Bacteria Associated with the Bleached and Cave Coral Oculina patagonica

The relative abundance of bacteria in the mucus and tissues of Oculina patagonica taken from bleached and cave (azooxanthellae) corals was determined by analyses of the 16S rRNA genes from cloned libraries of extracted DNA and from isolated colonies. The results were compared to previously published data on healthy O. patagonica. The bacterial community of bleached, cave, and healthy corals were completely different from each other. A tight cluster (>99.5% identity) of bacteria, showing 100% identity to Acinetobacter species, dominated bleached corals, comprising 25% of the 316 clones sequenced. The dominant bacterial cluster found in cave corals, representing 29% of the 97 clones sequenced, showed 98% identity to an uncultured bacterium from the Great Barrier Reef. Vibrio splendidus was the most dominant species in healthy O. patagonica. The culturable bacteria represented 0.1–1.0% of the total bacteria (SYBR Gold staining) of the corals. The most abundant culturable bacteria in bleached, cave, and healthy corals were clusters that most closely matched Microbulbifer sp., an α-proteobacterium previously isolated from healthy corals and an α-protobacterium (AB026194), respectively. Three generalizations emerge from this study on O. patagonica: (1) More bacteria are associated with coral tissue than mucus; (2) tissue and mucus populations are different; (3) bacterial populations associated with corals change dramatically when corals lack their symbiotic zooxanthellae, either as a result of the bleaching disease or when growing in the absence of light.     

Cellular processes of bleaching in the Mediterranean coral Oculina patagonica

Annual bleaching of Oculina patagonica on the Israeli Mediterranean coastline has been reported since 1993, although the cellular mechanisms underlying the bleaching have not yet been investigated. This survey examined 48 coral colonies of O. patagonica (bleached and unbleached) from various sites along the Israeli coast. Histopathological investigations of bleached lesions revealed a loss of endosymbionts, and an apparent in situ degradation of the endosymbionts. In situ end labelling of bleaching lesions did not provide evidence of apoptotic cell death. Electron microscopy of bleaching lesions also demonstrated an apparent in situ degradation and no evidence of apoptotic cell death of the host.     

Bleached Porites compressa and Montipora capitata corals catabolize ��13C-enriched lipids

Corals rely on stored energy reserves (i.e., lipids, carbohydrates, and protein) to survive bleaching events. To better understand the physiological implications of coral bleaching on lipid catabolism and/or synthesis, we measured the δ¹³C of coral total lipids (δ¹³C_TL) in experimentally bleached (treatment) and non-bleached (control) Porites compressa and Montipora capitata corals immediately after bleaching and after 1.5 and 4 months of recovery on the reef. Overall δ¹³C_TL values in treatment corals were significantly lower than in control corals because of a 1.9 and 3.4‰ decrease in δ¹³C_TL immediately after bleaching in P. compressa and M. capitata, respectively. The decrease in δ¹³C_TL coincided with decreases in total lipid concentration, indicating that corals catabolized δ¹³C-enriched lipids. Since storage lipids are primarily depleted during bleaching, we hypothesize that they are isotopically enriched relative to other lipid classes. This work further helps clarify our understanding of changes to coral metabolism and biogeochemistry when bleached and helps elucidate how lipid classes may influence recovery from bleaching and ultimately coral survival.     

Coral-associated nitrogen fixation rates and diazotrophic diversity on a nutrient-replete equatorial reef

The role of diazotrophs in coral physiology and reef biogeochemistry remains poorly understood, in part because N₂ fixation rates and diazotrophic community composition have only been jointly analyzed in the tissue of one tropical coral species. We performed field-based ¹⁵N₂ tracer incubations during nutrient-replete conditions to measure diazotroph-derived nitrogen (DDN) assimilation into three species of scleractinian coral (Pocillopora acuta, Goniopora columna, Platygyra sinensis). Using multi-marker metabarcoding (16S rRNA, nifH, 18S rRNA), we analyzed DNA- and RNA-based communities in coral tissue and skeleton. Despite low N₂ fixation rates, DDN assimilation supplied up to 6% of the holobiont’s N demand. Active coral-associated diazotrophs were chiefly Cluster I (aerobes or facultative anaerobes), suggesting that oxygen may control coral-associated diazotrophy. Highest N₂ fixation rates were observed in the endolithic community (0.20 µg N cm⁻² per day). While the diazotrophic community was similar between the tissue and skeleton, RNA:DNA ratios indicate potential differences in relative diazotrophic activity between these compartments. In Pocillopora, DDN was found in endolithic, host, and symbiont compartments, while diazotrophic nifH sequences were only observed in the endolithic layer, suggesting a possible DDN exchange between the endolithic community and the overlying coral tissue. Our findings demonstrate that coral-associated diazotrophy is significant, even in nutrient-rich waters, and suggest that endolithic microbes are major contributors to coral nitrogen cycling on reefs.Subject terms: Microbial ecology, Biogeochemistry, Stable isotope analysis     

New insights into Oculina patagonica coral diseases and their associated Vibrio spp. communities

Bleaching of Oculina patagonica has been extensively studied in the Eastern Mediterranean Sea, although no studies have been carried out in the Western basin. In 1996 Vibrio mediterranei was reported as the causative agent of bleaching in O. patagonica but it has not been related to bleached or healthy corals since 2003, suggesting that it was no longer involved in bleaching of O. patagonica. In an attempt to clarify the relationship between Vibrio spp., seawater temperature and coral diseases, as well as to investigate the putative differences between Eastern and Western Mediterranean basins, we have analysed the seasonal patterns of the culturable Vibrio spp. assemblages associated with healthy and diseased O. patagonica colonies. Two sampling points located in the Spanish Mediterranean coast were chosen for this study: Alicante Harbour and the Marine Reserve of Tabarca. A complex and dynamic assemblage of Vibrio spp. was present in O. patagonica along the whole year and under different environmental conditions and coral health status. While some Vibrio spp. were detected all year around in corals, the known pathogens V. mediteranei and V. coralliilyticus were only present in diseased specimens. The pathogenic potential of these bacteria was studied by experimental infection under laboratory conditions. Both vibrios caused diseased signs from 24 °C, being higher and faster at 28 °C. Unexpectedly, the co-inoculation of these two Vibrio species seemed to have a synergistic pathogenic effect over O. patagonica, as disease signs were readily observed at temperatures at which bleaching is not normally observed.     

Can heterotrophic uptake of dissolved organic carbon and zooplankton mitigate carbon budget deficits in annually bleached corals?

Annual coral bleaching events due to increasing sea surface temperatures are predicted to occur globally by the mid-century and as early as 2025 in the Caribbean, and severely impact coral reefs. We hypothesize that heterotrophic carbon (C) in the form of zooplankton and dissolved organic carbon (DOC) is a significant source of C to bleached corals. Thus, the ability to utilize multiple pools of fixed carbon and/or increase the amount of fixed carbon acquired from one or more pools of fixed carbon (defined here as heterotrophic plasticity) could underlie coral acclimatization and persistence under future ocean-warming scenarios. Here, three species of Caribbean coral—Porites divaricata, P. astreoides, and Orbicella faveolata—were experimentally bleached for 2.5 weeks in two successive years and allowed to recover in the field. Zooplankton feeding was assessed after single and repeat bleaching, while DOC fluxes and the contribution of DOC to the total C budget were determined after single bleaching, 11 months on the reef, and repeat bleaching. Zooplankton was a large C source for P. astreoides, but only following single bleaching. DOC was a source of C for single-bleached corals and accounted for 11–36 % of daily metabolic demand (CHAR_DOC), but represented a net loss of C in repeat-bleached corals. In repeat-bleached corals, DOC loss exacerbated the negative C budgets in all three species. Thus, the capacity for heterotrophic plasticity in corals is compromised under annual bleaching, and heterotrophic uptake of DOC and zooplankton does not mitigate C budget deficits in annually bleached corals. Overall, these findings suggest that some Caribbean corals may be more susceptible to repeat bleaching than to single bleaching due to a lack of heterotrophic plasticity, and coral persistence under increasing bleaching frequency may ultimately depend on other factors such as energy reserves and symbiont shuffling.     

Caribbean massive corals not recovering from repeated thermal stress events during 2005–2013

Massive coral bleaching events associated with high sea surface temperatures are forecast to become more frequent and severe in the future due to climate change. Monitoring colony recovery from bleaching disturbances over multiyear time frames is important for improving predictions of future coral community changes. However, there are currently few multiyear studies describing long‐term outcomes for coral colonies following acute bleaching events. We recorded colony pigmentation and size for bleached and unbleached groups of co‐located conspecifics of three major reef‐building scleractinian corals (Orbicella franksi, Siderastrea siderea, and Stephanocoenia michelini; n = 198 total) in Bocas del Toro, Panama, during the major 2005 bleaching event and then monitored pigmentation status and changes live tissue colony size for 8 years (2005–2013). Corals that were bleached in 2005 demonstrated markedly different response trajectories compared to unbleached colony groups, with extensive live tissue loss for bleached corals of all species following bleaching, with mean live tissue losses per colony 9 months postbleaching of 26.2% (±5.4 SE) for O. franksi, 35.7% (±4.7 SE) for S. michelini, and 11.2% (±3.9 SE) for S. siderea. Two species, O. franksi and S. michelini, later recovered to net positive growth, which continued until a second thermal stress event in 2010. Following this event, all species again lost tissue, with previously unbleached colony species groups experiencing greater declines than conspecific sample groups, which were previously bleached, indicating a possible positive acclimative response. However, despite this beneficial effect for previously bleached corals, all groups experienced substantial net tissue loss between 2005 and 2013, indicating that many important Caribbean reef‐building corals will likely suffer continued tissue loss and may be unable to maintain current benthic coverage when faced with future thermal stress forecast for the region, even with potential benefits from bleaching‐related acclimation.     

High rates of nitrogen fixation (acetylene reduction) on coral skeletons following bleaching mortality

Nubbins of the coral Acropora aspera were artificially bleached and nitrogen fixation (acetylene reduction) rates were measured on the developing epilithic communities. Seasonal comparisons were made between corals that died in summer of heat stress and corals that died in winter from natural cold stress. Rates of acetylene reduction from artificially bleached corals peaked at 26.66 nmol cm⁻² h⁻¹ 2 weeks after summer mortality, while rates from natural winter mortality peaked at 18.07 nmol cm⁻² h⁻¹ 12 days after coral death. Comparative rates of acetylene reduction taken from live corals and coral rubble ranged between 0.56 and 1.16 nmol cm⁻² h⁻¹, and 0.15 and 12.77 nmol cm⁻² h⁻¹, respectively. N₂-fixation rates from dead corals were up to 30 times greater than those measured on live corals. The observed increase in N₂-fixation from dead corals may increase the availability of nitrogen for use in trophic processes within the reef for an extended period following the initial mortality event. If the spatial scale over which coral mortality has occurred in past thermal bleaching events is considered the ramifications of such an increase may be substantial.     

Effects of coral bleaching on the feeding response of two species of coral-feeding fish

Coral bleaching is an increasingly prominent threat to coral reef ecosystems, not only to corals, but also to the many organisms that rely on coral for food and shelter. Coral-feeding fishes are negatively affected by coral loss caused by extensive bleaching, but it is unknown how feeding behaviour of most corallivorous fishes changes in response to coral bleaching. In this study, coral bleaching was experimentally induced in situ to examine the feeding response of two obligate corallivorous fish, Labrichthys unilineatus (Labridae) and Chaetodon baronessa (Chaetodontidae). Feeding rates were monitored before, during, and immediately after experimental bleaching of prey corals. L. unilineatus significantly increased its feeding on impacted corals during bleaching, but showed a steady decline in feeding once corals were fully bleached. Feeding response of L. unilineatus appears to parallel the expected stress-induced mucous production by bleaching colonies. In contrast, C. baronessa preferentially fed from healthy colonies over bleached colonies, although bleached colonies were consumed for five days following manipulation. Feeding by corallivorous fishes can play an important role in determining coral condition and mortality of corals following stress induced bleaching.     

Characterization of fatty acid composition in healthy and bleached corals from Okinawa, Japan

Under bleaching conditions, corals lose their symbiotic zooxanthellae, and thus, the ability to synthesize fatty acids (FAs) from photosynthetically derived carbon. This study investigated the lipid content and FA composition in healthy and bleached corals from the Odo reef flat in Okinawa, southern Japan, following a bleaching event. It was hypothesized that the FA composition and abundance would change as algae are lost or die, and possibly microbial abundance would increase in corals as a consequence of bleaching. The lipid content and FA composition of three healthy coral species (Pavona frondifera, Acropora pulchra, and Goniastrea aspera) and of partially bleached and completely bleached colonies of P. frondifera were examined. The FA composition did not differ among healthy corals, but differed significantly among healthy, partially bleached, and completely bleached specimens of P. frondifera. Completely bleached corals contained significantly lower lipid and total FA content, as well as lower relative amounts of polyunsaturated FAs and higher relative amounts of saturated FAs, than healthy and partially bleached corals. Furthermore, there was a significantly higher relative concentration of monounsaturated FAs and odd-numbered branched FAs in completely bleached corals, indicating an increase in bacterial colonization in the bleached corals.     

Effects of coral bleaching on the obligate coral-dwelling crab Trapezia cymodoce

Corals are an essential and threatened habitat for a diverse range of reef-associated animals. Episodes of coral bleaching are predicted to increase in frequency and intensity over coming decades, yet the effects of coral-host bleaching on the associated animal communities remain poorly understood. The present study investigated the effects of host-colony bleaching on the obligate coral-dwelling crab, Trapezia cymodoce, during a natural bleaching event in the lagoon of Lizard Island, Australia. Branching corals, which harbour the highest diversity of coral associates, comprised 13% of live coral cover at the study site, with 83% affected by bleaching. Crabs on healthy and bleached colonies of Pocillopora damicornis were monitored over a 5-week period to determine whether coral bleaching affected crab density and movement patterns. All coral colonies initially contained one breeding pair of crabs. There was a significant decline in crab density on bleached corals after 5 weeks, with many corals losing one or both crabs, yet all healthy colonies retained a mating pair. Fecundity of crabs collected from bleached and healthy colonies of P. damicornis was also compared. The size of egg clutches of crabs collected from bleached hosts was 40% smaller than those from healthy hosts, indicating a significant reduction in fecundity. A laboratory experiment on movement patterns found that host-colony bleaching also prompted crabs to emigrate in search of more suitable colonies. Emigrant crabs engaged in aggressive interactions with occupants of healthy hosts, with larger crabs always usurping occupants of a smaller size. Decreased densities and clutch sizes, along with increased competitive interactions, could potentially result in a population decline of these important coral associates with cascading effects on coral health.     

Thermally tolerant corals have limited capacity to acclimatize to future warming

Thermal stress affects organism performance differently depending on the ambient temperature to which they are acclimatized, which varies along latitudinal gradients. This study investigated whether differences in physiological responses to temperature are consistent with regional differences in temperature regimes for the stony coral Oculina patagonica. To resolve this question, we experimentally assessed how colonies originating from four different locations characterized by >3 °C variation in mean maximum annual temperature responded to warming from 20 to 32 °C. We assessed plasticity in symbiont identity, density, and photosynthetic properties, together with changes in host tissue biomass. Results show that, without changes in the type of symbiont hosted by coral colonies, O. patagonica has limited capacity to acclimatize to future warming. We found little evidence of variation in overall thermal tolerance, or in thermal optima, in response to spatial variation in ambient temperature. Given that the invader O. patagonica is a relatively new member of the Mediterranean coral fauna, our results also suggest that coral populations may need to remain isolated for a long period of time for thermal adaptation to potentially take place. Our study indicates that for O. patagonica, mortality associated with thermal stress manifests primarily through tissue breakdown under moderate but prolonged warming (which does not impair symbiont photosynthesis and, therefore, does not lead to bleaching). Consequently, projected global warming is likely to cause repeat incidents of partial and whole colony mortality and might drive a gradual range contraction of Mediterranean corals.     

Resilience and acclimation to bleaching stressors in the scleractinian coral Porites cylindrica

‘Resilience’, the capacity of the coral symbiosis with dinoflagellate algal symbionts (‘zooxanthellae’) to recover after bleaching, is a little-studied but crucial aspect of coral responses to bleaching stressors. This study investigated the response of the zooxanthella population in the coral Porites cylindrica after bleaching either naturally on a shallow subtidal reef or experimentally in response to elevated temperature and darkness. Coral resilience was influenced by the nature and duration of the stressor. Corals strongly bleached by natural stressors were less resilient than those that had been partially bleached; and a similar recovery profile was obtained for corals experimentally bleached by exposure to elevated temperature, in which recovery was slower for corals thermally-stressed 96 h than for 72 h. The opposite trend was evident for corals exposed to darkness, indicating that the bleaching trigger had a strong impact on coral resilience. When P. cylindrica recently recovered from bleaching was subjected to a repetition of bleaching stressors, it did not display acclimation, i.e. experience-mediated acquisition of resistance to bleaching stressors. The zooxanthella populations in all corals tested throughout the experiments were typed by PCR-RFLP as clade C, indicating that coral responses were not accompanied by any substantial change in zooxanthella composition at the cladal level.     

Skeletal isotope microprofiles of growth perturbations in<Emphasis Type="Italic"> Porites</Emphasis> corals during the 1997–1998 mass bleaching event

Severe coral bleaching occurred throughout the tropics in 1997/98. We report high-resolution skeletal oxygen isotope (¹⁸O) and carbon isotope (¹³C) microprofiles for bleached corals from Pandora Reef, Great Barrier Reef, and Ishigaki Island, Japan, in order to examine the ability of Porites corals to record clear signals of bleaching. Analysis of the annual cycle in ¹⁸O revealed abrupt reductions in skeletal extension immediately after the 1997–98 summer temperature maximum, indicating that bleaching inhibits coral calcification. Skeletal ¹³C in the Ishigaki corals showed lower values during bleaching, indicating depressed coral metabolism associated with a reduction in calcification. In contrast, microprofiles of skeletal ¹³C from the shaded sides of Pandora Reef corals exhibited little change, possibly because algal photosynthesis was already slow prior to bleaching, thus subduing the ¹³C-response to bleaching. Comparison of ¹⁸O microprofiles from bleached corals with instrumental temperature records showed that Porites corals can recover following 5 months with little skeletogenesis. The results indicate that isotopic microprofiling may be the key to identifying gaps in coral growth that are diagnostic of past bleaching events. We have tested this hypothesis using blue UV fluorescent bands to guide us to coral skeleton where isotope microprofiling identifies bleaching events in 1986, 1989, and 1990. These events, detected by proxy, suggest that coral bleaching may have occurred more commonly on Ishigaki Island than previously recorded.     

Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions

Functional traits define species by their ecological role in the ecosystem. Animals themselves are host–microbe ecosystems (holobionts), and the application of ecophysiological approaches can help to understand their functioning. In hard coral holobionts, communities of dinitrogen (N₂)-fixing prokaryotes (diazotrophs) may contribute a functional trait by providing bioavailable nitrogen (N) that could sustain coral productivity under oligotrophic conditions. This study quantified N₂ fixation by diazotrophs associated with four genera of hermatypic corals on a northern Red Sea fringing reef exposed to high seasonality. We found N₂ fixation activity to be 5- to 10-fold higher in summer, when inorganic nutrient concentrations were lowest and water temperature and light availability highest. Concurrently, coral gross primary productivity remained stable despite lower Symbiodinium densities and tissue chlorophyll a contents. In contrast, chlorophyll a content per Symbiodinium cell increased from spring to summer, suggesting that algal cells overcame limitation of N, an essential element for chlorophyll synthesis. In fact, N₂ fixation was positively correlated with coral productivity in summer, when its contribution was estimated to meet 11% of the Symbiodinium N requirements. These results provide evidence of an important functional role of diazotrophs in sustaining coral productivity when alternative external N sources are scarce.     

Changes in Bleaching Susceptibility among Corals Subject to Ocean Warming and Recurrent Bleaching in Moorea,French Polynesia

Background

Climate-induced coral bleaching poses a major threat to coral reef ecosystems, mostly because of the sensitivities of key habitat-forming corals to increasing temperature. However, susceptibility to bleaching varies greatly among coral genera and there are likely to be major changes in the relative abundance of different corals, even if the wholesale loss of corals does not occur for several decades. Here we document variation in bleaching susceptibility among key genera of reef-building corals in Moorea, French Polynesia, and compare bleaching incidence during mass-bleaching events documented in 1991, 1994, 2002 and 2007.

Methodology/Principal Findings

This study compared the proportion of colonies that bleached for four major genera of reef-building corals (Acropora, Montipora, Pocillopora and Porites), during each of four well-documented bleaching events from 1991 to 2007. Acropora and Montipora consistently bleached in far greater proportions (up to 98%) than Pocillopora and Porites. However, there was an apparent and sustained decline in the proportion of colonies that bleached during successive bleaching events, especially for Acropora and Montipora. In 2007, only 77% of Acropora colonies bleached compared with 98% in 1991. Temporal variation in the proportion of coral colonies bleached may be attributable to differences in environmental conditions among years. Alternately, the sustained declines in bleaching incidence among highly susceptible corals may be indicative of acclimation or adaptation.

Conclusions/Significance

Coral genera that are highly susceptible to coral bleaching, and especially Acropora and Montipora, exhibit temporal declines in their susceptibility to thermal anomalies at Moorea, French Polynesia. One possible explanation for these findings is that gradual removal of highly susceptible genotypes (through selective mortality of individuals, populations, and/or species) is producing a coral assemblage that is more resistant to sustained and ongoing ocean warming.     

Relocating bleached Platygyra sinensis facilitates recovery from thermal stress during a minor bleaching event

The recovery of bleached corals is crucial in ensuring the persistence of the coral reef ecosystem function. This study investigated whether relocating bleached Platygyra sinensis colonies was a viable measure to accelerate their recovery. During a mild bleaching event in 2014, eight bleached colonies of P. sinensis were relocated from an affected reef at Sultan Shoal, Singapore, to a reef at Kusu that was less impacted. Another eight colonies at Sultan Shoal were tagged as controls. After five months, 88% of relocated bleached colonies at Kusu showed full recovery whereas only 25% of the control bleached colonies at Sultan Shoal had recovered. The differential coral recovery among the two sites was most likely due to lower seawater temperatures and faster water flow at Kusu, which helped to mitigate the effects of thermal stress on the bleached corals. This relocation study demonstrated that relocating bleached P. sinensis to sites with more favourable environmental conditions is a viable approach to reduce bleaching impacts for this species.     

Reduced growth rate of Montastrea annularis following the 1987–1988 coral-bleaching event

Montastrea annularis, the major Caribbean reef building coral, was severely affected by the unprecedented 1987–1988 bleaching event. Most colonies on the fore reef were affected but few were bleached in the back reef. Skeletal growth rates of M. annularis populations were measured non-destructively in the field at Discovery Bay, Jamaica, from the peak of bleaching in Nov. 1987 until recovery was almost complete, in May 1988. Unbleached corals grew at normal rates. Partially bleached corals survived but skeletal growth ceased through this period.     

Endolithic algae: an alternative source of photoassimilates during coral bleaching

Recent reports of worldwide coral bleaching events leading to devastating coral mortality have caused alarm among scientists and resource managers. Differential survival of coral species through bleaching events has been widely documented. We suggest that among the possible factors contributing to survival of coral species during such events are endolithic algae harboured in their skeleton, providing an alternative source of energy. We studied the dynamics of photosynthetic pigment concentrations and biomass of endoliths in the skeleton of the encrusting coral Oculina patagonica throughout a bleaching event. During repeated summer bleaching events these endolithic algae receive increased photosynthetically active radiation, increase markedly in biomass, and produce increasing amounts of photoassimilates, which are translocated to the coral. Chlorophyll concentrations and biomass of endoliths were 4.6 +/- 1.57 and 1570 +/- 427 microg cm(-2) respectively, in skeletons of relatively healthy colonies (0-40% bleaching) but up to 14.8 +/- 2.5 and 4036 +/- 764 microg cm(-2) endolith chlorophyll and biomass respectively, in skeletons of bleached colonies (greater than 40% bleaching). The translocation dynamics of (14)C-labelled photoassimilates from the endoliths to bleached coral tissue showed significantly higher 14C activity of the endoliths harboured within the skeletons of bleached corals than that of the endoliths in non-bleached corals. This alternative source of energy may be vital for the survivorship of O. patagonica, allowing gradual recruitment of zooxanthellae and subsequent recovery during the following winter.     

The effects of prolonged “bleaching” on the tissue biomass and reproduction of the reef coral Montastrea annularis

Colonies of Montastrea annularis from Carysfort Reef, Florida, that remained bleached seven months after the 1987 Caribbean bleaching event were studied to determine the long term effects of bleaching on coral physiology. Two types of bleached colonies were found: colonies with low numbers of zooxanthellae with normal pigment content, and a colony with high densities of lowpigment zooxanthellae. In both types, the zooxanthellae had an abnormal distribution within polyp tissues: highest densities were observed in basal endoderm and in mesenteries where zooxanthellae are not normally found. Bleached corals had 30% less tissue carbon and 44% less tissue nitrogen biomass per skeletal surface area, but the same tissue C:N ratio as other colonies that either did not bleach (normal) or that bleached and regained their zooxanthellae (recovered). Bleached corals were not able to complete gametogenesis during the reproductive season following the bleaching, while recovered corals were able to follow a normal gametogenic cycle. It appears that bleached corals were able to survive the prolonged period without nutritional contribution from their zooxanthellae by consuming their own structural materials for maintenance, but then, did not have the resources necessary for reproduction. The recovered corals, on the other hand, must have regained their zooxanthellae soon after the bleaching event since neither their tissue biomass nor their ability to reproduce were impaired.