Spatially distinct and regionally endemic Symbiodinium assemblages in the threatened Caribbean reef-building coral Orbicella faveolata

Abstract

Recently, the Caribbean reef-building coral Orbicella faveolata was listed as “threatened” under the U.S. Endangered Species Act. Despite attention to this species’ conservation, the extent of geographic variation within O. faveolata warrants further investigation. O. faveolata is unusual in that it can simultaneously harbor multiple genetically distinct and co-dominant species of endosymbiotic dinoflagellates in the genus Symbiodinium. Here, we investigate the geographic and within-colony complexity of Symbiodinium-O. faveolata associations from Florida Keys, USA; Exuma Cays, Bahamas; Puerto Morelos, Mexico; and Carrie Bow Cay, Belize. We collected coral samples along intracolony axes, and Symbiodinium within O. faveolata samples was analyzed using the nuclear ITS2 region and chloroplast 23S rDNA genotyping. O. faveolata associated with species of Symbiodinium in clades A (type A3), B (B1 and B17), C (C3, C7, and C7a), and D (D1a/Symbiodinium trenchii). Within-colony distributions of Symbiodinium species correlated with light availability, cardinal direction, and depth, resulting in distinct zonation patterns of endosymbionts within a host. Symbiodinium species from clades A and B occurred predominantly in the light-exposed tops, while species of clade C generally occurred in the shaded sides of colonies or in deeper-water habitats. Furthermore, geographic comparisons of host–symbiont associations revealed regional differences in Symbiodinium associations. Symbiodinium A3 was detected in Mesoamerican coral colonies, but not in colonies from the Florida Keys or Bahamas. Likewise, Symbiodinium B17 was unique to Mesoamerican O. faveolata, whereas Symbiodinium B1 was found at all localities sampled. However, using cp23S genotyping paired with ITS2 analysis revealed geographically endemic haplotypes among Symbiodinium clades A, B, and C. Since Symbiodinium spatial heterogeneity among this coral species is greater than most corals, a question arises as to whether all western Atlantic populations of O. faveolata should be considered equally “threatened”? Alternatively, geographically and spatially distinct coral–symbiont associations may benefit from specialized management protocols.