The evolutionary history of Symbiodinium and scleractinian hosts - Symbiosis, diversity, and the effect of climate change

Marine invertebrates representing at least five phyla are symbiotic with dinoflagellates from the genus Symbiodinium. This group of single-celled protists was once considered to be a single pandemic species, Symbiodinium microadriaticum. Molecular investigations over the past 25 years have revealed, however, that Symbiodinium is a diverse group of organisms with at least eight (A-H) divergent clades that in turn contain multiple molecular subclade types. The diversity within this genus may subsequently determine the response of corals to normal and stressful conditions, leading to the proposal that the symbiosis may impart unusually rapid adaptation to environmental change by the metazoan host. These questions have added importance due to the critical challenges that corals and the reefs they build face as a consequence of current rapid climate change. This review outlines our current understanding of the diverse genus Symbiodinium and explores the ability of this genus and its symbioses to adapt to rapid environmental change. (c) 2006 Rubel Foundation, ETH Zurich. Published by Elsevier GmbH. All rights reserved.

Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching

Rising sea temperatures are increasing the incidences of mass coral bleaching (the dissociation of the coral-algal symbiosis) and coral mortality. In this study, the effects of bleaching (induced by elevated light and temperature) on the condition of symbiotic dinoflagellates (Symbiodinium sp.) within the tissue of the hard coral Stylophora pistillata (Esper) were assessed using a suite of techniques. Bleaching of S. pistillata was accompanied by declines in the maximum potential quantum yield of photosynthesis (F-v/F-m, measured using pulse amplitude modulated [PAM] fluorometry), an increase in the number of Sytox-green-stained algae (indicating compromised algal membrane integrity and cell death), an increase in 2',7'-dichlorodihydrofluroscein diacetate (H(2)DCFDA)stained algae (indicating increased oxidative stress), as well as ultrastructural changes (vacuolisation, losses of chlorophyll, and an increase in accumulation bodies). Algae expelled from S. pistillata exhibited a complete disorganisation of cellular contents; expelled cells contained only amorphous material. In situ samples taken during a natural mass coral bleaching event on the Great Barrier Reef in February 2002 also revealed a high number of Sytox-labelled algae cells in symbio. Dinoflagellate degeneration during bleaching seems to be similar to the changes resulting from senescence-phase cell death in cultured algae. These data support a role for oxidative stress in the mechanism of coral bleaching and highlight the importance of algal degeneration during the bleaching of a reef coral.

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

Spatial and temporal patterns of coral bleaching around Buck Island Reef National Monument, St. Croix, U.S. Virgin Islands [poster]

Limited information currently exists on the recovery periods of bleached corals as well as the spatial extent, causative factors, and the overall impact of bleaching on coral reef ecosystems. During October, 2005, widespread coral bleaching was observed within Buck Island Reef National Monument (BUIS) St. Croix, USVI. The bleaching event was preceded by 10 weeks of higher than average water temperatures (28.9-30.1°C). Random transects (100 square meters) over hard bottom habitats (N=94) revealed that approximately 51% of live coral cover was bleached. Nineteen of 23 coral species within 16 genera and two hydrocoral species exhibited signs of bleaching; species-specific bleaching patterns were variable throughout the study area. Coral cover for Montastraea annularisand species of the genus Agariciawere the most affected, while other species exhibited variability to bleaching. Although a weak but significant negative relationship (r2=0.10, P=0.0220) was observed, bleaching was evident at all depths (1.5-28 m). Bleaching was spatially autocorrelated (P=0.001) and hot-spot analysis identified a cluster of high bleaching stations northeast of Buck Island. Bleaching was significantly reduced within all depth zones and habitat types upon subsequent monitoring during April (15%) and October (3%) 2006.

Response of a floodplain fish community to river-floodplain connectivity: natural versus managed reconnection

To restore lateral connectivity in highly regulated river-floodplain systems, it has become necessary to implement localized, "managed" connection flows, made possible using floodplain irrigation infrastructure. These managed flows contrast with "natural", large-scale, overbank flood pulses. We compared the effects of a managed and a natural connection event on (i) the composition of the large-bodied fish community and (ii) the structure of an endangered catfish population of a large floodplain lake. The change in community composition following the managed connection was not greater than that exhibited between seasons or years during disconnection. By contrast, the change in fish community structure following the natural connection was much larger than that attributed to background, within-and between-year variability during disconnection. Catfish population structure only changed significantly following the natural flood. While the natural flood increased various population rates of native fishes, it also increased those of non-native carp, a pest species. To have a positive influence on native biodiversity, environmental flows may need to be delivered to floodplains in a way that simulates the properties of natural flood pulses. A challenge, however, will be managing river-floodplain connectivity to benefit native more than non-native species.

Rapid transition in the structure of a coral reef community: The effects of coral bleaching and physical disturbance

Coral reef communities are in a state of change throughout their geographical range. Factors contributing to this change include bleaching (the loss of algal symbionts), storm damage, disease, and increasing abundance of macroalgae. An additional factor for Caribbean reefs is the aftereffects of the epizootic that reduced the abundance of the herbivorous sea urchin, Diadema antillarum. Although coral reef communities have undergone phase shifts, there are few studies that document the details of such transitions. We report the results of a 40-month study that documents changes in a Caribbean reef community affected by bleaching, hurricane damage, and an increasing abundance of macroalgae. The study site was in a relatively pristine area of the reef surrounding the island of San Salvador in the Bahamas. Ten transects were sampled every 3–9 months from November 1994 to February 1998. During this period, the corals experienced a massive bleaching event resulting in a significant decline in coral abundance. Algae, especially macroalgae, increased in abundance until they effectively dominated the substrate. The direct impact of Hurricane Lili in October 1996 did not alter the developing community structure and may have facilitated increasing algal abundance. The results of this study document the rapid transition of this reef community from one in which corals and algae were codominant to a community dominated by macroalgae. The relatively brief time period required for this transition illustrates the dynamic nature of reef communities.

Endolithic algae photoacclimate to increased irradiance during coral bleaching

The photoacclimation of endolithic algae ( of the genus Ostreobium) inhabiting the skeleton of the Mediterranean coral Oculina patagonica during a bleaching event was examined. Pulse amplitude modulated (PAM) chlorophyll fluorescence techniques in situ were used to assess the photosynthetic efficiency of endolithic algae in the coral skeleton and the symbiotic dinoflagellates (zooxanthellae) in the coral tissue. Relative photosynthetic electron transport rates (ETRs) of the endolithic algae under bleached areas of the colony were significantly higher than those of endolithic algae from a healthy section of the colony and those of zooxanthellae isolated from the same section. Endolithic algae under healthy parts of the colony demonstrated an ETRmax of 16.5% that of zooxanthellae from tissue in the same section whereas endolithic algae under bleached sections showed ETRmax values that were 39% of those found for healthy zooxanthellae. The study demonstrates that endolithic algae undergo photoacclimation with increased irradiance reaching the skeleton. As PAM fluorometry has become a major tool for assessing levels of stress and bleaching in corals, the importance of considering the contribution of the endolithic algae to the overall chlorophyll fluorescence measured is highlighted.

Increased mortality and photoinhibition in the symbiotic dinoflagellates of the Indo-Pacific coral Stylophora pistillata (Esper) after summer bleaching

Coral bleaching (the loss of symbiotic dinoflagellates from reef-building corals) is most frequently caused by high-light and temperature conditions. We exposed the explants of the hermatypic coral Stylophora pistillata to four combinations of light and temperature in late spring and also in late summer. During mid-summer, two NOAA bleaching warnings were issued for Heron Island reef (Southern Great Barrier Reef, Australia) when sea temperature exceeded the NOAA bleaching threshold, and a 'mild' (in terms of the whole coral community) bleaching event occurred, resulting in widespread S. pistillata bleaching and mortality. Symbiotic dinoflagellate biomass decreased by more than half from late spring to late summer (from 2.5x10(6) to 0.8x10(6) dinoflagellates cm(2) coral tissue), and those dinoflagellates that remained after summer became photoinhibited more readily (dark-adapted F (V) : F (M) decreased to (0.3 compared with 0.4 in spring), and died in greater numbers (up to 17% dinoflagellate mortality compared with 5% in the spring) when exposed to artificially elevated light and temperature. Adding exogenous antioxidants (D-mannitol and L-ascorbic acid) to the water surrounding the coral had no clear effect on either photoinhibition or symbiont mortality. These data show that light and temperature stress cause mortality of the dinoflagellate symbionts within the coral, and that susceptibility to light and temperature stress is strongly related to coral condition. Photoinhibitory mechanisms are clearly involved, and will increase through a positive feedback mechanism: symbiont loss promotes further symbiont loss as the light microenvironment becomes progressively harsher.

Specificity, stability and comparative physiology of coral-Symbiodinium mutualisms: Evaluating the potential for acclimation and/or adaptation in reef corals

The relationship between reef corals and endosymbiotic dinoflagellates is fundamental to the existence of coral reefs. To evaluate the fidelity of coral-Symbiodinium mutualisms, corals maintained in aquaria for years were analyzed by denaturant gradient gel electrophoresis (DGGE). Comparing Symbiodinium populations of captive aquarium colonies with known associations in nature is a practical way of examining partner flexibility. The finding of "normal" symbiont populations in corals existing under highly variable conditions supports the premise that most coral colonies possess stable associations. High sensitivity real-time PCR (rtPCR) was used to evaluate background populations of the putatively stress-tolerant Symbiodinium D in reef corals of the Caribbean. Analyses of samples collected during periods of environmental stability indicate the ability of Symbiodinium D to associate with a wider diversity of host taxa than previously recognized. To gain a broader perspective with regard to the ecology of Symbiodinium D1a, rtPCR and DGGE were used to evaluate the symbiont populations of reef corals from Barbados before and after the 2005 mass coral bleaching. Background populations were observed in 56% of the host genera prior to observations of bleaching. These findings indicate that 'stress', not 'bleaching', caused the displacement of 'natural' symbiont population and the opportunistic proliferation of D1a in many host taxa. Of the 12 host taxa monitored before and after the bleaching event, there was a 40% increase in colonies hosting Symbiodinium D1a. Together, these studies elucidate the mechanism responsible for recent observations reporting the emergence of Symbiodinium D following thermal disturbances. These observations are now most easily explained as the disproportionate growth of existing in hospite symbiont populations, rather than novel symbiont acquisition subsequent to bleaching. To evaluate the comparative "fitness" of corals able to host multiple symbiont types, rates of calcification were measured in P. verrucosa hosting either Symbiodinium C1b-c or D1 at elevated temperature. Rates of calcification decreased significantly for both host-symbiont combinations, but differences attributable to symbiont composition were not detected. This research improves our knowledge of the symbiosis biology and ecology of reef corals and contributes information necessary to most accurately predict the response of these ecosystems to global climate changes.

Long-term monitoring of habitats and reef fish found inside and outside the U.S. Virgin Islands Coral Reef National Monument: a comparative assessment

The primary objective of this study was to assess the efficacy of the Virgin Islands Coral Reef National Monument (VICR), a marine protected area in St John, US Virgin Islands. Surveys of habitat and fishes inside and outside of VICR were conducted in 2003-2008. Areas outside the VICR had significantly more scleractinian corals, greater habitat complexity, and greater species richness and density of reef fishes than areas inside., Areas inside and outside the VICR exhibited significant decreases in percent scleractinian coral coverage over the study period. A contrasting trend of increasing macroalgal cover was also observed. No clear effect of the severe 2005 coral bleaching event was observed suggesting other causal factors. No obvious trends in the fish community were observed across the study period. The significant decline in habitat condition, coupled with the initial incorporation of some of the more degraded reefs into the marine protected area may result in a longer time period necessary to detect positive changes in the St. John coral reef ecosystem and associated reef fish abundance and community structure.

Explosive development of winter storm Xynthia over the subtropical North Atlantic Ocean

In winter of 2009–2010 south-western Europe was hit by several destructive windstorms. The most important was Xynthia (26–28 February 2010), which caused 64 reported casualties and was classified as the 2nd most expensive natural hazard event for 2010 in terms of economic losses. In this work we assess the synoptic evolution, dynamical characteristics and the main impacts of storm Xynthia, whose genesis, development and path were very uncommon. Wind speed gusts observed at more than 500 stations across Europe are evaluated as well as the wind gust field obtained with a regional climate model simulation for the entire North Atlantic and European area. Storm Xynthia was first identified on 25 February around 30° N, 50° W over the subtropical North Atlantic Ocean. Its genesis occurred on a region characterized by warm and moist air under the influence of a strong upper level wave embedded in the westerlies. Xynthia followed an unusual SW–NE path towards Iberia, France and central Europe. The role of moist air masses on the explosive development of Xynthia is analysed by considering the evaporative sources. A lagrangian model is used to identify the moisture sources, sinks and moisture transport associated with the cyclone during its development phase. The main supply of moisture is located over an elongated region of the subtropical North Atlantic Ocean with anomalously high SST, confirming that the explosive development of storm Xynthia had a significant contribution from the subtropics.

Avaliação da cobertura e monitoramento do branqueamento de corais nos

Coral bleaching has been increasingly the focus of research around the world since the early 1980s, when it was verified to be increasing in frequency, intensity and amount of areas affected. The phenomenon has been recorded since 1993, associated with elevation of the sea surface temperature due to El Niños and water thermal anomalies, according to most reports around the world. On the coast of Rio Grande do Norte, Brazil, a mass coral bleaching event was recorded in the Environmental Protection Area of Coral Reefs (APARC) during March and April 2010, when the water temperature reached 34°C for several days. About 80% of the corals in Maracajaú reef-complex exhibited partial or total bleaching. The aims of this study were to verify representativeness of coral coverage and how the bleaching dynamic has developed among different species. Coral coverage was estimated according to Reef Check Brazil protocol associated with quadrant method, and bleaching was evaluated from biweekly visual surveys in 80 colonies of Favia gravida, Porites astreoides, Siderastrea stellata and Millepora alcicornis. At the same time temperature, pH, salinity and horizontal transparency, as well as mortality and disease occurrence were monitored. Analysis of variance and Multiple Regression from the perspective of time lag concept were used to evaluate the bleaching dynamics among species and the relationship between variation of means of bleaching and variations of abiotic parameters, respectively. Species showed significant differences among themselves as to variation of means of bleaching over time, but the dynamic of variation exhibited similar patterns