Exaptation in corals to high seawater temperatures: Low concentrations of apoptotic and necrotic cells in host coral tissue under bleaching conditions

Scleractinian corals are known to suffer bleaching or loss of their symbiotic zooxanthellae under conditions of elevated seawater temperatures often associated with climate change (i.e. global warming). This can occur on a massive scale and has caused the decimation of reefs on a global basis. During the bleaching process, the expelled zooxanthellae suffer cell damage from heat stress, characterized by irreversible ultrastructural and physiological changes which are symptomatic of cell degeneration and death (called apoptosis) or necrosis. A question that remains unanswered, however, is whether the coral hosts themselves are sensitive to seawater temperatures, and, if so, to what degree? In a controlled experiment, we exposed corals Acropora hyacinthus (Dana, 1846) and Porites solida (Forskål, 1775) with their symbiotic zooxanthellae (Symbiodinium sp.) to temperatures of 28 °C (control), 30 °C, 32 °C, and 34 °C for 48 h and also to 36 °C for 12 h. We assessed coral and zooxanthellar cells in-situ for symptoms of apoptosis and necrosis using transmission electron microscopy (TEM), fluorescent microscopy (FM), and flow cytometry (FC). We found that the coral host cells in-situ exhibited, for the most part, little or no mortality from increased seawater temperatures. Damage to the coral hosts only occurred under conditions of prolonged exposure (≥ 12 h) at high temperatures (34 °C), or at exceptionally high temperatures (e.g. 36 °C). On the other hand, we found high levels of apoptosis and necrosis in the zooxanthellae in-situ under all treatment conditions of elevated seawater temperatures. We found that during bleaching, the host cells are not experiencing much mortality - but the zooxanthellae, even while still within the host, are. The host corals exhibit exaptation to accommodate temperatures as high as ≥ 34 °C. Temperature stress within these highly specific and coevolved symbiotic systems is derived not from host sensitivity to temperature, but from the symbiont's sensitivity and the loss of the coral's endosymbiotic partners.     

Monthly variations in calix growth, polyp tissue, and density banding of the Mediterranean scleractinian Cladocora caespitosa (L.)

Monthly skeletal growth of the scleractinian, temperate coral Cladocora caespitosa (L.) from the Ligurian Sea (NW Mediterranean) was analysed for a period of 1 year and compared with seawater parameters. Measurements on corallite sections and on X-ray images showed that the formation of the high-density (HD) band and two dissepiments are favoured by fall–winter conditions, characterised by high quantities of rain, rough seas, and cold seawater. In summer, when the low-density (LD) band is formed, the corallites stretch upward and form one new dissepiment and one deep calix, where the polyps recede almost completely in August. These findings confirmed the adaptation of the temperate coral to winter environmental conditions, characterised by low irradiance and high availability of nutrients and food particles resuspended from bottom sediments. On the contrary, the high seawater temperature, irradiance, and ammonia contents stressed the coral in August and, when they persist in September, may cause the onset of mortality events.     

Thermal threshold and sensitivity of the only symbiotic Mediterranean gorgonian Eunicella singularis by morphometric and genotypic analyses

The only symbiotic Mediterranean gorgonian, Eunicella singularis, has faced several mortality events connected to abnormal high temperatures. Since thermotolerance data remain scarce, heat-induced necrosis was monitored in aquarium by morphometric analysis. Gorgonian tips were sampled at two sites: Medes (Spain) and Riou (France) Islands, and at two depths: –15 m and–35 m. Although coming from contrasting thermal regimes, seawater above 28 °C led to rapid and complete tissue necrosis for all four populations. However, at 27 °C, the time length leading to 50% tissue necrosis allowed us to classify samples within three classes of thermal sensitivity. Irrespectively of the depth, Medes specimens were either very sensitive or resistant, while Riou fragments presented a medium sensitivity. Microsatellite analysis revealed that host and symbiont were genetically differentiated between sites, but not between depths. Finally, these genetic differentiations were not directly correlated to a specific thermal sensitivity whose molecular bases remain to be discovered.     

Effects of temperature on growth rate and body size in the Mediterranean Sea anemone Actinia equina

Actinia equina is the most common sea anemone in the rocky intertidal zone of the Mediterranean coast of Israel, yet little is known about its biology in this habitat. We examined variation in polyp growth at several temperatures within the local range. Under laboratory conditions, only polyps at low temperatures (15 and 20 °C) grew, whereas those at higher temperatures (25 and 30 °C) lost body mass. Seasonal monitoring of pedal disk diameter over 18 months at field sites showed that polyps shrank significantly during the summer when temperatures were high. We conclude that at summer seawater temperatures along the coast of Israel (28.7-29.5 °C), polyps of A. equina are unable to balance their metabolic requirements with energy input, resulting in a seasonal reduction in biomass. Polyps appear able to acclimate to high temperatures, but not sufficiently to avoid shrinkage of tissues.     

Thermodependent bacterial pathogens and mass mortalities in temperate benthic communities: a new case of emerging disease linked to climate change

In the temperate north-western Mediterranean Sea, large-scale disease outbreaks in benthic invertebrate species have recently occurred during climatic anomalies characterized by elevated seawater temperatures. One of the most affected species was the red gorgonian Paramuricea clavata , a key species of highly diverse communities dwelling in dim-lit habitats in the Mediterranean. From diseased P. clavata colonies, we isolated culturable bacteria associated to tissue lesions in order to investigate their potential as pathogens. Inoculation of four bacterial isolates onto healthy P. clavata in aquaria caused disease signs similar to those observed during the 2003 mortality event. The infection process was dependent on elevated seawater temperatures, in a range of values consistent with recordings performed in the field during the climatic anomalies. Among the four isolates, we identified a Vibrio coralliilyticus strain that showed virulence to P. clavata . This strain was re-isolated from diseased colonies during the experimentations. V. coralliilyticus has been previously identified as a thermodependent pathogen of a tropical coral species, emphasizing a causal role of this infectious agent in the P. clavata disease. Taking into consideration predicted global warming over the coming decades, a better understanding of the factors and mechanisms that affect the disease process will be of critical importance in predicting future threats to temperate gorgonians communities in the Mediterranean Sea.     

Calcification rate and the effect of temperature in a zooxanthellate and an azooxanthellate scleractinian reef coral

Calcification rates, normalized to skeletal mass, in the zooxanthellate Galaxea fascicularis and the azooxanthellate Dendrophyllia sp. were similar over the whole temperature range of 18–29 °C. Calcification was measured by Ca⁴⁵ incorporation in corals that were naturally acclimated to the prevailing seawater temperature. In both species maximum calcification rate occurred at about 25 °C and calcification rates can be fitted to a Gaussian distribution with respect to temperature. The similarity in temperature dependence of the zooxanthellate and azooxanthellate coral suggests that temperature affects some fundamental process of calcification that is independent of light effects. It is shown that two different populations of Galaxea fascicularis have distinctly different ratios of tissue protein to skeletal mass per polyp. This indicates that tissue protein may not be suitable for normalizing calcification rates in individual coral polyps, both within and between species. Intra- and interspecific comparisons of calcification rates may be better made on the basis of skeletal mass when polyps are similar in size and shape.Communicated by Topic Editor C. Barnes     

End of the Century pCO2 Levels Do Not Impact Calcification in Mediterranean Cold-Water Corals

Ocean acidification caused by anthropogenic uptake of CO₂ is perceived to be a major threat to calcifying organisms. Cold-water corals were thought to be strongly affected by a decrease in ocean pH due to their abundance in deep and cold waters which, in contrast to tropical coral reef waters, will soon become corrosive to calcium carbonate. Calcification rates of two Mediterranean cold-water coral species, Lophelia pertusa and Madrepora oculata, were measured under variable partial pressure of CO₂ (pCO₂) that ranged between 380 µatm for present-day conditions and 930 µatm for the end of the century. The present study addressed both short- and long-term responses by repeatedly determining calcification rates on the same specimens over a period of 9 months. Besides studying the direct, short-term response to elevated pCO₂ levels, the study aimed to elucidate the potential for acclimation of calcification of cold-water corals to ocean acidification. Net calcification of both species was unaffected by the levels of pCO₂ investigated and revealed no short-term shock and, therefore, no long-term acclimation in calcification to changes in the carbonate chemistry. There was an effect of time during repeated experiments with increasing net calcification rates for both species, however, as this pattern was found in all treatments, there is no indication that acclimation of calcification to ocean acidification occurred. The use of controls (initial and ambient net calcification rates) indicated that this increase was not caused by acclimation in calcification response to higher pCO₂. An extrapolation of these data suggests that calcification of these two cold-water corals will not be affected by the pCO₂ level projected at the end of the century.     

Calcification rates and the effect of ocean acidification on Mediterranean cold-water corals

Global environmental changes, including ocean acidification, have been identified as a major threat to scleractinian corals. General predictions are that ocean acidification will be detrimental to reef growth and that 40 to more than 80 per cent of present-day reefs will decline during the next 50 years. Cold-water corals (CWCs) are thought to be strongly affected by changes in ocean acidification owing to their distribution in deep and/or cold waters, which naturally exhibit a CaCO(3) saturation state lower than in shallow/warm waters. Calcification was measured in three species of Mediterranean cold-water scleractinian corals (Lophelia pertusa, Madrepora oculata and Desmophyllum dianthus) on-board research vessels and soon after collection. Incubations were performed in ambient sea water. The species M. oculata was additionally incubated in sea water reduced or enriched in CO(2). At ambient conditions, calcification rates ranged between -0.01 and 0.23% d(-1). Calcification rates of M. oculata under variable partial pressure of CO(2) (pCO(2)) were the same for ambient and elevated pCO(2) (404 and 867 μatm) with 0.06 ± 0.06% d(-1), while calcification was 0.12 ± 0.06% d(-1) when pCO(2) was reduced to its pre-industrial level (285 μatm). This suggests that present-day CWC calcification in the Mediterranean Sea has already drastically declined (by 50%) as a consequence of anthropogenic-induced ocean acidification.     

Caribbean mesophotic coral ecosystems are unlikely climate change refugia

Deeper coral reefs experience reduced temperatures and light and are often shielded from localized anthropogenic stressors such as pollution and fishing. The deep reef refugia hypothesis posits that light‐dependent stony coral species at deeper depths are buffered from thermal stress and will avoid bleaching‐related mass mortalities caused by increasing sea surface temperatures under climate change. This hypothesis has not been tested because data collection on deeper coral reefs is difficult. Here we show that deeper (mesophotic) reefs, 30–75 m depth, in the Caribbean are not refugia because they have lower bleaching threshold temperatures than shallow reefs. Over two thermal stress events, mesophotic reef bleaching was driven by a bleaching threshold that declines 0.26 °C every +10 m depth. Thus, the main premise of the deep reef refugia hypothesis that cooler environments are protective is incorrect; any increase in temperatures above the local mean warmest conditions can lead to thermal stress and bleaching. Thus, relatively cooler temperatures can no longer be considered a de facto refugium for corals and it is likely that many deeper coral reefs are as vulnerable to climate change as shallow water reefs.     

Long-Term Responses of the Endemic Reef-Builder Cladocora caespitosa to Mediterranean Warming

Recurrent climate-induced mass-mortalities have been recorded in the Mediterranean Sea over the past 15 years. Cladocora caespitosa, the sole zooxanthellate scleractinian reef-builder in the Mediterranean, is among the organisms affected by these episodes. Extensive bioconstructions of this endemic coral are very rare at the present time and are threatened by several stressors. In this study, we assessed the long-term response of this temperate coral to warming sea-water in the Columbretes Islands (NW Mediterranean) and described, for the first time, the relationship between recurrent mortality events and local sea surface temperature (SST) regimes in the Mediterranean Sea. A water temperature series spanning more than 20 years showed a summer warming trend of 0.06°C per year and an increased frequency of positive thermal anomalies. Mortality resulted from tissue necrosis without massive zooxanthellae loss and during the 11-year study, necrosis was recorded during nine summers separated into two mortality periods (2003–2006 and 2008–2012). The highest necrosis rates were registered during the first mortality period, after the exceptionally hot summer of 2003. Although necrosis and temperature were significantly associated, the variability in necrosis rates during summers with similar thermal anomalies pointed to other acting factors. In this sense, our results showed that these differences were more closely related to the interannual temperature context and delayed thermal stress after extreme summers, rather than to acclimatisation and adaption processes.     

High zooxanthella density shortens the survival time of coral cell aggregates under thermal stress

To investigate bleaching mechanisms in coral-zooxanthella symbiotic systems, it is important to study the cellular- or tissue-level responses of corals to stress. We established an experimental system to study the stress responses of coral cells using coral cell aggregates. Dissociated coral cells aggregate to form spherical bodies, which rotate by ciliary movement. These spherical bodies (tissue balls) stop rotating and disintegrate when exposed to a thermal stress. Tissue balls prepared from dissociated cells of Fungia sp. and Pavona divaricata were exposed to either elevated temperature (31 °C, with 25 °C as the control) or elevated temperature in the presence of exogenous antioxidants (ascorbic acid and catalase, or mannitol). The survival curves of tissue balls were markedly different between 31 and 25 °C. At 31 °C, most tissue balls disintegrated within 24 h, whereas at 25 °C, most tissue balls survived for more than 24 h. There was a negative correlation between survival time and the zooxanthella density of tissue balls at 31 °C, but no significant relationship was found at 25 °C. Antioxidants extended the survival time of tissue balls at high temperature, suggesting that zooxanthellae produce reactive oxygen species under stress. These results indicate that zooxanthellae produce harmful substances and damage coral cells under high-temperature stress. Tissue balls provide a good experimental system with which to study the effects of stress and various chemical reagents on corals cells.     

Increased temperature mitigates the effects of ocean acidification on the calcification of juvenile Pocillopora damicornis,but at a cost

This study tested the interactive effects of increased seawater temperature and CO₂ partial pressure (pCO₂) on the photochemistry, bleaching, and early growth of the reef coral Pocillopora damicornis. New recruits were maintained at ambient or high temperature (29 or 30.8 °C) and pCO₂ (~ 500 and ~ 1100 μatm) in a full-factorial experiment for 3 weeks. Neither a sharp decline in photochemical efficiency (Fv/Fm) nor evident bleaching was observed at high temperature and/or high pCO₂. Furthermore, elevated temperature greatly promoted lateral growth and calcification, while polyp budding exhibited temperature-dependent responses to pCO₂. High pCO₂ depressed calcification by 28% at ambient temperature, but did not impact calcification at 30.8 °C. Interestingly, elevated temperature in concert with high pCO₂ significantly retarded the budding process. These results suggest that increased temperature can mitigate the adverse effects of acidification on the calcification of juvenile P. damicornis, but at a substantial cost to asexual budding.

     

The physiological response of reef corals to diel fluctuations in seawater temperature

An opportunity to explore the effects of fluctuating temperatures on tropical scleractinian corals arose when diurnal warming (as large as 4.7 °C) was detected over the rich coral communities found within the back reef of Moorea, French Polynesia. In April and May 2007, experiments were completed to determine the effects of fluctuating temperature on Pocillopora meandrina and Porites rus, and consecutive trials were used to expose them for 13 days to 26 °C, 28 °C (ambient conditions), 30 °C, or a fluctuating treatment ranging from 26 to 30 °C over 24 h. The multivariate response was assessed using maximum dark-adapted quantum yield of PSII (F_V/F_M), Symbiodinium density, chlorophyll-a content, and calcification. In trial 1, multivariate physiology of both species was significantly affected by treatments, with the fluctuating temperature resulting in a 17-45% decline in Symbiodinium density (relative to the ambient) matching that occurring at a constant 30 °C; F_V/F_M, chlorophyll-a content, and calcification, did not differ between the fluctuating and the steady treatments. In contrast, in trial 2 that utilized corals collected two weeks after those used in trial 1, the corals were unaffected by the treatments, likely due to an environment × trial interaction caused by seasonal declines in Symbiodinium density. Together, these results demonstrate that short transgressions to ecologically relevant high and low temperatures can elicit a potentially detrimental response equivalent to that occurring upon exposure to a constant high temperature. The dissimilar responses among dependent variables and consecutive trials underscore the importance of temporal replication and multivariate approaches in coral ecophysiology. It is likely that recent history has a stronger effect on the response of corals to treatments than is currently recognized.     

Effects of intermittent flow and irradiance level on back reef Porites corals at elevated seawater temperatures

Corals inhabiting shallow back reef habitats are often simultaneously exposed to elevated seawater temperatures and high irradiance levels, conditions known to cause coral bleaching. Water flow in many tropical back reef systems is tidally influenced, resulting in semi-diurnal or diurnal flow patterns. Controlled experiments were conducted to test effects of semi-diurnally intermittent water flow on photoinhibition and bleaching of the corals Porites lobata and P. cylindrica kept at elevated seawater temperatures and different irradiance levels. All coral colonies were collected from a shallow back reef pool on Ofu Island, American Samoa. In the high irradiance experiments, photoinhibition and bleaching were less for both species in the intermittent high-low flow treatment than in the constant low flow treatment. In the low irradiance experiments, there were no differences in photoinhibition or bleaching for either species between the flow treatments, despite continuously elevated seawater temperatures. These results suggest that intermittent flow associated with semi-diurnal tides, and low irradiances caused by turbidity or shading, may reduce photoinhibition and bleaching of back reef corals during warming events.     

Antimicrobial and stress responses to increased temperature and bacterial pathogen challenge in the holobiont of a reef‐building coral

Global increases in coral disease prevalence have been linked to ocean warming through changes in coral‐associated bacterial communities, pathogen virulence and immune system function. However, the interactive effects of temperature and pathogens on the coral holobiont are poorly understood. Here, we assessed three compartments of the holobiont (host, Symbiodinium and bacterial community) of the coral Montipora aequituberculata challenged with the pathogen Vibrio coralliilyticus and the commensal bacterium Oceanospirillales sp. under ambient (27°C) and elevated (29.5 and 32°C) seawater temperatures. Few visual signs of bleaching and disease development were apparent in any of the treatments, but responses were detected in the holobiont compartments. V. coralliilyticus acted synergistically and negatively impacted the photochemical efficiency of Symbiodinium at 32°C, while Oceanospirillales had no significant effect on photosynthetic efficiency. The coral, however, exhibited a minor response to the bacterial challenges, with the response towards V. coralliilyticus being significantly more pronounced, and involving the prophenoloxidase‐activating system and multiple immune system‐related genes. Elevated seawater temperatures did not induce shifts in the coral‐associated bacterial community, but caused significant gene expression modulation in both Symbiodinium and the coral host. While Symbiodinium exhibited an antiviral response and upregulated stress response genes, M. aequituberculata showed regulation of genes involved in stress and innate immune response processes, including immune and cytokine receptor signalling, the complement system, immune cell activation and phagocytosis, as well as molecular chaperones. These observations show that M. aequituberculata is capable of maintaining a stable bacterial community under elevated seawater temperatures and thereby contributes to preventing disease development.     

Coral disease following massive bleaching in 2005 causes 60% decline in coral cover on reefs in the US Virgin Islands

In the northeast Caribbean, doldrum-like conditions combined with elevated water temperatures in the summer/fall 2005 created the most severe coral bleaching event ever documented within this region. Video monitoring of 100 randomly chosen, permanent transects at five study sites in the US Virgin Islands revealed over 90% of the scleractinian coral cover showed signs of thermal stress by paling or becoming completely white. Lower water temperatures in October allowed some re-coloring of corals; however, a subsequent unprecedented regional outbreak of coral disease affected all sites. Five known diseases or syndromes were recorded; however, most lesions showed signs similar to white plague. Nineteen scleractinian species were affected by disease, with >90% of the disease-induced lesions occurring on the genus Montastraea. The disease outbreak peaked several months after the onset of bleaching at all sites but did not occur at the same time. The mean number of disease-induced lesions increased 51-fold and the mean area of disease-associated mortality increased 13-fold when compared with pre-bleaching disease levels. In the 12 months following the onset of bleaching, coral cover declined at all sites (average loss: 51.5%, range: 42.4–61.8%) reducing the five-site average from 21.4% before bleaching to 10.3% with most mortality caused by white plague disease, not bleaching. Continued losses through October 2007 reduced the average coral cover of the five sites to 8.3% (average 2-year loss: 61.1%, range: 53.0–79.3%). Mean cover by M. annularis (complex) decreased 51%, Colpophyllia natans 78% and Agaricia agaricites 87%. Isolated disease outbreaks have been documented before in the Virgin Islands, but never as widespread or devastating as the one that occurred after the 2005 Caribbean coral-bleaching event. This study provides insight into the effects of continued seawater warming and subsequent coral bleaching events in the Caribbean and highlights the need to understand links between coral bleaching and disease.     

Acquisition of thermotolerance in bay scallops, Argopecten irradians irradians, via differential induction of heat shock proteins

Many cells and organisms are rendered transiently resistant to lethal heat shock by short exposure to sublethal temperatures. This induced thermotolerance is thought to be related to increased amounts of heat shock proteins (HSPs) which, as molecular chaperones, protect cells from stress-induced damage. As part of a study on bivalve stress and thermotolerance, work was undertaken to examine the effects of sublethal heat shock on stress tolerance of juveniles of the northern bay scallop, Argopecten irradians irradians, in association with changes in the levels of cytoplasmic HSP70 and 40. Juvenile bay scallops heat-shocked at a sublethal temperature of 32 °C survived an otherwise lethal heat treatment at 35 °C for at least 7 days. As determined by ELISA, acquisition of induced thermotolerance closely paralleled HSP70 accumulation, whereas HSP40 accrual appeared less closely associated with thermotolerance. Quantification of scallop HSPs following lethal heat treatment, with or without conditioning, suggested a causal role for HSP70 in stress tolerance, with HSP40 contributing to a lesser, but significant extent. Overall, this study demonstrated that sublethal heat shock promotes survival of A. irradians irradians juveniles upon thermal stress and the results support the hypothesis that HSPs have a role in this induced thermotolerance. Exploitation of the induced thermotolerance response shows promise as a means to improve survival of bay scallops in commercial culture.     

Coral reef crisis in deep and shallow reefs: 30 years of constancy and change in reefs of Curacao and Bonaire

Coral reefs are thought to be in worldwide decline but available data are practically limited to reefs shallower than 25 m. Zooxanthellate coral communities in deep reefs (30–40 m) are relatively unstudied. Our question is: what is happening in deep reefs in terms of coral cover and coral mortality? We compare changes in species composition, coral mortality, and coral cover at Caribbean (Curacao and Bonaire) deep (30–40 m) and shallow reefs (10–20 m) using long-term (1973–2002) data from permanent photo quadrats. About 20 zooxanthellate coral species are common in the deep-reef communities, dominated by Agaricia sp., with coral cover up to 60%. In contrast with shallow reefs, there is no decrease in coral cover or number of coral colonies in deep reefs over the last 30 years. In deep reefs, non-agaricid species are decreasing but agaricid domination will be interrupted by natural catastrophic mortality such as deep coral bleaching and storms. Temperature is a vastly fluctuating variable in the deep-reef environment with extremely low temperatures possibly related to deep-reef bleaching. An erratum to this article can be found at     

Red Coral Fishery at the Costa Brava (NW Mediterranean): Case Study of an Overharvested Precious Coral

Abstract The Mediterranean red coral (Corallium rubrum, L. 1758) is a slow-growing longevous gorgonian that produces a red calcium carbonate skeleton, which is in high demand by the jewellery industry. Its long history of intensive commercial harvesting has resulted in a well-documented decline of its stocks throughout the Mediterranean, becoming especially apparent during the last two decades. Based on the extensive ecological data from the Costa Brava (NE Spain) stocks, this study reviews, for the first time, socioeconomic aspects and the impact of current fishing practices on the red coral population structure and reproductive biology. A comparison of the intensively harvested populations in shallow water with that of the infrequently harvested ones in deep water, along with a population in a marine reserve as well, reveals that 98% of all shallow water colonies show a juvenile size and branching pattern as a result of harvesting. Recent data on the reproductive biology of the species show that 91% of the colonies in shallow water populations (<60 m depth) are not 100% sexually mature. These populations are clearly at the limit of their recoverability potential. The maximum sustainable yield (estimated using the Beverton-Holt model) is reached at an age of first capture of 98 years, although the current regulations allow harvesting of approximately 11-year-old colonies (corresponding to a basal diameter of 7 mm). The presented data reveal how this renewable resource is being exploited in a clearly non-sustainable and inefficient way, changing significantly the underwater landscape of the Mediterranean coast. The review of all available data suggests that the shallow water stocks are depleted. Furthermore, recent trends in poaching of juvenile colonies and mass mortality events threaten the survival of the shallow water populations. A ban on reconstituted coral from the market appears to be the only option to control this form of poaching.