Turbinaria Reniformis Research Articles

Effects of Light, Food Availability and Temperature Stress on the Function of Photosystem II and Photosystem I of Coral Symbionts

BackgroundReef corals are heterotrophic coelenterates that achieve high productivity through their photosynthetic dinoflagellate symbionts. Excessive seawater temperature destabilises this symbiosis and causes corals to “bleach,” lowering their photosynthetic capacity. Bleaching poses a serious threat to the persistence of coral reefs on a global scale. Despite expanding research on the causes of bleaching, the mechanisms remain a subject of debate.Methodology/Principal FindingsThis study determined how light and food availability modulate the effects of temperature stress on photosynthesis in two reef coral species. We quantified the activities of Photosystem II, Photosystem I and whole chain electron transport under combinations of normal and stressful growth temperatures, moderate and high light levels and the presence or absence of feeding of the coral hosts. Our results show that PS1 function is comparatively robust against temperature stress in both species, whereas PS2 and whole chain electron transport are susceptible to temperature stress. In the symbiotic dinoflagellates of Stylophora pistillata the contents of chlorophyll and major photosynthetic complexes were primarily affected by food availability. In Turbinaria reniformis growth temperature was the dominant influence on the contents of the photosynthetic complexes. In both species feeding the host significantly protected photosynthetic function from high temperature stress.Conclusions/SignificanceOur findings support the photoinhibition model of coral bleaching and demonstrate that PS1 is not a major site for thermal damage during bleaching events. Feeding mitigates bleaching in two scleractinian corals, so that reef responses to temperature stresses will likely be influenced by the coinciding availabilities of prey for the host.

Hsp60 protein pattern in coral is altered by environmental changes in light and temperature

The heat shock protein Hsp60 exhibited marked oscillation during a 12-hour day period when the coral Turbinaria reniformis was maintained in the laboratory under constant conditions of light (200 μE) and temperature (27 °C). A biphasic pattern of Hsp60 was apparent, punctuated by a low protein level at the midpoint of the 12-hour day period. Oscillation of Hsp60 was also apparent when coral was kept in darkness in lieu of a scheduled light period. The pattern of Hsp60 was altered when coral was exposed to increased light intensity (400 μE) or temperature elevation (32 °C). These observations suggest that Hsp60 in coral exhibits oscillation that is altered by increased light and temperature elevation.

Experimental comparison of skeletal growth rates in the cold-water coral Madrepora oculata Linnaeus, 1758 and three tropical scleractinian corals

The skeletal growth rate of the cold-water coral (CWC) Madrepora oculata Linnaeus, 1758 was measured during 3 months under controlled conditions (at 12 °C in the dark, fed five times a week), using the buoyant weight technique. In order to interpret CWC growth in a wider context, we also measured the skeletal growth rates of three tropical scleractinian species: Stylophora pistillata (Esper, 1797), Turbinaria reniformis (Bernard, 1896) and Galaxea fascicularis (Linnaeus, 1767), likewise maintained under controlled conditions (at 25 °C, 250 μmol photons m − 2 s − 1 , either fed five times a week or unfed). The skeletal growth rate of M. oculata was equal to 0.20 ± 0.09% d − 1 (mean ± SD), similar to the growth of unfed and fed nubbins of G. fascicularis (0.14 ± 0.01% d − 1 and 0.36 ± 0.11% d − 1 respectively) despite the large differences in seawater temperatures. Skeletal growth rates of S. pistillata (1.20 ± 0.49% d − 1 to 2.68 ± 0.65% d − 1 unfed/fed) and T. reniformis (0.78 ± 0.34% d − 1 to 0.94 ± 0.14% d − 1 unfed/fed) were significantly higher. These results confirm that the CWC M. oculata can grow at rates that are comparable to those of some tropical corals, despite the lack of autotrophy (lacking zooxanthellae) and the low temperatures of its environment.

Variation in photosynthesis and respiration in ­geographically distinct populations of two reef‑building coral species

Studies of the regulation and importance of physiological processes such as coral photo- synthesis and respiration on coral reefs require knowledge of spatio-temporal patterns of variability at different scales. Oxygen microelectrodes were used to measure photosynthesis and dark respira- tion of 2 corals, Pocillopora damicornis and Turbinaria reniformis, in the northern (Lizard Island) and central (Davies and Broadhurst Reefs) regions of the Great Barrier Reef (GBR) in winter and summer. Genetic characterisation of Symbiodinium revealed that P. damicornis hosted a single symbiont type (Symbiodinium C1) in both regions, whereas T. reniformis harboured 2 types, dependent on location. Colonies at Lizard Island harboured Symbiodinium D, whereas colonies at Davies Reef harboured Symbiodinium C2. Rates of gross photosynthesis were greater in the central than in the northern GBR in summer. A similar pattern was detected for dark respiration rates in T. reniformis. No seasonal change in either photosynthesis or dark respiration was evident in the northern GBR, possibly due to less annual variability in light conditions, and for T. reniformis, additionally the presence of Symbio- dinium D. These results highlight that environmental conditions coupled with regional-scale distrib- ution of Symbiodinium are likely to exert important influences on respiration and photosynthetic per- formance of reef-building corals.

Impact of feeding and short-term temperature stress on the content and isotopic signature of fatty acids, sterols, and alcohols in the scleractinian coral Turbinaria reniformis

This study assesses the combined effect of feeding and short-term thermal stress on various physiological parameters and on the fatty acid, sterol, and alcohol composition of the scleractinian coral Turbinaria reniformis. The compound-specific carbon isotope composition of the lipids was also measured. Under control conditions (26°C), feeding with Artemia salina significantly increased the symbiont density and chlorophyll content and the growth rates of the corals. It also doubled the concentrations of almost all fatty acid (FA) compounds and increased the n-alcohol and sterol contents. δ13C results showed that the feeding enhancement of FA concentrations occurred either via a direct pathway, for one of the major polyunsaturated fatty acid (PUFA) compounds of the food (18:3n-3 FA), or via an enhancement of photosynthate transfer (indirect pathway), for the other coral FAs. Cholesterol (C27Δ5) was also directly acquired from the food. Thermal stress (31°C) affected corals, but differently according to their feeding status. Chlorophyll, protein content, and maximal photosynthetic efficiency of photosystem II (PSII) decreased to a greater extent in starved corals. In such corals, FA concentrations were reduced by 33%, (especially C16, C18 FAs, and n-3 PUFA) and the sterol content by 27% (especially the C28∆5,22 and C28∆5). The enrichment in the δ13C signature of the storage and structural FAs suggests that they were the main compounds respired during the stress to maintain the coral metabolism. Thermal stress had less effect on the lipid concentrations of fed corals, as only FA levels were reduced by 13%, with no major changes in their isotope carbon signatures. In conclusion, feeding plays an essential role in sustaining T. reniformis metabolism during the thermal stress.

Heterotrophy in the Mediterranean symbiotic coral Cladocora caespitosa: comparison with two other scleractinian species

This experimental study assessed the grazing rates of the Mediterranean symbiotic coral Cladocora caespitosa on the 4 main food sources available in its natural environment: detrital partic- ulate organic matter (DPOM) and pico-, nano-, and microzooplankton. These rates were compared to the rates of 2 other scleractinian symbiotic species, the Mediterranean coral Oculina patagonica and the tropical coral Turbinaria reniformis. Results showed that C. caespitosa was the species with the highest grazing rates of pico- and nanoplankton, which contributed to more than half of the carbon supplied by photosynthesis. The daily heterotrophic carbon (C) input from these prey (at in situ con- centrations) was 88.3 ± 22.9, 16.9 ± 8.2, and 17.6 ± 4.3 µg C cm -2 d -1 for C. caespitosa, O. patagonica, and T. reniformis, respectively, corresponding to a percent contribution of heterotrophically acquired C to daily animal respiration (CHAR) of 119.8, 28.7, and 15.9%, respectively. C. caespitosa was also able to derive a significant part of its carbon needs from the grazing of microzooplankton and DPOM. Indeed, considering the in situ concentrations, the daily heterotrophic C input from microzoo- plankton and DPOM would be 32.6 and 10.0 µg C cm -2 d -1 , giving a CHAR estimation of 44.2 and 13.6%, respectively. Heterotrophy therefore plays a major role in the energy budget of this temper- ate species.

Experimental assessment of the feeding effort of three scleractinian coral species during a thermal stress: Effect on the rates of photosynthesis

This study aimed at investigating changes in feeding rates of three scleractinian coral species (Stylophora pistillata, Turbinaria reniformis and Galaxea fascicularis) between control (26°C) and short-term stress conditions (31°C), and to assess the effect of feeding on the photosynthetic efficiency of the corals. Feeding rates varied according to the feeding effort of the corals, itself depending on the environmental conditions. Indeed, S. pistillata significantly decreased its feeding rates at 31°C, while rates of T. reniformis and G. fascicularis were increased between 26 and 31°C. Independently of the feeding rates, food supply helped in preventing damage to the photosynthetic apparatus of the zooxanthellae. Indeed, starved corals from the three species showed significant decrease in both the electron transport rates and in the photosynthetic rates, following a loss in the amount of chlorophyll and experiencing photoinhibition of the photosystem II. However, no bleaching was observed in heated fed corals, with no decrease in their photosynthetic efficiency or performance.

Carbon isotope composition of fatty acids and sterols in the scleractinian coral Turbinaria reniformis: Effect of light and feeding

The effect of auto‐ and heterotrophy on the carbon isotope composition (δ13C) of fatty acids (FA) and sterols was studied in the scleractinian coral Turbinaria reniformis. Colonies were maintained in aquaria for 6 weeks under two light levels (100 and 300 mmol photons m−2 s−1) and/or two trophic conditions (starved and fed twice a week with zooplankton). In high‐light conditions, lipid biomarkers, both in the zooxanthellae and animal tissue, presented significantly higher δ13C values compared to those exposed to low light, supporting the widespread theory of enhanced 13C fixation with increasing irradiance and photosynthesis. This result and the similar lipid δ13C‐values of the host and the symbionts are a strong indication that most lipids are synthesized by the zooxanthellae. Feeding had a smaller effect than light on the lipid δ13C‐signatures and a more pronounced effect at low‐light level. Despite the depleted δ13C values of the zooplankton lipids, slight enrichment in 13C was observed in some FA from the host and zooxanthellae, whereas the main host sterol was depleted in 13C. These differences between FA and sterols give evidence for different biosynthesis pathways: FA might have been synthesized from the assimilation of carbohydrates or amino acids contained in the food, whereas sterols might derive from modification of dietary lipids.

Effect of light and feeding on the fatty acid and sterol composition of zooxanthellae and host tissue isolated from the scleractinian coral Turbinaria reniformis

The fatty acid and sterol compositions of zooxanthellae and animal fractions of the scleractinian coral Turbinaria reniformis were investigated under different light and feeding conditions, to study the symbiont‐host exchanges. Nubbins were maintained during 6 weeks under two light levels (100 [mol photons m−2 s−1 and 300 [mol photons m−2 s−1) and two feeding levels (starved and fed with zooplankton) in a factorial experiment. There were greater proportions of some polyunsaturated fatty acids (PUFA; e.g., C18:4 n‐3, C20:5 n‐3, C22:6 n‐3) in the zooxanthellae than in the host, suggesting that these PUFA were synthesized by the algae and transferred to the animal. Conversely, C20:4 n‐6 exhibited a greater proportion in the host and might have been synthesized by the animal. Light affected the chlorophyll content, the rates of photosynthesis, and the lipid production of all coral samples. Corals maintained in high‐light conditions had lower relative phytol content but higher concentrations of fatty acids (FA) and sterols than the shaded corals. Feeding also affected coral metabolism, but differently according to the light level and despite the fact that the host did not directly incorporate the zooplankton lipids (PUFA and cholesterol). In low light, feeding resulted in an increase of growth rates and storage lipid concentrations, mainly saturated fatty acids (SAFA) and membrane constituents (PUFA and sterols). In high light, the lipid energy from the food was directed toward an increase in calcification, as well as in chlorophyll content and protein content. This study highlights the importance of feeding in sustaining coral metabolism, especially when light, or stress events, is limiting photosynthesis.

Larval metamorphic competence in four species of Phestilla (Gastropoda; Opisthobranchia)

Many marine invertebrates depend on their larvae for dispersal and to find the appropriate habitat for adult survival, yet their larval ecology remains poorly known. In this study we test the time required until metamorphic competence in the veliger larvae of four species of Phestilla nudibranch. Larvae of Phestilla melanobrachia are planktotrophic and had the highest percentage of metamorphosis in response to the prey coral Tubastraea aurea. Twelve days after hatching these veligers had approximately 30% metamorphosis in response to Tubastraea aurea polyps and to waterborne compounds released from T. aurea. Larvae of the facultative lecithotroph Phestilla sibogae had the highest rates of metamorphosis in response to Porites cylindrica after five days. However, P. sibogae also had approximately 50% metamorphosis in response to the non-prey coral Turbinaria reniformis. Phestilla minor had significantly more metamorphosis in response to Porites annae than to filtered seawater. Phestilla minor was the only species to have spontaneous metamorphosis in response to filtered seawater; 27% metamorphosis was observed after four days. The lecithotroph Phestilla sp. 2 had 80% metamorphosis in response to its host coral Goniopora fruticosa and to waterborne cues from G. fruticosa five days after hatching. This species also had approximately 40% metamorphosis in response to non-prey corals Porites cylindrica and Turbinaria reniformis. These different larval development times make Phestilla spp. an ideal group to study the ecological and evolutionary consequences of different life history strategies in marine invertebrates.

Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling

Reef corals form associations with an array of genetically and physiologically distinct endosymbionts from the genus Symbiodinium. Some corals harbor different clades of symbionts simultaneously, and over time the relative abundances of these clades may change through a process called symbiont shuffling. It is hypothesized that this process provides a mechanism for corals to respond to environmental threats such as global warming. However, only a minority of coral species have been found to harbor more than one symbiont clade simultaneously and the current view is that the potential for symbiont shuffling is limited. Using a newly developed real-time PCR assay, this paper demonstrates that previous studies have underestimated the presence of background symbionts because of the low sensitivity of the techniques used. The assay used here targets the multi-copy rDNA ITS1 region and is able to detect Symbiodinium clades C and D with >100-fold higher sensitivity compared to conventional techniques. Technical considerations relating to intragenomic variation, estimating copy number and non-symbiotic contamination are discussed. Eighty-two colonies from four common scleractinian species (Acropora millepora, Acropora tenuis, Stylophora pistillata and Turbinaria reniformis) and 11 locations on the Great Barrier Reef were tested for background Symbiodinium clades. Although these colonies had been previously identified as harboring only a single clade based on SSCP analyses, background clades were detected in 78% of the samples, indicating that the potential for symbiont shuffling may be much larger than currently thought.

Variation in bleaching sensitivity of two coral species across a latitudinal gradient on the Great Barrier Reef: the role of zooxanthellae

The ability of corals to cope with environmental change, such as increased temperature, relies on the physiological mechanisms of acclimatisation and long-term genetic adaptation. We experimentally examined the bleaching sensitivity exhibited by 2 species of coral, Pocillopora damicornis and Turbinaria reniformis, at 3 locations across a latitudinal gradient of almost 6 degrees on the Great Barrier Reef (GBR). Target bleaching temperature was reached by using a ramping rate of 0.2°C/h. We found that the bleaching sensitivity and recovery of both species differed between corals with clade D symbionts and those with clade C. However, in P. damicornis bleaching susceptibility corresponded more strongly with latitude than with zooxanthella type and hence, temperature history, suggesting that local adaptation has occurred. The observed bleaching sensitivity was shown by a decrease in photochemical efficiency (F v /F m ) in both species of coral. The rate of recovery in T. reniformis was highest in explants containing clade D symbionts. The occurrence of clade D in the northern section of the GBR may reflect a long-term response to high sea water temperatures, while the presence of clade D in low abundance in T. reniformis at Heralds Prong Reef and Percy Island may be a result of recent bleaching events.

Suppression of skeletal growth in scleractinian corals by decreasing ambient carbonate-ion concentration: a cross-family comparison

Biogenic calcification is influenced by the concentration of available carbonate ions. The recent confirmation of this for hermatypic corals has raised concern over the future of coral reefs because [CO(3)(2-)] is a decreasing function of increasing pCO(2) in the atmosphere. As one of the overriding features of coral reefs is their diversity, understanding the degree of variability between species in their ability to cope with a change in [CO(3)(2-)] is a priority. We cultured four phylogenetically and physiologically different species of hermatypic coral (Acropora verweyi, Galaxea fascicularis, Pavona cactus and Turbinaria reniformis) under 'normal' (280 micromol kg(-1)) and 'low' (140 micromol kg(-1)) carbonate-ion concentrations. The effect on skeletogenesis was investigated quantitatively (by calcification rate) and qualitatively (by microstructural appearance of growing crystalline fibres using scanning electron microscopy (SEM)). The 'low carbonate' treatment resulted in a significant suppression of calcification rate and a tendency for weaker crystallization at the distal tips of fibres. However, while the calcification rate was affected uniformly across species (13-18% reduction), the magnitude of the microstructural response was highly species specific: crystallization was most markedly affected in A. verweyi and least in T. reniformis. These results are discussed in relation to past records and future predictions of carbonate variability in the oceans.

A new coral disease from the southern Arabian Gulf

During an ecological survey of coral communities at Jebel Ali in Dubai, United Arab Emirates, a high incidence of coral diseases was observed. Although coral disease has been reported from the Gulf of Oman (Coles 1994), this is the first report from in the Arabian Gulf. The encountered diseases were the well described Black Band and White Band Diseases (Antonius, 1995) and a hitherto undescribed disease, which we refer to as Yellow Band Disease. It manifests itself as a broad yellow band moving across healthy coral tissue in a manner similar to the Black Band disease (Rutzler, Santavy and Antonius, 1983) insofar as where the yellow band actively moves onto healthy tissue, a band of decaying and sloughing off tissue is observed. However, the entire area denuded by the infection can retain the characteristic yellow colour. The Yellow Band Disease is not similar to the Aggressive Orange Band recently described by Littler and Littler (1994), which attacks coralline algae. Investigations into establishing the pathogen are underway. Preliminary measurements indicate that within-colony spreading rates (on Acropora clathrata) are faster in summer (x = 19.7 ± 4.9 mm per week, measured mid October), than in winter (x = 9.4 ± 3.9 mm per week, measured beginning February). Disease spread is significantly different between these seasons (Mann-Whitney U-Test, Z = 2.67, P < 0.001). Species found to be affected by Yellow Band Disease were: Acropora clathrata, A. pharaonis, A. tenuis, A. valida, A. florida, Porites lutea, P. lichen, P. nodifera, Turbinaria reniformis, Cyphastrea microphthalma. Acknowledgements. We acknowledge funding assistance by the Dubai Municipality and Charles Martin of Martin Mid East for the opportunity to work in Gulf waters, and for logistical support.