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Seasonal Stability of Coral–Symbiodinium Associations in The Vol. 532: 137–151, 2015 MARINE ECOLOGY PROGRESS SERIES Published July 21 doi: 10.3354/meps11369 Mar Ecol Prog Ser Seasonal stability of coral−Symbiodinium associations in the subtropical coral habitat of St. Lucie Reef, Florida Courtney N. Klepac1,*, Jeff Beal2, Carly D. Kenkel3, Ashley Sproles4, Jennifer M. Polinski1, Maureen A. Williams5, Mikhail V. Matz6, Joshua D. Voss1 1Harbor Branch Oceanographic Institute, Florida Atlantic University, 5600 US 1 Hwy N, Ft. Pierce, FL 34946, USA 2Florida Fish & Wildlife Conservation Commission, Ft. Pierce, FL 34946, USA 3The Australian Institute of Marine Science, PMB No. 3, Townsville MC, Queensland 4810, Australia 4Victoria University of Wellington, Wellington 6012, New Zealand 5Department of Zoology, Trinity College Dublin, College Green, Dublin 2, Ireland 6Department of Integrative Biology, The University of Texas at Austin, 1 University Station C0990, Austin, TX 78712, USA ABSTRACT: The coral community at St. Lucie Reef (Stuart, Florida; 27° 8’ N, 80° 8’ W) is found near the northern latitudinal range limit for Florida reefs and persists under environmental vari- ability from freshwater discharges, summer upwelling, and thermal instability. Since aspects of coral physiology can be attributed to the composition of endosymbiotic zooxanthellae (genus Sym- biodinium), we examined the dynamics of Symbiodinium strains in St. Lucie corals to gain insight into the organization of coral−algal symbioses under local stressors. Two scleractinian coral spe- cies that dominate the reef, Montastraea cavernosa and Pseudodiploria clivosa, were repeatedly sampled at 4 reef sites over 17 mo, during both wet and dry seasons. Symbiodinium cellular den- sity and photosynthetic pigments differed between the 2 coral hosts, where Pseudodiploria clivosa had higher cell densities and chlorophyll concentrations than Montastraea cavernosa. Over time, these parameters varied, but were not significantly altered following freshwater discharge events. Symbiodinium diversity and abundances were identified using ITS2 region amplification and next-generation sequencing, which revealed remarkable stability of the relative proportions of different Symbiodinium genotypes throughout the sampling period. Novel associations with unique Symbiodinium strains observed for each coral species as well as the stability of these symbioses could indicate local adaptation of St. Lucie Reef corals to their marginal environmental conditions. KEY WORDS: Montastraea · Pseudodiploria · Symbiodinium · Symbiosis · Zooxanthellae · Next-generation sequencing Resale or republication not permitted without written consent of the publisher INTRODUCTION clades A–D, F, and G are known to occur in sclerac- tinian corals (Baker 2003). Over the past 2 decades, High productivity of coral ecosystems in shallow much research has focused on determining the diver- waters is primarily attributed to the symbiotic associ- sity and organization of Symbiodinium spp. (Trench ations between corals and single-celled dinoflagel- 1993, LaJeunesse 2002, Savage et al. 2002, La - late algae. These algal symbionts are classified in the Jeunesse et al. 2004, 2010a, Pochon et al. 2006, genus Symbiodinium (Muscatine & Porter 1977), Thornhill et al. 2007, Finney et al. 2010, LaJeunesse which is subsequently subdivided into 9 clades rang- & Thornhill 2011). Taxonomic understanding is lim- ing from A to I (Pochon & Gates 2010). Of these, ited, where sub-generic clades are recognized, and *Corresponding author: [email protected] © Inter-Research 2015 · www.int-res.com 138 Mar Ecol Prog Ser 532: 137–151, 2015 within each clade are types (or sub-clades) that have ence of reef-building corals. The coral−algal symbio- been identified using molecular marker sequence sis can persist, breakdown (as observed during coral differences and DGGE profiles (LaJeunesse 2002, bleaching), undergo advantageous modifications, or 2005, Litaker et al. 2007, Loram et al. 2007, Thornhill evolve adaptive traits (Buddemeier & Fautin 1993, et al. 2007, 2014, Bellantuono & Baker 2008, Sam- Baker 2003, Chen et al. 2005, Berkelmans & van payo et al. 2009, Pochon et al. 2012). Oppen 2006, Thornhill et al. 2006a, LaJeunesse et al. The current understanding of Symbiodinium diver- 2010b). Generally, stable or monotypic Symbio- sity has primarily been achieved through molecular dinium assemblages are maintained under steady genotyping of the ribosomal internal transcribed environmental conditions (La Jeunesse 2002, 2005, spacer region 2 (ITS2; Litaker et al. 2007, Sampayo et LaJeunesse et al. 2004, Thornhill et al. 2006a, Bellan- al. 2009, Stat et al. 2011), but a suite of other markers tuono et al. 2012). Unless resident Symbiodinium are including ITS1, microsatellites, the non-coding re - broadly tolerant to the local environment, advanta- gion of the plastid psbA minicircle, mitochondrial geous responses to environmental change must cytochrome b, and actin genes have been employed occur with the necessary scale and pace to allow for to characterize Symbiodinium variants (van Oppen et acclimatization (Hoegh-Guldberg et al. 2007, Mc - al. 2001, Sampayo et al. 2009, LaJeunesse & Thorn- Ginley et al. 2012, Putnam et al. 2012). To overcome hill 2011, Pochon et al. 2012, LaJeunesse et al. 2014, or recover from stress events, adaptive mechanisms Thornhill et al. 2014). The multicopy nature of the such as symbiont ‘switching’ (symbiont acquisition ITS2 gene (Thornhill et al. 2007, Arif et al. 2014) and from external environmental sources) or ‘shuffling’ the intragenomic sequence variation detected among (differential growth of resident background popula- Symbiodinium within an individual coral can influ- tions) can promote endosymbionts that are physio- ence interpretations regarding the composition of the logically tolerant to thermal stress (Baker et al. 2004). algal assemblage (LaJeunesse 2002, Thornhill et al. Broadly, there is evidence that persistent Symbio- 2007, Sampayo et al. 2009). Increased sequence dinium assemblages can confer increased host sur- diversity estimates revealed using next-generation vival (Berkelmans & van Oppen 2006, Jones et al. sequencing has identified numerous low-abundance 2008). Symbiont switching and shuffling are depicted ITS2 variants that were not previously detected with as a short-term benefit (Mieog 2009, Mieog et al. DGGE (Stat et al. 2011, Silverstein et al. 2012). 2009, Putnam et al. 2012), with ecological conse- Symbiodinium clade distribution within a reef loca- quences such as reduced growth (Jones & Berkel- tion is believed to be primarily determined by reef mans 2010) or increased intraspecific competition. If host species (LaJeunesse et al. 2010b, Davies et al. the coral−algal holobiont association can remain sta- 2014), biogeography (Rodriguez-Lanetty et al. 2003, ble under environmental fluctuations, low symbion- LaJeunesse 2005, Finney et al. 2010, LaJeunesse et tic flexibility may be the result of a fixed trait (Thorn- al. 2010a, Davies et al. 2014, Thornhill et al. 2014) and hill et al. 2006b, Bellantuono et al. 2012, McGinley et environmental conditions that affect photophysiology, al. 2012, Kenkel et al. 2013) or evidence of physio - most notably light and temperature (Rowan & Knowl- logical flexibility by the particular holobiont (Bellan- ton 1995, Warner et al. 1996, LaJeunesse & Trench tuono et al. 2012). 2000, LaJeunesse 2002, Baker 2003, Berkelmans & Many coastal coral reef habitats persist despite van Oppen 2006, Sampayo et al. 2007, Thornhill et al. high thermal variability and intermittent eutrophic 2008, Finney et al. 2010). It is likely that each Symbio- conditions. Elucidating the mechanisms of coral resil- dinium strain has particular environmental thresholds ience has become a priority of coral reef ecology (LaJeunesse & Trench 2000, LaJeunesse 2002), and (ISRS 2004, NOAA Coral Reef Conservation Program genetic differentiation can arise under the demands 2009). Numerous studies have documented coral− of unique environments. One reef locale or region algal responses to episodic and seasonal temperature can contain an ecologically dominant type or an fluctuations (Gates et al. 1992, Jones 1997, Brown et assortment of coexisting types (LaJeunesse 2002, al. 1999). However, the mechanisms that allow corals Baker 2003, Goulet 2006, LaJeunesse et al. 2010a). to persist in subtropical habitats influenced by both Furthermore, the particular coral−Symbiodinium coastal runoff stressors (fluctuating light, salinity, nu- com bination can influence how the holobiont func- trients, and water clarity; Fabricius 2005) and strong tions as an ecological unit and responds to environ- seasonal environmental changes are less understood. mental changes (Berkelmans & van Oppen 2006). Locally adapted Symbiodinium assemblages could Maintenance of Symbiodinium assemblages under exhibit top-down control on responses to changing fluctuating environments is important for the persist- environmental factors, or the environment may im- Klepac et al.: Symbiodinium in Florida corals 139 pose bottom-up influences that ultimately dictate Conversely, if the coral−Symbiodinium association coral−Symbiodinium strain composition. remains relatively stable through time, this relation- St. Lucie Reef (SLR) is a shallow reef habitat within ship may have been conditioned to tolerate the envi- the St. Lucie Inlet State Park in Stuart, Florida, lying ronmental conditions present. 2.3 km south of the St. Lucie Inlet and subject to episodic freshwater discharge events from regulated canals
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