Niche specialization of reef-building corals in the mesophotic zone: metabolic trade-offs between divergent Symbiodinium types

The photobiology of two reef corals and the distribution of associated symbiont types were investigated over a depth gradient of 0–60 m at Scott Reef, Western Australia. Pachyseris speciosa hosted mainly the same Symbiodinium C type similar to C3 irrespective of sampling depth. By contrast, Seriatopora hystrix hosted predominantly Symbiodinium type D1a or D1a-like at shallow depths while those in deeper water were dominated by a Symbiodinium C type closely related to C1. The photosynthesis/respiration (P/R) ratio increased consistently with depth at the two sampling times (November 2008 and April 2009) for P. speciosa and in November 2008 only for S. hystrix, suggesting a reduction in metabolic energy expended for every unit of energy obtained from photosynthesis. However, in April 2009, shallow colonies of S. hystrix exhibited decreased P/R ratios down to depths of approximately 23 m, below which the ratio increased towards the maximum depth sampled. This pattern was mirrored by changes in tissue biomass determined as total protein content. The depth of change in the direction of the P/R ratio correlated with a shift from Symbiodinium D to C-dominated colonies. We conclude that while photobiological flexibility is vital for persistence in contrasting light regimes, a shift in Symbiodinium type may also confer a functional advantage albeit at a metabolic cost with increased depth

Symbiodinium Genotypic and Environmental Controls on Lipids in Reef Building Corals

BACKGROUND: Lipids in reef building corals can be divided into two classes; non-polar storage lipids, e.g. wax esters and triglycerides, and polar structural lipids, e.g. phospholipids and cholesterol. Differences among algal endosymbiont types are known to have important influences on processes including growth and the photobiology of scleractinian corals yet very little is known about the role of symbiont types on lipid energy reserves. METHODOLOGY/PRINCIPAL FINDINGS: The ratio of storage lipid and structural lipid fractions of Scott Reef corals were determined by thin layer chromatography. The lipid fraction ratio varied with depth and depended on symbiont type harboured by two corals (Seriatopora hystrix and Pachyseris speciosa). S. hystrix colonies associated with Symbiodinium C1 or C1/C# at deep depths (>23 m) had lower lipid fraction ratios (i.e. approximately equal parts of storage and structural lipids) than those with Symbiodinium D1 in shallow depths (<23 m), which had higher lipid fraction ratios (i.e. approximately double amounts of storage relative to structural lipid). Further, there was a non-linear relationship between the lipid fraction ratio and depth for S. hystrix with a modal peak at ∼23 m coinciding with the same depth as the shift from clade D to C types. In contrast, the proportional relationship between the lipid fraction ratio and depth for P. speciosa, which exhibited high specificity for Symbiodinium C3 like across the depth gradient, was indicative of greater amounts of storage lipids contained in the deep colonies. CONCLUSIONS/SIGNIFICANCE: This study has demonstrated that Symbiodinium exert significant controls over the quality of coral energy reserves over a large-scale depth gradient. We conclude that the competitive advantages and metabolic costs that arise from flexible associations with divergent symbiont types are offset by energetic trade-offs for the coral host

Environmental Factors Controlling the Distribution of Symbiodinium Harboured by the Coral Acropora millepora on the Great Barrier Reef

Background: The Symbiodinium community associated with scleractinian corals is widely considered to be shaped by seawater temperature, as the coral's upper temperature tolerance is largely contingent on the Symbiodinium types harboured. Few studies have challenged this paradigm as knowledge of other environmental drivers on the distribution of Symbiodinium is limited. Here, we examine the influence of a range of environmental variables on the distribution of Symbiodinium associated with Acropora millepora collected from 47 coral reefs spanning 1,400 km on the Great Barrier Reef (GBR), Australia

Mesoscale variation in the photophysiology of the reef building coral Pocillopora damicornis along an environmental gradient

Spatial variation in the photophysiology of symbiotic dinoflagellates (zooxanthellae) of the scleractinian coral Pocillopora damicornis was examined along an environmental gradient in the Whitsunday Islands (Great Barrier Reef) at two depths (3 m and 6 m). Chlorophyll a fluorescence of photosystem II (PSII) and PAR-absorptivity measurements were conducted using an Imaging-PAM (pulse-amplitude-modulation) fluorometer. Most photophysiological parameters correlated with changes in environmental conditions quantified by differences in water quality along the gradient. For example, maximum quantum yield (Fv/Fm) increased and PAR-absorptivity decreased as water quality improved along the gradient from nearshore reefs (low irradiance, elevated nutrients and sediments) to outer islands (high irradiance, low nutrients and sediments). For apparent photosynthetic rate (PSmax) and minimum saturating irradiance (Ek), the direction of change differed depending on sampling depth, suggesting that different mechanisms\ud of photo-acclimatisation operated between shallow and deep corals. Deep corals conformed to typical patterns of light/shade acclimatisation whereas shallow corals exhibited reduced PSmax and Ek with improving water quality coinciding with greater heat dissipation (NPQ241). Furthermore, deep corals on nearshore reefs exhibited elevated Q241 in comparison to outer islands possibly due to effects of sedimentation and/or pollutants rather than irradiance. These results highlight the importance of\ud mesoscale sampling to obtain useful estimates of the variability of photophysiological parameters, particularly if such measures are to be used as bioindicators of the condition of coral reefs

Zooxanthellae Harvested by Ciliates Associated with Brown Band Syndrome of Corals Remain Photosynthetically Competent

Brown band syndrome is a new coral affliction characterized by a local accumulation of yet-unidentified ciliates migrating as a band along the branches of coral colonies. In the current study, morphologically intact zooxanthellae (= Symbiodinium) were observed in great numbers inside the ciliates (>50 dinoflagellates per ciliate). Microscale oxygen measurements and variable chlorophyll a fluorescence analysis along with microscopic observations demonstrated that zooxanthellae within the ciliates are photosynthetically competent and do not become compromised during the progression of the brown band zone. Zooxanthellae showed similar trends in light acclimation in a comparison of rapid light curve and steady-state light curve measures of variable chlorophyll a fluorescence. Extended light exposure of steady-state light curves resulted in higher quantum yields of photosystem II. The brown band tissue exhibited higher photosynthetically active radiation absorptivity, indicating more efficient light absorption due to a higher density of zooxanthellae in the ciliate-dominated zone. This caused relatively higher gross photosynthesis rates in the zone with zooxanthella-containing ciliates compared to healthy coral tissue. The observation of photosynthetically active intracellular zooxanthellae in the ciliates suggests that the latter can benefit from photosynthates produced by ingested zooxanthellae and from photosynthetic oxygen production that alleviates diffusion limitation of oxic respiration in the densely populated brown band tissue. It remains to be shown whether the zooxanthellae form a stable symbiotic association with the ciliate or are engulfed incidentally during grazing on coral tissue and then maintained as active inside the ciliate for a period before being digested and replaced by new zooxanthellae

The effects of clove oil on coral: an experimental evaluation using Pocillopora damicornis (Linnaeus)

Clove oil solution (10% clove oil, 90% ethanol) is an anaesthetic that is widely used to catch demersal fish on coral reefs. This study assessed the effects of clove oil solution on colonies of Pocillopora damicornis, a cosmopolitan reef coral. In the laboratory, low concentrations (0.5 ppt) of clove oil solution had no effect on coral colour or photosynthetic efficiency, irrespective of exposure time (1–60 min). Corals treated with high concentrations (50 ppt) of clove oil solution died immediately, including those that were exposed briefly (1 min). Intermediate concentrations (5 ppt) of clove oil solution produced variable results: a 1 min exposure had no effect, a 10 min exposure caused bleaching and reduced photosynthetic efficiency, and a 60 min exposure caused total mortality. To validate these observations, clove oil solution was applied to corals in situ. Sixty-three days after application, corals treated with 10 ml of clove oil solution appeared to be unaffected. It was concluded that (1) limited amounts of clove oil solution are unlikely to harm this coral, and (2) clove oil solution may represent an 'eco-friendly' alternative to cyanide for use in the live reef-fish trade

Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress

The impacts of warming seas on the frequency and severity of bleaching events are well documented, but the potential for different Symbiodinium types to enhance the physiological tolerance of reef corals is not well understood. Here we compare the functionality and physiological properties of juvenile corals when experimentally infected with one of two homologous Symbiodinium types and exposed to combined heat and light stress. A suite of physiological indicators including chlorophyll a fluorescence, oxygen production and respiration, as well as pigment concentration consistently demonstrated lower metabolic costs and enhanced physiological tolerance of Acropora tenuis juveniles when hosting Symbiodinium type C1 compared with type D. In other studies, the same D-type has been shown to confer higher thermal tolerance than both C2 in adults and C1 in juveniles of the closely related species Acropora millepora. Our results challenge speculations that associations with type D are universally most robust to thermal stress. Although the heat tolerance of corals may be contingent on the Symbiodinium strain in hospite, our results highlight the complexity of interactions between symbiotic partners and a potential role for host factors in determining the physiological performance of reef corals

Species–specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress

The impacts of warming seas on the frequency and severity of bleaching events are well documented, but the potential for different Symbiodinium types to enhance the physiological tolerance of reef corals is not well understood. Here we compare the functionality and physiological properties of juvenile corals when experimentally infected with one of two homologous Symbiodinium types and exposed to combined heat and light stress. A suite of physiological indicators including chlorophyll a fluorescence, oxygen production and respiration, as well as pigment concentration consistently demonstrated lower metabolic costs and enhanced physiological tolerance of Acropora tenuis juveniles when hosting Symbiodinium type C1 compared with type D. In other studies, the same D-type has been shown to confer higher thermal tolerance than both C2 in adults and C1 in juveniles of the closely related species Acropora millepora. Our results challenge speculations that associations with type D are universally most robust to thermal stress. Although the heat tolerance of corals may be contingent on the Symbiodinium strain in hospite, our results highlight the complexity of interactions between symbiotic partners and a potential role for host factors in determining the physiological performance of reef corals

Temporal changes in gene expression of corals from two locations translocated to a common laboratory environment.

<p>Lines represent means of normalized log2 transformed expression values among replicate colonies (solid line = Davies Reef, dashed line = Orpheus Island). The grey-shaded areas represent 95% confidence intervals of means. Plots are organised by the significance of model factors (FDR adj. <i>P</i>_LRT<0.022). Model-derived significant differences over time-points are indicated with stars above means (and are population specific in A–C, FDR adj. <i>P</i>_MCMC<0.024 or 0.018). Significant differences between populations at specific time-points are indicated by stars below means in A–C (FDR adj. <i>P</i>_MCMC<0.022).</p