Temperature-Regulated Bleaching and Lysis of the Coral Pocillopora damicornis by the Novel Pathogen Vibrio coralliilyticus

Coral bleaching is the disruption of symbioses between coral animals and their photosynthetic microalgal endosymbionts (zooxanthellae). It has been suggested that large-scale bleaching episodes are linked to global warming. The data presented here demonstrate that Vibrio coralliilyticus is an etiological agent of bleaching of the coral Pocillopora damicornis. This bacterium was present at high levels in bleached P. damicornis but absent from healthy corals. The bacterium was isolated in pure culture, characterized microbiologically, and shown to cause bleaching when it was inoculated onto healthy corals at 25°C. The pathogen was reisolated from the diseased tissues of the infected corals. The zooxanthella concentration in the bacterium-bleached corals was less than 12% of the zooxanthella concentration in healthy corals. When P. damicornis was infected with V. coralliilyticus at higher temperatures (27 and 29°C), the corals lysed within 2 weeks, indicating that the seawater temperature is a critical environmental parameter in determining the outcome of infection. A large increase in the level of the extracellular protease activity of V. coralliilyticus occurred at the same temperature range (24 to 28°C) as the transition from bleaching to lysis of the corals. We suggest that bleaching of P. damicornis results from an attack on the algae, whereas bacterium-induced lysis and death are promoted by bacterial extracellular proteases. The data presented here support the bacterial hypothesis of coral bleaching.     

Elevated Temperature Alters the Lunar Timing of Planulation in the Brooding Coral Pocillopora damicornis

Reproductive timing in corals is associated with environmental variables including temperature, lunar periodicity, and seasonality. Although it is clear that these variables are interrelated, it remains unknown if one variable in particular acts as the proximate signaler for gamete and or larval release. Furthermore, in an era of global warming, the degree to which increases in ocean temperatures will disrupt normal reproductive patterns in corals remains unknown. Pocillopora damicornis, a brooding coral widely distributed in the Indo-Pacific, has been the subject of multiple reproductive ecology studies that show correlations between temperature, lunar periodicity, and reproductive timing. However, to date, no study has empirically measured changes in reproductive timing associated with increased seawater temperature. In this study, the effect of increased seawater temperature on the timing of planula release was examined during the lunar cycles of March and June 2012. Twelve brooding corals were removed from Hobihu reef in Nanwan Bay, southern Taiwan and placed in 23 and 28°C controlled temperature treatment tanks. For both seasons, the timing of planulation was found to be plastic, with the high temperature treatment resulting in significantly earlier peaks of planula release compared to the low temperature treatment. This suggests that temperature alone can influence the timing of larval release in Pocillopora damicornis in Nanwan Bay. Therefore, it is expected that continued increases in ocean temperature will result in earlier timing of reproductive events in corals, which may lead to either variations in reproductive success or phenotypic acclimatization.     

Physiological Response of the Hard Coral Pocillopora verrucosa from Lombok,Indonesia, to Two Common Pollutants in Combination with High Temperature

Knowledge on interactive effects of global (e.g. ocean warming) and local stressors (e.g. pollution) is needed to develop appropriate management strategies for coral reefs. Surfactants and diesel are common coastal pollutants, but knowledge of their effects on hard corals as key reef ecosystem engineers is scarce. This study thus investigated the physiological reaction of Pocillopora verrucosa from Lombok, Indonesia, to exposure with a) the water-soluble fraction of diesel (determined by total polycyclic aromatic hydrocarbons (PAH); 0.69 ± 0.14 mg L-1), b) the surfactant linear alkylbenzene sulfonate (LAS; 0.95 ± 0.02 mg L-1) and c) combinations of each pollutant with high temperature (+3°C). To determine effects on metabolism, respiration, photosynthetic efficiency and coral tissue health were measured. Findings revealed no significant effects of diesel, while LAS resulted in severe coral tissue losses (16–95% after 84 h). High temperature led to an increase in photosynthetic yield of corals after 48 h compared to the control treatment, but no difference was detected thereafter. In combination, diesel and high temperature significantly increased coral dark respiration, whereas LAS and high temperature caused higher tissue losses (81–100% after 84 h) and indicated a severe decline in maximum quantum yield. These results confirm the hypothesized combined effects of high temperature with either of the two investigated pollutants. Our study demonstrates the importance of reducing import of these pollutants in coastal areas in future adaptive reef management, particularly in the context of ocean warming.     

Threatened Caribbean Coral Is Able to Mitigate the Adverse Effects of Ocean Acidification on Calcification by Increasing Feeding Rate

Global climate change threatens coral growth and reef ecosystem health via ocean warming and ocean acidification (OA). Whereas the negative impacts of these stressors are increasingly well-documented, studies identifying pathways to resilience are still poorly understood. Heterotrophy has been shown to help corals experiencing decreases in growth due to either thermal or OA stress; however, the mechanism by which it mitigates these decreases remains unclear. This study tested the ability of coral heterotrophy to mitigate reductions in growth due to climate change stress in the critically endangered Caribbean coral Acropora cervicornis via changes in feeding rate and lipid content. Corals were either fed or unfed and exposed to elevated temperature (30°C), enriched pCO₂ (800 ppm), or both (30°C/800 ppm) as compared to a control (26°C/390 ppm) for 8 weeks. Feeding rate and lipid content both increased in corals experiencing OA vs. present-day conditions, and were significantly correlated. Fed corals were able to maintain ambient growth rates at both elevated temperature and elevated CO₂, while unfed corals experienced significant decreases in growth with respect to fed conspecifics. Our results show for the first time that a threatened coral species can buffer OA-reduced calcification by increasing feeding rates and lipid content.     

The reef-building coral Siderastrea siderea exhibits parabolic responses to ocean acidification and warming

Anthropogenic increases in atmospheric CO₂ over this century are predicted to cause global average surface ocean pH to decline by 0.1–0.3 pH units and sea surface temperature to increase by 1–4°C. We conducted controlled laboratory experiments to investigate the impacts of CO₂-induced ocean acidification (pCO₂ = 324, 477, 604, 2553 µatm) and warming (25, 28, 32°C) on the calcification rate of the zooxanthellate scleractinian coral Siderastrea siderea, a widespread, abundant and keystone reef-builder in the Caribbean Sea. We show that both acidification and warming cause a parabolic response in the calcification rate within this coral species. Moderate increases in pCO₂ and warming, relative to near-present-day values, enhanced coral calcification, with calcification rates declining under the highest pCO₂ and thermal conditions. Equivalent responses to acidification and warming were exhibited by colonies across reef zones and the parabolic nature of the corals'' response to these stressors was evident across all three of the experiment''s 30-day observational intervals. Furthermore, the warming projected by the Intergovernmental Panel on Climate Change for the end of the twenty-first century caused a fivefold decrease in the rate of coral calcification, while the acidification projected for the same interval had no statistically significant impact on the calcification rate—suggesting that ocean warming poses a more immediate threat than acidification for this important coral species.     

Effects of water motion on reef corals

The Hawaiian reef coral Pocillopora meandrina Dana is restricted to turbulent environments. P. damicornis (L.) is most abundant on semi-protected reefs, while Montipora verrucosa (Lamarck) is characteristic of very calm environments. These species were grown in the laboratory under various conditions of water motion. Water motion influenced the growth, mortality, and reproductive rate, of each species differently. The differences may be attributed to morphological adaptations of the corals to their normal hydrodynamic environment. Water motion appears to influence corals by controlling the rate of exchange of material across the interface between the sea water and the coral tissue.     

Experimental fragmentation reduces sexual reproductive output by the reef-building coral Pocillopora damicornis

Natural and anthropogenic disturbances may fragment stony reef corals, but few quantitative data exist on the impacts of skeletal fragmentation on sexual reproduction in corals. We experimentally fragmented colonies of the branching coral Pocillopora damicornis and determined the number and size of planula larvae released during one lunar reproductive cycle. Partially fragmented colonies significantly delayed both the onset and peak period of planula release compared with intact control colonies. Most fragments removed from the corals died within 11–18 days, and released few planulae. The total number of planulae released per coral colony varied exponentially with remaining tissue volume, and was significantly lower in damaged versus undamaged colonies. However, the number of planulae produced per unit tissue volume, and planula size, did not vary with damage treatment. We conclude that even partial fragmentation of P. damicornis colonies (<25% of tissue removed) decreases their larval output by reducing reproductive tissue volume. Repeated breakage of corals, such as caused by intensive diving tourism or frequent storms, may lead to substantially reduced sexual reproduction. Therefore, reef management should limit human activities that fracture stony corals and lead to decreases in colony size and reproductive output. Accepted: 2 February 2000     

Coral growth with thermal stress and ocean acidification: lessons from the eastern tropical Pacific

The rapid growth of scleractinian corals is responsible for the persistence of coral reefs through time. Coral growth rates have declined over the past 30 years in the western Pacific, Indian, and North Atlantic Oceans. The spatial scale of this decline has led researchers to suggest that a global phenomenon like ocean acidification may be responsible. A multi-species inventory of coral growth from Pacific Panamá confirms that declines have occurred in some, but not all species. Linear extension declined significantly in the most important reef builder of the eastern tropical Pacific, Pocillopora damicornis, by nearly one-third from 1974 to 2006. The rate of decline in skeletal extension for P. damicornis from Pacific Panamá (0.9% year⁻¹) was nearly identical to massive Porites in the Indo-Pacific over the past 20–30 years (0.89–1.23% year⁻¹). The branching pocilloporid corals have shown an increased tolerance to recurrent thermal stress events in Panamá, but appear to be susceptible to acidification. In contrast, the massive pavonid corals have shown less tolerance to thermal stress, but may be less sensitive to acidification. These differing sensitivities will be a fundamental determinant of eastern tropical Pacific coral reef community structure with accelerating climate change that has implications for the future of reef communities worldwide.     

Corals shed bacteria as a potential mechanism of resilience to organic matter enrichment

Understanding the mechanisms of resilience of coral reefs to anthropogenic stressors is a critical step toward mitigating their current global decline. Coral–bacteria associations are fundamental to reef health and disease, but direct observations of these interactions remain largely unexplored. Here, we use novel technology, high-speed laser scanning confocal microscopy on live coral (Pocillopora damicornis), to test the hypothesis that corals exert control over the abundance of their associated bacterial communities by releasing (‘shedding'') bacteria from their surface, and that this mechanism can counteract bacterial growth stimulated by organic inputs. We also test the hypothesis that the coral pathogen Vibrio coralliilyticus can evade such a defense mechanism. This first report of direct observation with high-speed confocal microscopy of living coral and its associated bacterial community revealed a layer (3.3–146.8 μm thick) on the coral surface where bacteria were concentrated. The results of two independent experiments showed that the bacterial abundance in this layer was not sensitive to enrichment (5 mg l⁻¹ peptone), and that coral fragments exposed to enrichment released significantly more bacteria from their surfaces than control corals (P<0.01; 35.9±1.4 × 10⁵ cells cm⁻² coral versus 1.3±0.5 × 10⁵ cells cm⁻² coral). Our results provide direct support to the hypothesis that shedding bacteria may be an important mechanism by which coral-associated bacterial abundances are regulated under organic matter stress. Additionally, the novel ability to watch this ecological behavior in real-time at the microscale opens an unexplored avenue for mechanistic studies of coral–microbe interactions.     

Light Respiratory Processes and Gross Photosynthesis in Two Scleractinian Corals

The light dependency of respiratory activity of two scleractinian corals was examined using O₂ microsensors and CO₂ exchange measurements. Light respiration increased strongly but asymptotically with elevated irradiance in both species. Light respiration in Pocillopora damicornis was higher than in Pavona decussata under low irradiance, indicating species-specific differences in light-dependent metabolic processes. Overall, the coral P. decussata exhibited higher CO₂ uptake rates than P. damicornis over the experimental irradiance range. P. decussata also harboured twice as many algal symbionts and higher total protein biomass compared to P. damicornis, possibly resulting in self-shading of the symbionts and/or changes in host tissue specific light distribution. Differences in light respiration and CO₂ availability could be due to host-specific characteristics that modulate the symbiont microenvironment, its photosynthesis, and hence the overall performance of the coral holobiont.     

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.     

Mixed asexual and sexual reproduction in the Indo‐Pacific reef coral Pocillopora damicornis

Pocillopora damicornis is one of the best studied reef‐building corals, yet it's somewhat unique reproductive strategy remains poorly understood. Genetic studies indicate that P. damicornis larvae are produced almost exclusively parthenogenetically, and yet population genetic surveys suggest frequent sexual reproduction. Using microsatellite data from over 580 larvae from 13 colonies, we demonstrate that P. damicornis displays a mixed reproductive strategy where sexual and asexual larvae are produced simultaneously within the same colony. The majority of larvae were parthenogenetic (94%), but most colonies (10 of the 13) produced a subset of their larvae sexually. Logistic regression indicates that the proportion of sexual larvae varied significantly with colony size, cycle day, and calendar day. In particular, the decrease in sexual larvae with colony size suggests that the mixed reproductive strategy changes across the life of the coral. This unique shift in reproductive strategy leads to increasingly asexual replications of successful genotypes, which (in contrast to exclusive parthenogens) have already contributed to the recombinant gene pool.     

Large-amplitude internal waves sustain coral health during thermal stress

Ocean warming is a major threat for coral reefs causing widespread coral bleaching and mortality. Potential refugia are thus crucial for coral survival. Exposure to large-amplitude internal waves (LAIW) mitigated heat stress and ensured coral survival and recovery during and after an extreme heat anomaly. The physiological status of two common corals, Porites lutea and Pocillopora meandrina, was monitored in host and symbiont traits, in response to LAIW-exposure throughout the unprecedented 2010 heat anomaly in the Andaman Sea. LAIW-exposed corals of both species survived and recovered, while LAIW-sheltered corals suffered partial and total mortality in P. lutea and P. meandrina, respectively. LAIW are ubiquitous in the tropics and potentially generate coral refuge areas. As thermal stress to corals is expected to increase in a warming ocean, the mechanisms linking coral bleaching to ocean dynamics will be crucial to predict coral survival on a warming planet.     

Experimental evidence for high temperature stress as the cause of El Niño-coincident coral mortality

High temperature tolerance experiments performed on Pocillopora damicornis, a major reef-building coral in the tropical eastern Pacific, resulted in loss of zooxanthellae, histopathological abnormalities, and mortality similar to that observed during the severe 1982–83 El Niño-Southern Oscillation (ENSO) event. Coral vitality declined significantly at 30–32°C during a 10-week period, but remained high at normal temperatures (26–28°C). Laboratory time courses to coral morbidity and death were similar to those observed in the field. Experimental high temperatures had a greater negative effect on corals from the Gulf of Panama, which experiences seasonally cool upwellings, than on corals from the nonupwelling Gulf of Chiriqui. The condition of obligate symbiotic crustaceans (Trapezia, Alpheus) associated with experimental corals declined with their host's declining condition. All Gulf of Panama corals subjected to 32°C were dead after 5 weeks, and all of their associated crustacean symbionts were dead after 9 weeks. Gulf of Chiriqui corals at 30°C survived for 9 weeks and 42% of their crustacean symbionts were still alive after 10 weeks. Coral mortality in the Gulf of Panama was significantly higher (68.5%) after El Niño warming than after subsequent episodes of unusually intense cool upwellings (10.4%). Low temperature stress (cool currents and upwelling) has been generally suggested as the critical limiting condition that prevents extensive coral reef development in the eastern Pacific. Our results suggest that infrequent but severe ENSO sea warming events also may limit reef development in this region.     

Projected Near-Future Levels of Temperature and pCO2 Reduce Coral Fertilization Success

Increases in atmospheric carbon dioxide (pCO₂) are projected to contribute to a 1.1–6.4°C rise in global average surface temperatures and a 0.14–0.35 reduction in the average pH of the global surface ocean by 2100. If realized, these changes are expected to have negative consequences for reef-building corals including increased frequency and severity of coral bleaching and reduced rates of calcification and reef accretion. Much less is known regarding the independent and combined effects of temperature and pCO₂ on critical early life history processes such as fertilization. Here we show that increases in temperature (+3°C) and pCO₂ (+400 µatm) projected for this century negatively impact fertilization success of a common Indo-Pacific coral species, Acropora tenuis. While maximum fertilization did not differ among treatments, the sperm concentration required to obtain 50% of maximum fertilization increased 6- to 8- fold with the addition of a single factor (temperature or CO₂) and nearly 50- fold when both factors interact. Our results indicate that near-future changes in temperature and pCO₂ narrow the range of sperm concentrations that are capable of yielding high fertilization success in A. tenuis. Increased sperm limitation, in conjunction with adult population decline, may have severe consequences for coral reproductive success. Impaired sexual reproduction will further challenge corals by inhibiting population recovery and adaptation potential.     

The settlement behaviour of planulae larvae of the hermatypic coral Favia fragum (Esper)

Experiments on the settlement behaviour of planulae larvae of the reef coral Favia fragum (Esper) are described. The larvae are positively phototaxic upon release but reverse this and become attracted to dark surfaces, corners, crevices, and the undersides of objects on the bottom. Clean glass surfaces were preferred to surfaces covered with biological slime but there was no preference for rough against smooth surfaces. There was clear evidence of gregarious settlement behaviour, the planulae being able to recognize both adult colonies and previously settled juveniles. A distinction was made between crawling and swimming larvae, and the consequences of their differences in behaviour on the spatial distribution of Favia on reef are discussed. Settlement behaviour of Favia is similar in many respects to that of the Pacific reef coral Pocillopora damicornis (Dana) but is distinguished by gregarious settlement and by a preference for clean surfaces over surfaces covered with biological slime.     

Development of coral and zooxanthella‐specific microsatellites in three species of Pocillopora (Cnidaria,Scleractinia) from French Polynesia

Since the building of coral reefs results from the association of corals and zooxanthellae, their intracellular algal symbionts, genetic markers for both organisms are essential for studying the contribution of their respective dispersal to the resilience of endangered reef ecosystems. Very few microsatellites have been obtained in corals thus far. Here we report the successful cloning of six polymorphic microsatellites (allele number: 5–15) from Pocillopora verrucosa, P. meandrina and P. damicornis. Four of them amplified coral, and two amplified zooxanthella DNA.     

Nutrient cycling in early coral life stages: Pocillopora damicornis larvae provide their algal symbiont (Symbiodinium) with nitrogen acquired from bacterial associates

The waters surrounding coral reef ecosystems are generally poor in nutrients, yet their levels of primary production are comparable with those reported from tropical rain forests. One explanation of this paradox is the efficient cycling of nutrients between the coral host, its endosymbiotic alga Symbiodinium and a wide array of microorganisms. Despite their importance for the animals' fitness, the cycling of nutrients in early coral life stages and the initial establishment of partnerships with the microbes involved in these processes has received little scrutiny to date. Nitrogen is an essential but limited nutrient in coral reef ecosystems. In order to assess the early nutrient exchange between bacteria and corals, coral larvae of the species Pocillopora damicornis were incubated with two coral‐associated bacteria (Alteromonas sp., or Vibrio alginolyticus), prelabeled with the stable nitrogen isotope ¹⁵N. The incorporation and translocation of nitrogen from Vibrio‐ and Alteromonas bacteria into P. damicornis coral larvae and specifically into the coral‐symbiotic Symbiodinium were detected by nanoscale secondary ion mass spectrometry (NanoSIMS). A significant increase in the amount of enriched ¹⁵N (two to threefold compared to natural abundance) was observed in P. damicornis larvae within 8 h of incubation for both bacterial treatments (one‐way ANOVA, F_5,53 = 18.03, P = 0.004 for Alteromonas sp. and F_5,53 = 18.03, P = 0.0001 for V. alginolyticus). These findings reveal that coral larvae acquire nutrients previously taken up from the environment by bacteria. The additional nitrogen may increase the survival rate and fitness of the developing coral and therefore contribute to the successful maintenance of coral reefs.     

The recovery of coral genetic diversity in the Sunda Strait following the 1883 eruption of Krakatau

Surveys of microsatellite variation show that genetic diversity has largely recovered in two reef-building corals, Pocillopora damicornis and Seriatopora hystrix (Scleractinia: Pocilloporidae), on reefs which were decimated by the eruption of the volcano Krakatau in 1883. Assignment methods and gene flow estimates indicate that the recolonization of Krakatau occurred mainly from the closest upstream reef system, Pulau Seribu, but that larval input from other regions has also occurred. This pattern is clearer in S. hystrix, which is traditionally the more dispersal-limited species. Despite these observed patterns of larval dispersal, self-recruitment appears to now be the most important factor in supplying larvae to coral populations in Krakatau. This suggests that the colonization of devastated reefs can occur quickly through larval dispersal; however, their survival requires local sources of larvae for self-recruitment. This research supports the observation that the recovery of genetic diversity in coral reef animals can occur on the order of decades and centuries rather than millennia. Conservation measures aimed at sustaining coral reef populations in Krakatau and elsewhere should include both the protection of upstream source populations for larval replenishment should disaster occur as well as the protection of large adult colonies to serve as local larval sources.