Coral Reefs (2015) 34:535–547 DOI 10.1007/s00338-015-1277-z REPORT Spatially distinct and regionally endemic Symbiodinium assemblages in the threatened Caribbean reef-building coral Orbicella faveolata Dustin W. Kemp • Daniel J. Thornhill • Randi D. Rotjan • Roberto Iglesias-Prieto • William K. Fitt • Gregory W. Schmidt Received: 28 October 2014 / Accepted: 19 February 2015 / Published online: 27 February 2015 Ó Springer-Verlag Berlin Heidelberg 2015 Abstract Recently, the Caribbean reef-building coral Or- with species of Symbiodinium in clades A (type A3), B (B1 bicella faveolata was listed as ‘‘threatened’’ under the U.S. and B17), C (C3, C7, and C7a), and D (D1a/Symbiodinium Endangered Species Act. Despite attention to this species’ trenchii). Within-colony distributions of Symbiodinium conservation, the extent of geographic variation within O. species correlated with light availability, cardinal direction, faveolata warrants further investigation. O. faveolata is and depth, resulting in distinct zonation patterns of en- unusual in that it can simultaneously harbor multiple ge- dosymbionts within a host. Symbiodinium species from netically distinct and co-dominant species of endosymbiotic clades A and B occurred predominantly in the light-exposed dinoflagellates in the genus Symbiodinium. Here, we inves- tops, while species of clade C generally occurred in the tigate the geographic and within-colony complexity of shaded sides of colonies or in deeper-water habitats. Fur- Symbiodinium-O. faveolata associations from Florida Keys, thermore, geographic comparisons of host–symbiont asso- USA; Exuma Cays, Bahamas; Puerto Morelos, Mexico; and ciations revealed regional differences in Symbiodinium Carrie Bow Cay, Belize. We collected coral samples along associations. Symbiodinium A3 was detected in Me- intracolony axes, and Symbiodinium within O. faveolata soamerican coral colonies, but not in colonies from the samples was analyzed using the nuclear ITS2 region and Florida Keys or Bahamas. Likewise, Symbiodinium B17 was chloroplast 23S rDNA genotyping. O. faveolata associated unique to Mesoamerican O. faveolata, whereas Symbio- dinium B1 was found at all localities sampled. However, using cp23S genotyping paired with ITS2 analysis revealed Communicated by Biology Editor Dr. Simon Davy geographically endemic haplotypes among Symbiodinium D. W. Kemp (&) Á W. K. Fitt clades A, B, and C. Since Symbiodinium spatial hetero- Odum School of Ecology, University of Georgia, Athens, geneity among this coral species is greater than most corals, a GA 30602, USA question arises as to whether all western Atlantic populations e-mail: [email protected] of O. faveolata should be considered equally ‘‘threatened’’? D. J. Thornhill Alternatively, geographically and spatially distinct coral– Department of Biological Sciences, Auburn University, Auburn, symbiont associations may benefit from specialized man- AL 36849, USA agement protocols. R. D. Rotjan John H. Prescott Marine Laboratory, New England Aquarium, Keywords Biogeography Á Ecological speciation Á Boston, MA 02110, USA Endangered Species Act Á Orbicella faveolata Á Symbiosis Á Symbiodinium R. Iglesias-Prieto Unidad Acade´mica de Sistemas Arrecifales, Puerto Morelos, Instituto de Ciencias del Mar y Limnologı´a, Universidad Nacional Auto´noma de Me´xico, Puerto Morelos, Mexico Introduction G. W. Schmidt Department of Plant Biology, University of Georgia, Athens, Coral reefs are among the most biologically rich and pro- GA 30602, USA ductive ecosystems in the world. Reef-building corals are 123 536 Coral Reefs (2015) 34:535–547 fundamentally important, serving as ecosystem engineers Reed 1985; Aronson et al. 2008). However, declines of this that form the structural basis for the ecosystem (Jones et al. species throughout the Caribbean (Miller et al. 2009) 1994). However, coral reefs are among the most globally caused the Center for Biological Diversity to seek protec- threatened ecosystems (Hoegh-Guldberg and Bruno 2010). tion of O. faveolata as a threatened species under the ESA. Rapid coral declines have resulted in substantial habitat Furthermore, O. faveolata routinely hosts multiple ge- loss revealing organismal sensitivity to environmental netically distinct and co-dominant Symbiodinium spp., and perturbations (Gardner et al. 2003). Current conservation these symbionts may likewise differ across the range of the and management efforts are focused on ways to minimize host (LaJeunesse 2002; Garren et al. 2006). Symbiodinium species decline and aid ecosystem recovery that may po- species associated with O. faveolata include members of tentially promote ecosystem resilience (capacity for stress clades A, B, C, and D that are distributed across the resistance and recovery) to local stressors (i.e., over-fish- landscape of the colony (Rowan and Knowlton 1995; ing, nutrient influx, sedimentation) and global climate Toller et al. 2001b; Garren et al. 2006; Kemp et al. 2008). change (Mumby and Steneck 2008; Anthony et al. 2014). Various types of Symbiodinium clades A and B tend to Reef-building corals confront managers with multiple dominate the light-exposed colony tops, with clade C types challenges due to biologic complexity and geographic found in greatest abundance on the colony sides, and specificity of host-symbiotic associations. Reef-building Symbiodinium ITS2 type D1a (S. trenchii) found in stress- corals are highly sensitive to environmental perturbations; exposed colonies (Rowan and Knowlton 1995; Toller et al. however, within-species physiologic differences (e.g., 2001a; Thornhill et al. 2006b; Kemp et al. 2008, 2014; thermal and high irradiance tolerance) can result from in- LaJeunesse et al. 2009, 2014). Flexibility in the symbiosis herent and acclimatization protection processes of coral ecology of O. faveolata has been documented spatially and and endosymbiotic algae (Warner and Berry-Lowe 2006; in response to environmental stress; such dynamism can Reynolds et al. 2008; Howells et al. 2013; Palumbi et al. alter coral physiology and stress responses (Rowan et al. 2014). 1997; Toller et al. 2001b; Thornhill et al. 2006b; Warner The relationship between reef-building corals and en- et al. 2006; LaJeunesse et al. 2009; Kemp et al. 2014). dosymbiotic dinoflagellates (genus Symbiodinium) enables Although the symbiosis of O. faveolata is well studied, no coral reefs to thrive in oligotrophic tropical and sub-tro- large-scale survey has investigated Symbiodinium species pical oceans (Muscatine and Porter 1977). Symbiodinium and type diversity within this species across the Caribbean can provide [90 % of the coral’s metabolic requirements basin. Recent evidence from Symbiodinium clade C via photosynthetically fixed carbon that is translocated to demonstrated that O. faveolata and its congeners associate the coral as carbohydrates, fatty acids, sugars, starches, and with highly specific endosymbionts—Symbiodinium species amino acids (reviewed by: Yellowlees et al. 2008). Sym- that apparently do not associate with other host taxa biodinium is a diverse group of dinoflagellates comprising (Thornhill et al. 2014). These host-specific symbionts can be nine major clades (A-I) (Coffroth and Santos 2005; Pochon further divided into regionally endemic lineages and haplo- and Gates 2010) that can be further divided using rapidly types (Thornhill et al. 2014). Such an evolutionary pattern evolving molecular markers into various phylotypes and likely resulted from long-term processes of lineage diversi- species (Sampayo et al. 2009; LaJeunesse and Thornhill fication due to ecological speciation (by host taxa) as well as 2011; LaJeunesse et al. 2012, 2014). Different Symbio- regional differentiation due to allopatry (Santos et al. 2004; dinium spp. often have biochemical differences leading to LaJeunesse 2005, 2010; Thornhill et al. 2009). However, species- and phlyotype-specific physiological responses to such patterns have only been documented in Symbiodinium environmental conditions (Warner et al. 1999; Tchernov clade C for Orbicella. The prevalence of other Symbiodinium et al. 2004; Reynolds et al. 2008; Takahashi et al. 2009). clades and types associated with O. faveolata has been Notably, differential thermal and irradiance tolerances inadequately determined, although preliminary results for have been identified in genetically distinct Symbiodinium, clades A and B—but not D—suggest similar patterns which can lead to different holobiont responses to stress (Thornhill et al. 2010a; Pinzo´n et al. 2011). Thus, we used (Rowan and Knowlton 1995; Baker 2003; Iglesias-Prieto here a micro-sampling technique combined with nuclear ri- et al. 2004). bosomal and chloroplast genotyping of Symbiodinium from Recently the National Oceanic Atmospheric Adminis- O. faveolata colonies to further explore the genotypic var- tration (NOAA) extended Endangered Species Act (ESA) iation in clades and types with respect to geographic corre- protections to the mountainous star coral, Orbicella lates. Colonies were examined in shallow (higher irradiance) faveolata, and 19 other species (NMFS 2014). O. faveolata and deeper (lower irradiance) reefs at four different regions is found from the intertidal zone to 80 m deep and is often of the western Atlantic. the most abundant reef-building coral in forereef environ- We document predictable and stratified heterogeneity of ments throughout the Caribbean (Goreau and Wells 1967; Symbiodinium spp. associated with O. faveolata that likely 123 Coral Reefs (2015) 34:535–547 537 reflects long-term