The effects of elevated seawater temperatures on Caribbean gorgonian corals and their algal symbionts, <i>Symbiodinium</i> spp.

<div><p>Global climate change not only leads to elevated seawater temperatures but also to episodic anomalously high or low temperatures lasting for several hours to days. Scleractinian corals are detrimentally affected by thermal fluctuations, which often lead to an uncoupling of their mutualism with <i>Symbiodinium</i> spp. (coral bleaching) and potentially coral death. Consequently, on many Caribbean reefs scleractinian coral cover has plummeted. Conversely, gorgonian corals persist, with their abundance even increasing. How gorgonians react to thermal anomalies has been investigated utilizing limited parameters of either the gorgonian, <i>Symbiodinium</i> or the combined symbiosis (holobiont). We employed a holistic approach to examine the effect of an experimental five-day elevated temperature episode on parameters of the host, symbiont, and the holobiont in <i>Eunicea tourneforti</i>, <i>E</i>. <i>flexuosa</i> and <i>Pseudoplexaura porosa</i>. These gorgonian corals reacted and coped with 32°C seawater temperatures. Neither <i>Symbiodinium</i> genotypes nor densities differed between the ambient 29.5°C and 32°C. Chlorophyll <i>a</i> and <i>c</i>_<i>2</i> per <i>Symbiodinium</i> cell, however, were lower at 32°C leading to a reduction in chlorophyll content in the branches and an associated reduction in estimated absorbance and increase in the chlorophyll <i>a</i> specific absorption coefficient. The adjustments in the photochemical parameters led to changes in photochemical efficiencies, although these too showed that the gorgonians were coping. For example, the maximum excitation pressure, <i>Q</i>_m, was significantly lower at 32°C than at 29.5°C. In addition, although per dry weight the amount of protein and lipids were lower at 32°C, the overall energy content in the tissues did not differ between the temperatures. Antioxidant activity either remained the same or increased following exposure to 32°C further reiterating a response that dealt with the stressor. Taken together, the capability of Caribbean gorgonian corals to modify symbiont, host and consequently holobiont parameters may partially explain their persistence on reefs faced with climate change.</p></div

<i>Symbiodinium</i> Photosynthesis in Caribbean Octocorals

<div><p>Symbioses with the dinoflagellate Symbiodinium form the foundation of tropical coral reef communities. Symbiodinium photosynthesis fuels the growth of an array of marine invertebrates, including cnidarians such as scleractinian corals and octocorals (e.g., gorgonian and soft corals). Studies examining the symbioses between Caribbean gorgonian corals and Symbiodinium are sparse, even though gorgonian corals blanket the landscape of Caribbean coral reefs. The objective of this study was to compare photosynthetic characteristics of Symbiodinium in four common Caribbean gorgonian species: Pterogorgia anceps, Eunicea tourneforti, Pseudoplexaura porosa, and Pseudoplexaura wagenaari. <i>Symbiodinium</i> associated with these four species exhibited differences in Symbiodinium density, chlorophyll a per cell, light absorption by chlorophyll a, and rates of photosynthetic oxygen production. The two Pseudoplexaura species had higher Symbiodinium densities and chlorophyll a per Symbiodinium cell but lower chlorophyll a specific absorption compared to P. anceps and E. tourneforti. Consequently, P. porosa and P. wagenaari had the highest average photosynthetic rates per cm² but the lowest average photosynthetic rates per Symbiodinium cell or chlorophyll a. With the exception of Symbiodinium from E. tourneforti, isolated Symbiodinium did not photosynthesize at the same rate as Symbiodinium in hospite. Differences in <i>Symbiodinium</i> photosynthetic performance could not be attributed to <i>Symbiodinium</i> type. All <i>P. anceps</i> (n = 9) and <i>P. wagenaari</i> (n = 6) colonies, in addition to one <i>E. tourneforti</i> and three <i>P. porosa</i> colonies, associated with <i>Symbiodinium</i> type B1. The B1 <i>Symbiodinium</i> from these four gorgonian species did not cluster with lineages of B1 <i>Symbiodinium</i> from scleractinian corals. The remaining eight <i>E. tourneforti</i> colonies harbored <i>Symbiodinium</i> type B1L, while six <i>P. porosa</i> colonies harbored type B1i. Understanding the symbioses between gorgonian corals and <i>Symbiodinium</i> will aid in deciphering why gorgonian corals dominate many Caribbean reefs.</p></div

Summary of the results of a linear mixed effects model analyses testing the effect of elevated temperature on <i>Symbiodinium</i> parameters in the Caribbean gorgonian corals <i>Eunicea tourneforti</i> (<i>ET)</i>, <i>E</i>. <i>flexuosa</i> (<i>EF</i>) and <i>Pseudoplexaura porosa</i> (<i>PP</i>).

<p>Summary of the results of a linear mixed effects model analyses testing the effect of elevated temperature on <i>Symbiodinium</i> parameters in the Caribbean gorgonian corals <i>Eunicea tourneforti</i> (<i>ET)</i>, <i>E</i>. <i>flexuosa</i> (<i>EF</i>) and <i>Pseudoplexaura porosa</i> (<i>PP</i>).</p

A maximum likelihood phylogenetic tree based on microsatellite flanking regions of B1 <i>Symbiodinium</i>.

<p>The phylogeny includes B1 <i>Symbiodinium</i> from the four gorgonian species in this study (highlighted in gray), from other gorgonian corals <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0106419#pone.0106419-Thornhill1" target="_blank">[47]</a>, from scleractinian and hydrozoan corals <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0106419#pone.0106419-Finney1" target="_blank">[36]</a>, as well as <i>Symbiodinium minutum</i> from <i>Aiptasia</i>, a sea anemone <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0106419#pone.0106419-Thornhill1" target="_blank">[47]</a>. Branch tips are labeled with host species and sample sizes when n>1. Gorgonian and scleractinian coral species are shown in black and red, respectively, and the other cnidarians are shown in blue. B1 lineages described by Finney et al. <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0106419#pone.0106419-Finney1" target="_blank">[36]</a> are listed besides the host taxa. Numbers above the branches are the posterior probability above the maximum likelihood consensus support for each group. B1 <i>Symbiodinium</i> from 16 of 19 gorgonian colonies sampled clustered in a phylogenetic group with high posterior probability (top gray box). Three gorgonian colonies were placed outside of this clade (bottom gray box) and were most closely related to <i>Symbiodinium</i> isolated from <i>Pseudoplexaura porosa</i> from Florida (indicated with (+1)) and cultured <i>Symbiodinium</i> from <i>Gorgonia ventalina</i><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0106419#pone.0106419-Thornhill1" target="_blank">[47]</a> indicated with *. (#) indicates a group recovered in the maximum likelihood tree, but not the Bayesian phylogenetic tree.</p

Photosynthetic characteristics of <i>Symbiodinium</i> in four Caribbean gorgonian species.

<p>Sample sizes for each gorgonian species (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0106419#pone-0106419-g001" target="_blank">Figure 1</a> legend for full genus names) are given in parentheses next to the species name. Parameters include the abundant <i>Symbiodinium</i> (<i>Sym</i>) internal transcribed spacer region two (<i>Sym</i> ITS2) type, <i>Sym</i> cell density, chlorophyll content (chl), estimated absorbance at 675 nm (D_{e 675}), as well as the pressure over photosystem II (<i>Q_m</i>). Table cells contain the sample mean ± standard deviation. The mean square (MS), F statistics (F), and significance value (p) from a one-way ANOVA, using gorgonian species as a factor, are shown for each variable. All variables were transformed prior to conducting the ANOVA. Means with different superscript letters were statistically different (α = 0.05) and this was diagnosed by Tukey's HSD post hoc tests. Power (1- β) is shown for non-significant results.</p><p>Photosynthetic characteristics of <i>Symbiodinium</i> in four Caribbean gorgonian species.</p

<i>In hospite</i> net photosynthesis-irradiance (P-E) curves from four Caribbean gorgonian species.

<p>(A) P-E curves per cm² of gorgonian branches and, (B) P-E curves per <i>Symbiodinium</i> cell. Solid lines represent the average fitted values for <i>Pterogorgia anceps</i> (n = 9), <i>Eunicea tourneforti</i> (n = 8), <i>Pseudoplexaura porosa</i> (n = 6), and <i>Pseudoplexaura wagenaari</i> (n = 6). Dotted lines represent ± standard error. The photosynthetic rate at 1800 µmol quanta was used as a proxy for the maximum photosynthetic rate.</p

Photosynthesis-irradiance (P-E) curve parameters for isolated <i>Symbiodinium</i>.

<p>Sample sizes for <i>Symbiodinium</i> isolates from each gorgonian species (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0106419#pone-0106419-g001" target="_blank">Figure 1</a> legend for full genus names) are given in parentheses next to the species' name. P_max and R represent the maximum photosynthetic and respiration rates, respectively, in µmol O₂ hr⁻¹. α is the initial slope of the P-E curve. Table cells contain the sample mean ± standard deviation. The mean square (MS), F statistics (F), and significance value (p) from a one-way ANOVA using gorgonian species as a factor are shown for each variable. All variables were transformed prior to conducting the ANOVA. Means with different superscript letters are statistically different (α = 0.05).</p><p>Photosynthesis-irradiance (P-E) curve parameters for isolated <i>Symbiodinium</i>.</p

<i>Symbiodinium</i> parameters in four Caribbean gorgonian species.

<p>(A) Cell densities and, (B) Concentration of chlorophylls <i>a</i> (circles) and <i>c</i>₂ (squares) per <i>Symbiodinium</i> cell. Points represent sample means ± standard error. Gorgonian species that do not share a letter are significantly different from each other in either density or chlorophyll <i>a</i> per cell (α = 0.05, see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0106419#pone-0106419-g001" target="_blank">Figure 1</a> for full species names and sample sizes). See <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0106419#pone-0106419-t003" target="_blank">Table 3</a> for significant differences in chlorophyll <i>c</i>₂ per cell.</p

Estimated absorbance spectra, D_e (A), and Chlorophyll <i>a</i> specific absorption, <i>a</i>*_{chl <i>a</i>} (B) in four Caribbean gorgonian species.

<p><i>Pterogorgia anceps</i> (red line; n = 9), <i>Eunicea tourneforti</i> (green line; n = 8), <i>Pseudoplexaura porosa</i> (blue line; n = 6), and <i>Pseudoplexaura wagenaari</i> (purple line; n = 6). Lines in (A) represent average D_e spectra for each species. The equation for the line in (B) is y = 0.7586*(x^−0.8976).</p

Photosynthesis-irradiance (P-E) curve parameters for gorgonian species.

<p>Sample sizes for each gorgonian species are given in parentheses next to the species name (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0106419#pone-0106419-g001" target="_blank">Figure 1</a> legend for full genus names). P and R represent photosynthetic and respiration in µmol O₂ hr⁻¹ rates at 1800 µmol quanta m⁻² s⁻¹, respectively. α represents the initial slope of the P-E curve. Table cells contain the sample mean ± standard deviation. The mean square (MS), F statistics (F), and significance value (p) are from a one-way ANOVA using gorgonian species as a factor. All variables were transformed prior to conducting ANOVA. Means with different superscript letters are statistically different (α = 0.05). Power (1- β) is shown for non-significant results.</p><p>Photosynthesis-irradiance (P-E) curve parameters for gorgonian species.</p