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.     

Diversity and spatial pattern of coral communities in the Red Sea upper twilight zone

Summary This is the first study based on numerical analysis of the abundance of 11 scleractinian corals of depths at between 100–210 m in the Red Sea twilight zone. Two distinct coral communities were found: a Leptoseris fragilis community at a depth of 100–130 m (zone 1) and a Dendrophillia horsti community below 130 m (zone 2, 3). Population densities and coral coverage are very low; distribution of individuals is highly clumped. Highest observed densities on 100 m² were 2720 individuals for L. fraglis, 2720 for D. horsti and 2260 for Javania insignis. Calculated coverage rates were maximally 3.6% (L. fragilis), 0.08% (D. horsti) and 0.11% (J. insignis). L. fragilis, the only symbiont bearing coral, was very abundant. It has an unusual depth range for a photosynthesising coral. Coral density is only weakly correlated with hard bottom coverage. Species diversity with an average of 8 species is highest at 120–170 m and decreases in shallower and deeper water. The study depth range is a transient zone for coral distribution. It contains the upper distribution limits of a few deep sea corals and the lower ones of several shallower water species. Ahermatypic corals, collected at 160–170 m depth, were transplanted from their original depth to 159, 118, 70 and 40 m; after one year most species survived transplantation far beyond their upper distributional limits. The symbiotic L. fragilis, collected at 120 m, survived transplantation to deep water (159 m) as well as shallow zones (90, 70 and 40 m). The study demonstrates the feasibility of line-transect methods for coral community studies with a submersible.     

Harmful algae on tropical coral reefs: Bottom-up eutrophication and top-down herbivory

A conceptual paradigm, the “Relative Dominance Model”, provides the perspective to assess the interactive external forcing-mechanisms controlling phase shifts among the dominant benthic functional groups on tropical coral reefs [i.e., microalgal turfs and frondose macroalgae (often harmful) versus reef-building corals and calcareous coralline algae (mostly beneficial due to accretion of calcareous reef framework)]. Manipulative experiments, analyses of existing communities and bioassays tested hypotheses that the relative dominances of these functional groups are mediated by two principal controlling factors: nutrients (i.e., bottom-up control) and herbivory (i.e., top-down control). The results show that reduced nutrients alone do not preclude fleshy algal growth when herbivory is low, and high herbivory alone does not prevent fleshy algal growth when nutrients are elevated. However, reduced nutrients in combination with high herbivory virtually eliminate all forms of fleshy micro- and macro-algae. The findings reveal considerable complexity in that increases in bottom-up nutrient controls and their interactions stimulate harmful fleshy algal blooms (that can alter the abundance patterns among functional groups, even under intense herbivory); conversely, elevated nutrients inhibit the growth of ecologically beneficial reef-building corals. The results show even further complexity in that nutrients also act directly as either limiting factors (e.g., physiological stresses) or as stimulatory mechanisms (e.g., growth enhancing factors), as well as functioning indirectly by influencing competitive outcomes. Herbivory directly reduces fleshy-algal biomass, which indirectly (via competitive release) favors the expansion of grazer-resistant reef-building corals and coralline algae. Because of the sensitive nature of direct/indirect and stimulating/limiting interacting factors, coral reefs are particularly vulnerable to anthropogenic reversal effects that decrease top-down controls and, concomitantly, increase bottom-up controls, dramatically altering ecosystem resiliencies.     

Monitoring coral bleaching using a colour reference card

Assessment of the extent of coral bleaching has become an important part of studies that aim to understand the condition of coral reefs. In this study a reference card that uses differences in coral colour was developed as an inexpensive, rapid and non-invasive method for the assessment of bleaching. The card uses a 6 point brightness/saturation scale within four colour hues to record changes in bleaching state. Changes on the scale of 2 units or more reflect a change in symbiont density and chlorophyll a content, and therefore the bleaching state of the coral. When used by non-specialist observers in the field (here on an intertidal reef flat), there was an inter-observer error of ± 1 colour score. This technique improves on existing subjective assessment of bleaching state by visual observation and offers the potential for rapid, wide-area assessment of changing coral condition.     

Net release of dissolved organic matter by the scleractinian coral Acropora pulchra

The net production of dissolved organic matter (DOM) and dissolved combined and free amino acids (DCAA and DFAA, respectively) by the hermatypic coral Acropora pulchra was measured in the submerged condition, and the production rates were normalized to the coral surface area, tissue biomass, and net photosynthetic rates by zooxanthellae. When normalized to the unit surface area, the production rates of dissolved organic carbon and nitrogen (DOC and DON, respectively) were 37 and 4.4 nmol cm^− 2 h^− 1, respectively. Comparing with the photosynthetic rate by zooxanthellae, which was measured by ¹³C-tracer accumulation in the soft tissue of the coral colony, the release rate of DOC corresponded to 5.4% of the daily net photosynthetic production. The tissue biomass of the coral colony was 178 µmol C cm^− 2 and 23 µmol N cm^− 2, indicating that the release of DOC and DON accounted for 0.021% h^− 1 and 0.019% h^− 1 of the tissue C and N, respectively. The C:N ratios of the released DOM (average 8.4) were not significantly different from those of the soft tissue of the coral colonies (average 7.7). While DFAA did almost not accumulate in the incubated seawater, DCAA was considerably released by the coral colonies at the rate of 2.1 nmol cm^− 2 h^− 1 on average. Calculating C and N contents of the hydrolyzable DCAA, it was revealed that about 20% and 50%–60% of the released bulk DOC and DON, respectively, were composed of DCAA.     

Nutrient manipulation methods for coral reef studies: A critical review and experimental field data

The results reported in this paper demonstrate suboptimal experimental designs in some of the previously published manipulative methods and provide insights for the improvement of in-situ nutrient studies on coral reefs. Overgrown 0.5-liter porous clay-pot diffusers (“mini-reefs”—following a decade of recruitment, colonization and competition) were utilized to evaluate protocols for studies of controlled nutrient enrichment on coral reefs. A commonly used fertilizer, Tree Food Stakes resulted in detrimental 11-fold and 20-fold decreases of fleshy algae and calcareous coralline algae, respectively, relative to the Control treatments; while blue-green algae (Cyanobacteria) became significantly (6 times) more abundant. Osmocote-filled mini-reefs showed no such negative differences in mortality from the Controls for any functional group. By avoiding the pitfalls of inappropriate sources of enrichment, insufficient durations of colonization/competition studies, suboptimal study areas and inadequate nutrient detection limits in future research, the potential to provide new insights into the nutrient status of coral reefs is greatly increased.     

Ontogenetic change in the abundance of mycosporine-like amino acids in non-zooxanthellate coral larvae

Although mycosporine-like amino acids (MAAs) have been extensively investigated in reef-building corals, the sources of these MAAs and the process of their interconversion remain a topic of interest. Here we examined ontogenetic change in the abundance of MAAs in planula larvae of the spawning scleractinian coral Goniastrea retiformis in the absence of zooxanthellae and other dietary input. In order to examine the potential contribution of prokaryotes in the synthesis of MAAs in animal tissue, one group of larvae were treated with the antibiotic rifampicin. High concentrations of MAAs (mycosporine-glycine, shinorine, palythinol, asterina-330), were present in the asymbiotic eggs and adults; however, no MAAs were present in the endosymbiotic zooxanthellae. We documented a steady decline in the total MAA concentrations through time in larvae treated with rifampicin; however, in the absence of antibiotic there was a significant increase in the concentration of MAAs, driven by a sharp increase in the abundance of shinorine and palythinol between day 3 and 7. Our results suggest that MAA synthesis and conversion in G. retiformis larvae occurred in the absence of symbiotic zooxanthellae, and indicate a possible contribution of prokaryotes associated with the animal tissue to these processes.     

Comparison of stress susceptibility of in hospite and isolated zooxanthellae among five coral species

Coral species in a similar habitat often show different bleaching susceptibilities. It is not understood which partner of coral-zooxanthellae complexes is responsible for differential stress susceptibility. Stress susceptibilities of in hospite and isolated zooxanthellae from five species of corals collected from shallow water in Okinawa were compared. To estimate stress susceptibility, we measured the maximum quantum yields (F_v/F_m) of in hospite and isolated zooxanthellae after 3-h exposure to either 28 or 34 °C at various light intensities and their recovery after 12 h under dim light at 26 °C. Significant reduction in photochemical efficiency (F_v/F_m) of photosystem II (PSII) was observed in in hospite zooxanthellae exposed to high light intensity (1000 μmol quanta m⁻² s⁻¹), while PSII activity of isolated zooxanthellae decreased significantly even at a lower light intensity (70 μmol quanta m⁻² s⁻¹). The recovery of the PSII activity after 12 h was incomplete in both in hospite and isolated zooxanthellae, indicating the presence of chronic photoinhibition. The stress susceptibility of isolated zooxanthellae was more variable among species than in hospite zooxanthellae. The order of stress susceptibility among the five coral species was different between in hospite and isolated zooxanthellae. The present results suggest that the host plays a significant role in determining bleaching susceptibility of corals, though zooxanthellae from different host have different stress susceptibilities.     

Early cellular changes are indicators of pre-bleaching thermal stress in the coral host

Thermal stress causes the coral-dinoflagellate symbiosis to disassociate and the coral tissues to whiten. The onset and occurrence of this coral bleaching is primarily defined via the dinoflagellate responses. Here we demonstrate that thermal stress responses occur in the coral host tissues in the days before the onset of coral bleaching. The observed sequence of thermal responses includes reductions in thickness of coral tissue layers and apoptosis of the cells prior to reductions in symbiont density. In the days before the onset of coral bleaching the outer coral tissue layer (epithelium) thickness reduces and apoptosis occurs within the gastrodermis. Two days following this, coinciding with an initial reduction of symbiont density (by approximately 25%), gastrodermal thickness decreased and apoptosis of host cells was identified in the epithelium. This was eventually followed by large reduction in symbiont density (by approximately 50%) consistent with coral bleaching. Both pro-apoptotic and anti-apoptotic genes are identified in the reef building coral Acropora aspera, demonstrating the necessary pathways are present for fine control of host apoptosis. Our study shows that defining periods of host stress based on the responses defined by dinoflagellate symbiont underestimates the importance of early cellular events and the cellular complexity of coral host.     

How does an animal behave like a plant? Physiological and molecular adaptations of zooxanthellae and their hosts to symbiosis

Cnidarians (corals and sea anemones) harbouring photosynthetic microalgae derive several benefits from their association. To allow this association, numerous symbiotic-dependent adaptations in both partners, resulting from evolutionary pressures, have been selected. The dinoflagellate symbionts (zooxanthellae) are located inside a vesicle in the cnidarian host cell and are therefore exposed to a very different environment compared to the free-living state of these microalgae in terms of ion concentration and carbon content and speciation. In addition, this intracellular localization imposes that they rely completely upon the host for their nutrient supply (nitrogen, CO₂). Symbiotic-dependent adaptations imposed to the animal host by phototrophic symbiosis are more relevant to photosynthetic organisms than to metazoans: indeed, the cnidarian host often harbours diurnal changes of morphology to adapt itself to the amount of light and possesses carbon-concentrating mechanisms, antioxidative defences and UV sunscreens similar to that present in phototrophs. These adaptations and the contrasting fragility of the association are discussed from both ecological and evolutionary points of view.     

Cellular processes of bleaching in the Mediterranean coral Oculina patagonica

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

Satellite observation of Keppel Islands (Great Barrier Reef) 2002 coral bleaching using IKONOS data

An examination of IKONOS satellite imagery of the Keppel Islands (Great Barrier Reef) acquired before and during a coral bleaching event indicates that severe bleaching of reefs can be detected as an increase in brightness in the band 1 (blue) and band 2 (green) IKONOS spectral bands (4-m resolution). The bleaching was not detected in band 3 (red), band 4 (near-infrared), or in the 1-m panchromatic band data. A total of 0.74 km² of bleached coral was identified, with detection occurring in waters as deep as 15 m. The procedure requires that one of the scenes be radiometrically normalized to match the reference scene prior to image differencing. A relative radiometric normalization was used in this case because variable cloud cover present in the image acquired during the bleaching event prevented reliable modeling of atmospheric effects. The success at coral bleaching detection at Keppel Islands represents both a best-case and a cloud-challenged scenario. It was a best-case scenario in that coral cover was extensive (70–90% live coral cover, mostly acroporids) and the bleaching level was extreme (92–95% of coral cover white bleached). It was a cloud-challenged scenario in terms of having extensive and highly variable cloud cover present in the image acquired during the bleaching event. Color difference images reveal extensive areas of bleached coral at sites away from our study area, indicating that this platform and methodology may be a valuable tool for mapping high coral cover areas during bleaching events. Additional studies and technique refinements would be required to test the detection limits of bleaching with IKONOS imagery or to develop a spectrally based bleaching detection index.An erratum to this article can be found at     

Phase shifts and the role of herbivory in the resilience of coral reefs

Cousin Island marine reserve (Seychelles) has been an effectively protected no-take marine protected area (MPA) since 1968 and was shown in 1994 to support a healthy herbivorous fish assemblage. In 1998 Cousin Island reefs suffered extensive coral mortality following a coral bleaching event, and a phase shift from coral to algal dominance ensued. By 2005 mean coral cover was <1%, structural complexity had fallen and there had been a substantial increase in macroalgal cover, up to 40% in some areas. No clear trends were apparent in the overall numerical abundance and biomass of herbivorous fishes between 1994 and 2005, although smaller individuals became relatively scarce, most likely due to the loss of reef structure. Analysis of the feeding habits of six abundant and representative herbivorous fish species around Cousin Island in 2006 demonstrated that epilithic algae were the preferred food resource of all species and that macroalgae were avoided. Given the current dominance of macroalgae and the apparent absence of macroalgal consumers, it is suggested that the increasing abundance of macroalgae is reducing the probability of the system reverting to a coral dominated state.     

Patterns of resistance and resilience of the stress-tolerant coral Siderastrea radians (Pallas) to sub-optimal salinity and sediment burial

The coastal lagoons of south Florida, U.S., experience fluctuating levels of sedimentation and salinity and contain only a subset of the coral species found at the adjacent reefs of the Florida Reef Tract. The dominant species within these habitats is Siderastrea radians, which can reach densities of up to 68 colonies m^- 2 and is commonly exposed to salinity extremes (< 10 psu to > 37 psu) and chronic sediment burial. In this study, we document the patterns of resistance and resilience of S. radians to sub-optimal salinity levels and sediment burial in a series of short-term, long-term, acute, chronic, single-stressor, and sequential-stressor experiments.S. radians displayed remarkable patterns of resistance and resilience and mortality was documented only under prolonged (≥ 48 h) continuous exposure to salinity extremes (15 and 45 psu) and chronic sediment burial. A reduction in photosynthetic rates was documented for all salinity exposures and the decrease in photosynthesis was linearly related to exposure time. Negative impacts on photosynthetic rates were more severe under low salinity (15 psu) than under high salinity (45 psu). Corals exposed to intermediate, low-salinity levels (25 psu), exhibited initial declines in photosynthesis that were followed by temporary increases that may represent transient acclimatization patterns. The impacts of sediment burial were influenced by the duration of the burial period and ranged from a temporary reduction in photosynthesis to significant reductions in growth and tissue mortality. The maintenance of P/R ratios > 1 and the rapid (< 24 h) recovery of photosynthetic rates after burial periods of 2-24 h indicates that S. radians is able to resist short-term burial periods with minor physiological consequences. However, as burial periods increase and colonies become covered at multiple chronic intervals, sediment burial resulted in extended photosynthetic recovery periods, reduced growth, and mortality. Under normal conditions (i.e., no salinity stress), S. radians was very effective at clearing sediments, and > 50% of the colonies' surface area was cleared within 1 h. However, clearing rates were influenced by physiological status, and prior exposure to sub-optimal salinity significantly reduced the clearing rates of stressed colonies.The response of S. radians to disturbance documented in this study characterizes this species as highly stress-tolerant and provides an explanation for its present high abundance in both reef and marginal environments. Moreover, the key life-history attributes of S. radians, such as brooding reproductive strategy, small colony size, high stress-tolerance, and high recruitment rates, suggest the potential for this species to replace reef-building taxa under increased disturbance scenarios in Florida and elsewhere in the region.     

Recent coral facies of the Indian Ocean Coast of Somalia with an interim check list of corals

Summary From a study of two areas, Jesira and the Bajuni Archipelago, about 400 km apart, a general pattern can be established for the Recent facies, together with the morphological and taxonomic features of the corals. Present day coral development is characterized by true fringing reefs in the Bajuni Archipelago and by scattered patches and knolls in the Jesira area. The coral fauna, consisting of 27 genera and 63 species so far (including all uncertainties, but not sight records), is rather poor, though coral communities are locally well developed. These figures probably reflect incomplete study and sampling. Although comparison with other areas may therefore be premature, a preliminary biogeographical analysis suggests that this fauna is more closely related to that of the Red Sea than to East Africa and the Seychelles. This differs from other published biogeographical work on Indian Ocean coral faunas, but further study of the corals in this and neighbouring areas of the Indian Ocean is needed in order to resolve this apparent anomaly.     

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

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

Genetic structure of a reef-building coral from thermally distinct environments on the Great Barrier Reef

Adaptation to localised thermal regimes is facilitated by restricted gene flow, ultimately leading to genetic divergence among populations and differences in their physiological tolerances. Allozyme analysis of six polymorphic loci was used to assess genetic differentiation between nine populations of the reef-building coral Acropora millepora over a latitudinal temperature gradient on the inshore regions of the Great Barrier Reef (GBR). Small but significant genetic differentiation indicative of moderate levels of gene flow (pairwise F _ST 0.023 to 0.077) was found between southern populations of A. millepora in cooler regions of the GBR and the warmer, central or northern GBR populations. Patterns of genetic differentiation at these putatively neutral allozyme loci broadly matched experimental variation in thermal tolerance and were consistent with local thermal regimes (warmest monthly-averages) for the A. millepora populations examined. It is therefore hypothesized that natural selection has influenced the thermal tolerance of the A. millepora populations examined and greater genetic divergence is likely to be revealed by examination of genetic markers under the direct effects of natural selection.     

A microsampling method for genotyping coral symbionts

Genotypic characterization of Symbiodinium symbionts in hard corals has routinely involved coring, or the removal of branches or a piece of the coral colony. These methods can potentially underestimate the complexity of the Symbiodinium community structure and may produce lesions. This study demonstrates that microscale sampling of individual coral polyps provided sufficient DNA for identifying zooxanthellae clades by RFLP analyses, and subclades through the use of PCR amplification of the ITS-2 region of rDNA and denaturing-gradient gel electrophoresis. Using this technique it was possible to detect distinct ITS-2 types of Symbiodinium from two or three adjacent coral polyps. These methods can be used to intensely sample coral-symbiont population/communities while causing minimal damage. The effectiveness and fine scale capabilities of these methods were demonstrated by sampling and identifying phylotypes of Symbiodinium clades A, B, and C that co-reside within a single Montastraea faveolata colony.     

Molecular diversity of symbiotic algae (zooxanthellae) in scleractinian corals of Kenya

In this first sequence analysis of ‘zooxanthellae’ (symbiotic algae of the genus Symbiodinium) in scleractinian corals in Africa, seven Kenyan species sampled in 2001–2002 were analysed by RFLP and sequencing of a PCR-amplified fragment of the LSU rRNA gene. Zooxanthellae of phylotypes A, C and D, all described previously in corals from other regions of the world, were detected. All sequences of phylotype D were identical, while phylotype C was variable, with 14 distinct sequences, seven of which clustered in a previously unreported subgroup of phylotype C, among the 22 samples. These data on the diversity of zooxanthellae in Kenyan corals 3–4 years after the 1998 bleaching event are of potential value for longitudinal studies of temporal changes in zooxanthella diversity in Kenyan corals, especially in relation to future large-scale bleaching episodes.