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ISME J
2015 Dec 01;912:2620-9. doi: 10.1038/ismej.2015.71.
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Productivity links morphology, symbiont specificity and bleaching in the evolution of Caribbean octocoral symbioses.
Baker DM
,
Freeman CJ
,
Knowlton N
,
Thacker RW
,
Kim K
,
Fogel ML
.
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Many cnidarians host endosymbiotic dinoflagellates from the genus Symbiodinium. It is generally assumed that the symbiosis is mutualistic, where the host benefits from symbiont photosynthesis while providing protection and photosynthetic substrates. Diverse assemblages of symbiotic gorgonian octocorals can be found in hard bottom communities throughout the Caribbean. While current research has focused on the phylo- and population genetics of gorgonian symbiont types and their photo-physiology, relatively less work has focused on biogeochemical benefits conferred to the host and how these benefits vary across host species. Here we examine this symbiosis among 11 gorgonian species collected in Bocas del Toro, Panama. By coupling light and dark bottle incubations (P/R) with (13)C-bicarbonate tracers, we quantified the link between holobiont oxygen metabolism with carbon assimilation and translocation from symbiont to host. Our data show that P/R varied among species, and was correlated with colony morphology and polyp size. Sea fans and sea plumes were net autotrophs (P/R>1.5), while nine species of sea rods were net heterotrophs with most below compensation (P/R<1.0). (13)C assimilation corroborated the P/R results, and maximum δ(13)Chost values were strongly correlated with polyp size, indicating higher productivity by colonies with high polyp SA:V. A survey of gorgonian-Symbiodinium associations revealed that productive species maintain specialized, obligate symbioses and are more resistant to coral bleaching, whereas generalist and facultative associations are common among sea rods that have higher bleaching sensitivities. Overall, productivity and polyp size had strong phylogenetic signals with carbon fixation and polyp size showing evidence of trait covariance.
Figure 2. (a) Mean δ13C of 11 species of gorgonians and their Symbiodinium after a ~7.5 h incubation in dark bottles (filled shapes) or light bottles (open shapes). (b) The same data for host and symbiont fractions incubated in darkness and with enlarged scale to illustrate differences. Gray horizontal lines indicate the upper and lower 95% confidence intervals of the mean natural abundance δ13C values for all species (initial samples). Species abbreviations are listed in the Methods section and are presented in order of decreasing P/R. Error bars represent the 95% confidence interval of the mean.
Figure 3. Phylogeny of Octocorallia used in this study, derived from sequences reported by McFadden et al. (2006). The scale bar indicates number of substitutions per site, while numbers at nodes indicate percentage Bayesian posterior probabilities. To the right of the phylogeny, four columns of circles represent values of photosynthesis to respiration ratios (P/R), δ13Chost, δ13Csymbiont and calyx depth (used as a proxy for polyp size). The size and shading of each circle are proportional to the values reported in Supplementary Table S1. In addition, the known Symbiodinium associations are shown as well as the colony morphology (not to scale). ‘unsp.' Indicates a unique Symbiodinium genotype with no clade designation.
Figure 4. Enriched δ13Chost values as a function of calyx depth (used as a proxy for polyp size) for eight species of gorgonians (data from Thibaudeau, 1983). Solid line represents a significant relationship between the variables. For species abbreviations refer to the Methods section.
Figure 5. Observed Symbiodinium genotypes (based on ITS2) obtained from the GeoSymbio database, representing eight gorgonian species analyzed in this study. All n≧3. *Indicates P/R data for A. acerosa, using symbiont records for A. elisabethae and A. bipinnata as there are no records for A. acerosa. **Indicates P/R for P. anceps and symbiont records for all Pterogorgia as there was only one record for P. anceps. For species abbreviations refer to the methods section.
Figure 6. Observed prevalence of bleaching of eight gorgonian species during the 2005 mass bleaching in Puerto Rico (data from Prada et al. (2010)) as a function of gorgonian P/R. The dashed line represents a logistic function fit to all data, whereas the solid line represents a logistic function fit to all data excluding P. anceps. For species abbreviations refer to the Methods section.
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