Photochemical response of the scleractinian coral Stylophora pistillata to some sunscreen ingredients

Coral Reefs - Ultraviolet (UV) filters and preservatives, which are common constituents of sunscreens and other cosmetics, are reported as a threat for coastal coral reef ecosystems; however, few...     

Response of a scleractinian coral, Stylophora pistillata, to iron and nitrate enrichment

The purpose of this study was to determine whether the addition of iron alone or in combination with nitrate affects growth and photosynthesis of the scleractinian coral, Stylophora pistillata, and its symbiotic dinoflagellates. For this purpose, we used three series of two tanks for a 3-week enrichment with iron (Fe), nitrate (N) and nitrate+iron (NFe). Two other tanks were kept as a control (C). Stock solutions of FeCl(3) and NaNO(3) were diluted to final concentrations of 6 nM Fe and 2 &mgr;M N and continuously pumped from batch tanks into the experimental tanks with a peristaltic pump. Results obtained showed that iron addition induced a significant increase in the areal density of zooxanthellae (ANOVA, p=0.0013; change from 6.3+/-0.7x10(5) in the control to 8.5+/-0.6x10(5) with iron). Maximal gross photosynthetic rates normalized per surface area also significantly increased following iron enrichment (ANOVA, p=0.02; change from 1.23+/-0.08 for the control colonies to 1.81+/-0.24 &mgr;mol O(2) cm(-2) h(-1) for the iron-enriched colonies). There was, however, no significant difference in the photosynthesis normalized on a per cell basis. Nitrate enrichment alone (2 &mgr;M) did not significantly change the zooxanthellae density or the rates of photosynthesis. Nutrient addition (both iron and nitrogen) increased the cell-specific density of the algae (CSD) compared to the control (G-test, p=0.3x10(-9)), with an increase in the number of doublets and triplets. CSD was equal to 1.70+/-0.04 in the Fe-enriched colonies, 1.54+/-0.12 in the N- and NFe-enriched colonies and 1.37+/-0.02 in the control. Growth rates measured after 3 weeks in colonies enriched with Fe, N and NFe were 23%, 34% and 40% lower than those obtained in control colonies (ANOVA, p=0.011).     

In situ release of mucus and DOC-lipid from the corals Acropora variabilis and Stylophora pistillata in different light regimes

Rates of mucus and DOC-lipid release were determined for colonies of Acropora variabilis and Stylophora pistillata at 5 m depth and for a colony of A. variabilis at 23 m depth. In addition, colonies at 5 m were shaded to simulate ambient irradiance at 6 m, 10 m and 16 m depth to evaluate the effect of light on the rates of release. A. variabilis released more mucus and DOC-lipid at 5 m than at 23 m depth. For both corals, the night rates were about 30% those of the day. A reduction in total integrated irradiance decreased mucus output from the corals. Similarly, DOC-lipid release showed a diurnal pattern and diminished with reduction in daily irradiance. For both coral species, DOC-lipid release rates were greater in the afternoon than in the morning. The night rates were less than 55% those of the day. The DOC-lipid comprised wax esters and a phospholipid fraction. The diurnal variation was due to changes in yield of wax esters which contributed >90% of the carbon released as DOC-lipid. In situ release of mucus and DOC-lipid was infuenced by light effects on phototrophic carbon metabolism. A daily budget for carbon released as mucus and DOC-lipid was estimated for each coral species at 5 m depth.     

Carbonic anhydrase in the scleractinian coral Stylophora pistillata: characterization, localization, and role in biomineralization

Carbonic anhydrases (CA) play an important role in biomineralization from invertebrates to vertebrates. Previous experiments have investigated the role of CA in coral calcification, mainly by pharmacological approaches. This study reports the molecular cloning, sequencing, and immunolocalization of a CA isolated from the scleractinian coral Stylophora pistillata, named STPCA. Results show that STPCA is a secreted form of alpha-CA, which possesses a CA catalytic function, similar to the secreted human CAVI. We localized this enzyme at the calicoblastic ectoderm level, which is responsible for the precipitation of the skeleton. This localization supports the role of STPCA in the calcification process. In symbiotic scleractinian corals, calcification is stimulated by light, a phenomenon called "light-enhanced calcification" (LEC). The mechanism by which symbiont photosynthesis stimulates calcification is still enigmatic. We tested the hypothesis that coral genes are differentially expressed under light and dark conditions. By real-time PCR, we investigated the differential expression of STPCA to determine its role in the LEC phenomenon. Results show that the STPCA gene is expressed 2-fold more during the dark than the light. We suggest that in the dark, up-regulation of the STPCA gene represents a mechanism to cope with night acidosis.     

Calcification and associated physiological parameters during a stress event in the scleractinian coral Stylophora pistillata

High calcification rates observed in reef coral organisms are due to the symbiotic relationship established between scleractinian corals and their photosynthetic dinoflagellates, commonly called zooxanthellae. Zooxanthellae are known to enhance calcification in the light, a process referred as "light-enhanced calcification". The disruption of the relationship between corals and their zooxanthellae leads to bleaching. Bleaching is one of the major causes of the present decline of coral reefs related to climate change and anthropogenic activities. In our aquaria, corals experienced a chemical pollution leading to bleaching and ending with the death of corals. During the time course of this bleaching event, we measured multiple parameters and could evidence four major consecutive steps: 1) at month 1 (January 2005), the stress affected primarily the photosystem II machinery of zooxanthellae resulting in an immediate decrease of photosystem II efficiency, 2) at month 2, the stress affected the photosynthetic production of O2 by zooxanthellae and the rate of light calcification, 3) at month 3, there was a decrease in both light and dark calcification rates, the appearance of the first oxidative damage in the zooxanthellae, the disruption of symbiosis, 4) and finally the death of corals at month 6.     

Caribbean corals in crisis: record thermal stress, bleaching, and mortality in 2005

Background

The rising temperature of the world''s oceans has become a major threat to coral reefs globally as the severity and frequency of mass coral bleaching and mortality events increase. In 2005, high ocean temperatures in the tropical Atlantic and Caribbean resulted in the most severe bleaching event ever recorded in the basin.

Methodology/Principal Findings

Satellite-based tools provided warnings for coral reef managers and scientists, guiding both the timing and location of researchers'' field observations as anomalously warm conditions developed and spread across the greater Caribbean region from June to October 2005. Field surveys of bleaching and mortality exceeded prior efforts in detail and extent, and provided a new standard for documenting the effects of bleaching and for testing nowcast and forecast products. Collaborators from 22 countries undertook the most comprehensive documentation of basin-scale bleaching to date and found that over 80% of corals bleached and over 40% died at many sites. The most severe bleaching coincided with waters nearest a western Atlantic warm pool that was centered off the northern end of the Lesser Antilles.

Conclusions/Significance

Thermal stress during the 2005 event exceeded any observed from the Caribbean in the prior 20 years, and regionally-averaged temperatures were the warmest in over 150 years. Comparison of satellite data against field surveys demonstrated a significant predictive relationship between accumulated heat stress (measured using NOAA Coral Reef Watch''s Degree Heating Weeks) and bleaching intensity. This severe, widespread bleaching and mortality will undoubtedly have long-term consequences for reef ecosystems and suggests a troubled future for tropical marine ecosystems under a warming climate.     

Differential susceptibility to oxidative stress of two scleractinian corals: antioxidant functioning of mycosporine-glycine

This study examined the importance of mycosporine-glycine (Myc-Gly) as a functional antioxidant in the thermal-stress susceptibility of two scleractinian corals, Platygyra ryukyuensis and Stylophora pistillata. Photochemical efficiency of PSII (F_v/F_m), activity of antioxidant enzymes, superoxide dismutase (SOD) and catalase (CAT), and composition and abundance of mycosporine-like amino acids (MAAs) in the coral tissue and in symbiotic zooxanthellae were analyzed during 12-h exposure to high temperature (33 °C). After 6- and 12-h exposures at 33 °C, S. pistillata showed a significantly more pronounced decline in F_v/F_m compared to P. ryukyuensis. A 6-h exposure at 33 °C induced a significant increase in the activities of SOD and CAT in both host and zooxanthellae components of S. pistillata while in P. ryukyuensis a significant increase was observed only in the CAT activity of zooxanthellae. After 12-h exposure, the SOD activity of P. ryukyuensis was unaffected in the coral tissue but slightly increased in zooxanthellae, whereas the CAT activity in the coral tissue showed a 2.5-fold increase. The total activity of antioxidant enzymes was significantly higher in S. pistillata than in P. ryukyuensis, suggesting that P. ryukyuensis is less sensitive to oxidative stress than S. pistillata. This differential susceptibility of the corals is consistent with a 20-fold higher initial concentration of Myc-Gly in P. ryukyuensis compared to S. pistillata. In the coral tissue and zooxanthellae of both species investigated, the first 6 h of exposure to thermal stress induced a pronounced reduction in the abundance of Myc-Gly but not in other MAAs. When exposure was prolonged to 12 h, the Myc-Gly pool continued to decrease in P. ryukyuensis and was completely depleted in S. pistillata. The delay in the onset of oxidative stress in P. ryukyuensis and the dramatic increase in the activities of the antioxidant enzymes in S. pistillata, which contains low concentrations of Myc-Gly suggest that Myc-Gly provides rapid protection against oxidative stress before the antioxidant enzymes are induced. These findings strongly suggest that Myc-Gly is functioning as a biological antioxidant in the coral tissue and zooxanthellae and demonstrate its importance in the survival of reef-building corals under thermal stress.     

Physiology and taxonomy of scleractinian corals: a case study in the genus Stylophora

The morphology and skeletal characteristics of colonies of the coral genus Stylophora living on the reef edge at 1 m depth on the Jordanian coast of the Gulf of Aqaba (Red Sea) are those of S. mordax (Dana 1846) which has not been reported previously from that area. These colonies were considered earlier as ecomorphs of S. pistillata (Esper 1797) which lives down to at least 67 m on the reef slopes. Growth, organic content and metabolism were compared in colonies living at different depths (1,5,10 and 30 m). The trends of twelve parameters between 1 and 5 m were different from the variation observed between 5 and 30 m. Colonies living at 1 m have a higher chlorophyll content but a lower metabolic activity and growth rate than colonies living at 5 m. Most of these pecularities cannot be explained by the influence of environmental factors. It is therefore suggested that S. mordax is a valid taxon.     

Photophysiological stress in scleractinian corals in response to short-term sedimentation

Effects of short-term sedimentation on common coastal coral species were investigated in laboratory and field experiments on the Great Barrier Reef (GBR) using pulse-amplitude modulated (PAM) chlorophyll fluorometry. In the laboratory, changes in maximal quantum yields of photosystem II (F_v/F_m) in Montipora peltiformis were examined in response to the amount of sedimentation (79-234 mg cm⁻²) and duration of exposure (0-36 h). In control colonies, F_v/F_m ranged from 0.67 to 0.71, and did not show any temporal trend, while maximum yields of sediment-covered fragments declined steadily and reached levels below 0.1 in most colonies after 36 h coverage. Maximal quantum yield in M. peltiformis declined linearly in relation to both the amount of sediment deposited per unit surface area and the duration of exposure. Zooxanthellae densities and chlorophyll concentrations per unit area of sediment-treated corals decreased in the same manner, however, their responses were not quite as strong as the changes in F_v/F_m. Within the ranges measured, sedimentation stress of colonies exposed to large amounts of sediment for short periods of time was similar to that exposed to low amounts of sediments for prolonged periods of time. Colonies were recovered from short-term, or low-level, sedimentation within <36 h, whereas long-term exposure, or high levels of sedimentation, killed exposed colony parts. Field experiments comparing susceptibilities of common coastal coral species towards sedimentation showed significant reductions in effective quantum yields (ΔF/F_m′) in 9 out of 12 common coastal species after 22 h of exposure. Three out of twelve investigated species were not affected by the experimental application of sediments (Galaxea fascicularis, Fungia crassa, and Pectinia lactuca). Our results suggest that anthropogenic sediment deposition can negatively affect the photosynthetic activity of zooxanthellae and thus the viability of corals. However, the results also showed the ability of corals to compartmentalise sedimentation stress, as the photosynthetic activity only from tissues directly underneath the sediment declined, whereas that of adjacent clean tissues did not change measurably.     

Coral bleaching response index: a new tool to standardize and compare susceptibility to thermal bleaching

As coral bleaching events become more frequent and intense, our ability to predict and mitigate future events depends upon our capacity to interpret patterns within previous episodes. Responses to thermal stress vary among coral species; however the diversity of coral assemblages, environmental conditions, assessment protocols, and severity criteria applied in the global effort to document bleaching patterns creates challenges for the development of a systemic metric of taxon‐specific response. Here, we describe and validate a novel framework to standardize bleaching response records and estimate their measurement uncertainties. Taxon‐specific bleaching and mortality records (2036) of 374 coral taxa (during 1982–2006) at 316 sites were standardized to average percent tissue area affected and a taxon‐specific bleaching response index (taxon‐BRI) was calculated by averaging taxon‐specific response over all sites where a taxon was present. Differential bleaching among corals was widely variable (mean taxon‐BRI = 25.06 ± 18.44%, ±SE). Coral response may differ because holobionts are biologically different (intrinsic factors), they were exposed to different environmental conditions (extrinsic factors), or inconsistencies in reporting (measurement uncertainty). We found that both extrinsic and intrinsic factors have comparable influence within a given site and event (60% and 40% of bleaching response variance of all records explained, respectively). However, when responses of individual taxa are averaged across sites to obtain taxon‐BRI, differential response was primarily driven by intrinsic differences among taxa (65% of taxon‐BRI variance explained), not conditions across sites (6% explained), nor measurement uncertainty (29% explained). Thus, taxon‐BRI is a robust metric of intrinsic susceptibility of coral taxa. Taxon‐BRI provides a broadly applicable framework for standardization and error estimation for disparate historical records and collection of novel data, allowing for unprecedented accuracy in parameterization of mechanistic and predictive models and conservation plans.     

Evidence of an inflammatory-like response in non-normally pigmented tissues of two scleractinian corals

Increasing evidence of links between climate change, anthropogenic stress and coral disease underscores the importance of understanding the mechanisms by which reef-building corals resist infection and recover from injury. Cellular inflammation and melanin-producing signalling pathway are two mechanisms employed by invertebrates to remove foreign organisms such as pathogens, but they have not been recorded previously in scleractinian corals. This study demonstrates the presence of the phenoloxidase (PO) activating melanin pathway in two species of coral, Acropora millepora and a massive species of Porites, which both develop local pigmentation in response to interactions with a variety of organisms. L-DOPA (3-(3,4-dihydroxyphenyl)-L-alanine) substrate-based enzyme activation assays demonstrated PO activity in healthy tissues of both species and upregulation in pigmented tissues of A. millepora. Histological staining conclusively identified the presence of melanin in Porites tissues. These results demonstrate that the PO pathway is active in both coral species. Moreover, the upregulation of PO activity in areas of non-normal pigmentation in A. millepora and increased melanin production in pigmented Porites tissues suggest the presence of a generalized defence response to localized stress. Interspecific differences in the usage of pathways involved in innate immunity may underlie the comparative success of massive Porites sp. as long-lived stress tolerators.     

Recruitment,mortality, and resilience potential of scleractinian corals at Eilat,Red Sea

Events of mass coral bleaching and mortality have increased in recent decades worldwide, making coral recruitment more important than ever in sustaining coral-reef ecosystems and ensuring their resilience. During the last four decades, the coral reefs of Eilat have undergone severe deterioration due to both anthropogenic and natural causes. Recruitment failure has been frequently suggested as one of the main mechanisms underlying this deterioration. Here we assess the demographic replenishment and resilience potential of the local reefs, i.e., the potential for new sexually derived corals to recruit and exceed the community’s mortality rate. We present a detailed analysis of coral community demography, obtained by means of high-resolution photographic monitoring of permanently marked plots. Coral spats as small as 1 mm were documented and the detailed dynamics of coral recruitment and mortality were recorded, in addition to other common ecological measurements. The cumulative quantity of recruited individuals was twofold to fivefold higher than total mortality. The most significant predictor variable for coral recruitment among all ecological parameters measured was the available substrate for settlement, and the survival of recruited corals was correlated with reef structural complexity. Two consecutive annual reproductive seasons (June–September of each year) with high recruitment rates were monitored. Combined with the high survival of recruits and the increase in coral live cover and abundance, the findings from this study indicate an encouraging potential for recovery of these reefs.

     

Competitive strategies of soft corals (Coelenterata: Octocorallia). II. Variable defensive responses and susceptibility to scleractinian corals

Interactions involving competition for space between several species of alcyonacean and scleractinian corals were assessed experimentally on Britomart Reef, central region of the Great Barrier Reef, Australia. Colonies of three soft coral species, Sarcophyton ehrenbergi Marenzeller, Nephthea brassica Kukenthal, and Capnella lacertiliensis Macfayden Forskal (Coelenterata:Alcyonacea) were relocated within stands of two scleractinian corals, Parités andrewsi Vaughan (= P. cylindrica Dana) and Pavona cactus Förskal (Coelenterata:Scleractinia). Undisturbed scleractinian and relocated alcyonacean controls were also monitored.Alcyonacean corals induced necrosis of tissue in scleractinian corals. Necrosis was significantly more pronounced when colonies were in contact but was also observed in the absence of contact, implicating the presence of active allelopathic agents. Scleractinian coral species varied in their susceptibility to the ill effects of alcyonaceans, with Pontes andrewsi being more susceptible than Pavona cactus. Of the soft corals, Nephthea caused the highest degree of mortality in the two scleractinian corals examined and Sarcophyton the least. Some soft corals appear to retain their toxins while others release them, implying a combination of anti-predatory and anti-competitor roles for the secondary metabolites. Scleractinian corals were often overgrown by soft corals.Both species of scleractinian corals were found to cause approximately equal amounts of tissue necrosis in alcyonaceans. These effects were more pronounced when colonies were in direct contact. The necrotic effects among alcyonacean corals were species-specific. Alcyonaceans also overgrew scleractinian corals and secreted a protective polysaccharide layer in areas proximal to scleractinians. Secretion of this layer was stimulated differentially by the two scleractinian species and also varied in frequency of occurrence among the alcyonaceans.High levels of tissue necrosis were observed in both groups of organisms within 3 wk of initiation of the experiment. Necrosis increased with time in the scleractinian corals and decreased in the alcyonaceans. The development of a protective polysaccharide layer in the alcyonaceans increased with time.     

Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress

Background

Coral bleaching events vary in severity, however, to date, the hierarchy of susceptibility to bleaching among coral taxa has been consistent over a broad geographic range and among bleaching episodes. Here we examine the extent of spatial and temporal variation in thermal tolerance among scleractinian coral taxa and between locations during the 2010 thermally induced, large-scale bleaching event in South East Asia.

Methodology/Principal Findings

Surveys to estimate the bleaching and mortality indices of coral genera were carried out at three locations with contrasting thermal and bleaching histories. Despite the magnitude of thermal stress being similar among locations in 2010, there was a remarkable contrast in the patterns of bleaching susceptibility. Comparisons of bleaching susceptibility within coral taxa and among locations revealed no significant differences between locations with similar thermal histories, but significant differences between locations with contrasting thermal histories (Friedman = 34.97; p<0.001). Bleaching was much less severe at locations that bleached during 1998, that had greater historical temperature variability and lower rates of warming. Remarkably, Acropora and Pocillopora, taxa that are typically highly susceptible, although among the most susceptible in Pulau Weh (Sumatra, Indonesia) where respectively, 94% and 87% of colonies died, were among the least susceptible in Singapore, where only 5% and 12% of colonies died.

Conclusions/Significance

The pattern of susceptibility among coral genera documented here is unprecedented. A parsimonious explanation for these results is that coral populations that bleached during the last major warming event in 1998 have adapted and/or acclimatised to thermal stress. These data also lend support to the hypothesis that corals in regions subject to more variable temperature regimes are more resistant to thermal stress than those in less variable environments.     

Environmental implications of skeletal micro-density and porosity variation in two scleractinian corals

The correlations between skeletal parameters (bulk density, micro-density and porosity), coral age and sea surface temperature were assessed along a latitudinal gradient in the zooxanthellate coral Balanophyllia europaea and in the azooxanthellate coral Leptopsammia pruvoti. In both coral species, the variation of bulk density was more influenced by the variation of porosity than of micro-density. With increasing polyp age, B. europaea formed denser and less porous skeletons while L. pruvoti showed the opposite trend, becoming less dense and more porous. B. europaea skeletons were generally less porous (more dense) than those of L. pruvoti, probably as a consequence of the different habitats colonized by the two species. Increasing temperature had a negative impact on the zooxanthellate species, leading to an increase of porosity. In contrast, micro-density increased with temperature in the azooxanthellate species. It is hypothesized that the increase in porosity with increasing temperatures observed in B. europaea could depend on an attenuation of calcification due to an inhibition of the photosynthetic process at elevated temperatures, while the azooxanthellate species appears more resistant to variations of temperature, highlighting possible differences in the sensitivity/tolerance of these two coral species to temperature changes in face of global climate change.     

A multi-trait systems approach reveals a response cascade to bleaching in corals

Background

Climate change causes the breakdown of the symbiotic relationships between reef-building corals and their photosynthetic symbionts (genus Symbiodinium), with thermal anomalies in 2015–2016 triggering the most widespread mass coral bleaching on record and unprecedented mortality on the Great Barrier Reef. Targeted studies using specific coral stress indicators have highlighted the complexity of the physiological processes occurring during thermal stress, but have been unable to provide a clear mechanistic understanding of coral bleaching.

Results

Here, we present an extensive multi-trait-based study in which we compare the thermal stress responses of two phylogenetically distinct and widely distributed coral species, Acropora millepora and Stylophora pistillata, integrating 14 individual stress indicators over time across a simulated thermal anomaly. We found that key stress responses were conserved across both taxa, with the loss of symbionts and the activation of antioxidant mechanisms occurring well before collapse of the physiological parameters, including gross oxygen production and chlorophyll a. Our study also revealed species-specific traits, including differences in the timing of antioxidant regulation, as well as drastic differences in the production of the sulfur compound dimethylsulfoniopropionate during bleaching. Indeed, the concentration of this antioxidant increased two-fold in A. millepora after the corals started to bleach, while it decreased 70% in S. pistillata.

Conclusions

We identify a well-defined cascading response to thermal stress, demarking clear pathophysiological reactions conserved across the two species, which might be central to fully understanding the mechanisms triggering thermally induced coral bleaching. These results highlight that bleaching is a conserved mechanism, but specific adaptations linked to the coral’s antioxidant capacity drive differences in the sensitivity and thus tolerance of each coral species to thermal stress.

     

Sexual reproduction,development and larval biology in scleractinian corals

This paper brings together widely scattered information on sexual reproduction in scleractinian corals. It includes a review of information and ideas on sex determination, gametogenesis, gametogenic cycles, fertilization and embryonic development, spawning and planula release, larval behavior, settlement and metamorphosis. The review deals with corals from different habitats and organismic assemblages, including tropical reef corals, temperate water corals, solitary and colonial forms. A summary table of coral species and their known reproductive characteristics is presented.