sites, in close proximity to each other, are discussed.
Citation: B. E. Brown and Suharsono, Coral Reefs, Volume 8, Number 4, 163-170, DOI: 10.1007/BF00265007.

Widespread Coral Mortality and the 1982–83 El Niño Warming Event – Glynn (1984)
Abstract: The massive ‘bleaching’ (loss of zooxanthellae) and death of reef corals that occurred in one area (Gulf of Chiriquí) on the Pacific side of Panamá and in the Galápagos Islands during February—April 1983 continued in these areas until September—October 1983, resulting in a catastrophic disturbance. Similar episodes have been reported subsequently throughout much of the tropical eastern Pacific region (Costa Rica, the entire Pacific coast of Panamá, and Colombia), in the central and western Pacific Ocean, in parts of the western Atlantic Ocean (Caribbean coasts of Costa Rica, Panamá, and Colombia), and in the Florida Keys and Bahama Islands.
Citation: Peter W. Glynn, Environmental Conservation (1984), 11: 133-146, DOI: 10.1017/S0376892900013825.