CORE Metadata, citation and similar papers at core.ac.uk Provided by HKU Scholars Hub The Effects Of Symbiodinium (pyrrhophyta) Identity On Growth, Title Survivorship, And Thermal Tolerance Of Newly Settled Coral Recruits McIlroy, SE; Gillette, P; Cunning, R; Klueter, A; Capo, T; Baker, Author(s) AC; Coffroth, MA Citation Journal of Phycology, 2016, v. 52 n. 6, p. 1114-1124 Issued Date 2016 URL http://hdl.handle.net/10722/232832 The definitive version is available at www.blackwell- synergy.com; This work is licensed under a Creative Commons Rights Attribution-NonCommercial-NoDerivatives 4.0 International License. J. Phycol. *, ***–*** (2016) © 2016 Phycological Society of America DOI: 10.1111/jpy.12471 THE EFFECTS OF SYMBIODINIUM (PYRRHOPHYTA) IDENTITY ON GROWTH, SURVIVORSHIP, AND THERMAL TOLERANCE OF NEWLY SETTLED CORAL RECRUITS1 Shelby E. McIlroy2,3 Graduate Program in Evolution, Ecology, and Behavior, University at Buffalo, 126 Cooke Hall, Buffalo New York 14260, USA Phillip Gillette, Ross Cunning Department of Marine Biology and Ecology, Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Csy, Miami Florida 33149, USA Anke Klueter Department of Geology, University at Buffalo, 126 Cooke Hall, Buffalo New York 14260, USA Tom Capo, Andrew C. Baker Department of Marine Biology and Ecology, Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Csy, Miami Florida 33149, USA and Mary Alice Coffroth Graduate Program in Evolution, Ecology, and Behavior, University at Buffalo, 126 Cooke Hall, Buffalo New York 14260, USA For many coral species, the obligate association conditions similar to those measured at settlement with phylogenetically diverse algal endosymbiont habitats. species is dynamic in time and space. Here, we used Key index words: Orbicella faveolata; photophysiology; controlled laboratory inoculations of newly settled, recruits; stress; symbiosis aposymbiotic corals (Orbicella faveolata) with two 0 cultured species of algal symbiont (Symbiodinium Abbreviations: ΔFv/F m, effective photochemical microadriaticum and S. minutum) to examine the role efficiency; cp23S, chloroplast large subunit; FSW, of symbiont identity on growth, survivorship, and filtered seawater; Fv/Fm, maximum photochemical thermal tolerance of the coral holobiont. We efficiency; ITS, internal transcribed spacer; KML, evaluated these data in the context of Symbiodinium Keys Marine Laboratory; PAM, pulse amplitude photophysiology for 9 months post-settlement and modulated; PSII, photosystem II; rETR, relative also during a 5-d period of elevated temperatures Electron Transport Rate; RLC, rapid light curves; Our data show that recruits that were inoculated rmANOVA, repeated measures analysis of variance; with S. minutum grew significantly slower than those SA, surface area; a, maximum light utilization inoculated with S. microadriaticum (occasionally coefficient co-occurring with S. minutum), but that there was no difference in survivorship of O. faveolata polyps infected Symbiodinium with . However, photophysiological metrics The symbiosis between scleractinian corals and (ΔFv/F0m, the efficiency with which available light is a their algal endosymbionts is a two-way exchange of used to drive photosynthesis and , the maximum resources that has allowed coral reefs to dominate light utilization coefficient) were higher in those S. minutum in high light, oligotrophic tropical oceans. With slower growing recruits containing . photosynthetically derived energy, algal symbionts These findings suggest that light use (i.e., of the genus Symbiodinium provide their host corals photophysiology) and carbon acquisition by the with both essential and energy-rich metabolites that coral host (i.e., host growth) are decoupled, but did drive growth, calcification and survival of reef build- not distinguish the source of this difference. Symbiodinium ing corals. The light-rich host tissue environment Neither treatment demonstrated a promotes photosynthesis in Symbiodinium, which also significant negative effect of a 5-d exposure to ° receives recycled inorganic nutrients from their host temperatures as high as 32 C under low light (reviewed in Sheppard et al. 2009). The genetically diverse genus Symbiodinium com- 1Received 11 March 2016. Accepted 23 August 2016. 2 prises at least nine deeply divergent “clades” Present address: The University of Hong Kong, Kadoorie Biologi- (Pochon et al. 2014) within and among which there cal Sciences Building, Pokfulam Road, Hong Kong. 3Author for correspondence: e-mail: [email protected]. is a high level of species, physiological, and ecologi- Editorial Responsibility: S. Lin (Associate Editor) cal diversity (reviewed in Baker 2003), including 1 2 SHELBY E. MCILROY ET AL. taxa that are host generalists and specialists, as well 2003, van Oppen et al. 2009), information on how as free living strains (Pochon et al. 2010, Thornhill Symbiodinium strains affect the ecology of newly set- et al. 2014). Much research has focused on how this tled and juvenile corals is limited. Indo-Pacific Acrop- diversity relates to holobiont (coral and associated ora have been the focus of the majority of these symbionts) fitness in the field (e.g., Glynn et al. studies, and that research has revealed that variation 2001, Baker et al. 2004, Little et al. 2004, Warner among juvenile host–symbiont pairings leads to et al. 2006, Abrego et al. 2008, Putnam et al. 2012, important differences in polyp budding rates (Little Edmunds et al. 2014, Kemp et al. 2014), particularly et al. 2004), host carbon acquisition (Cantin et al. thermal tolerance. Horizontal transmission of sym- 2009), skeletal deposition (Jones and Berkelmans bionts, in which aposymbiotic larvae or newly settled 2010, Yuyama and Higuchi 2014), energetics (Jones polyps take up a diverse set of Symbiodinium strains and Berkelmans 2011), and thermal stress responses from the environment de novo each generation, is (Abrego et al. 2008, Howells et al. 2012, Yuyama common in scleractinian corals (Little et al. 2004, and Higuchi 2014). Importantly, associations of the Coffroth et al. 2006, Baird et al. 2009, Cumbo et al. same Symbiodinium species can have differing effects 2013, Poland et al. 2013). However, only a small on juvenile versus adult hosts. For example, adult portion of the available research has focused on Acropora millepora hosting Symbiodinium D1a are less coral juveniles in the first year(s) post settlement, sensitive to thermally induced bleaching compared the time period during which the symbiosis is first to those hosting C2 (Berkelmans and van Oppen established for horizontally transmitting corals and 2006) while the opposite is true for juveniles of the can be highly flexible (Coffroth et al. 2001, Little closely related Acropora tenuis hosting Symbiodinium et al. 2004, Abrego et al. 2009, Poland et al. 2013). D1 or C2 (Abrego et al. 2008). In the Caribbean, While both host-mediated (Dunn and Weis 2009, the coral juvenile life stage has been shown to be an Voolstra et al. 2009, Poland 2010) and environmen- important factor in structuring reef communities tally mediated (Abrego et al. 2012) changes in the (Miller et al. 2000) with growth within the first 1– dominant symbiont type occur as corals develop 2 years post settlement having a critical influence into adults, it is common that representatives from on survival (Rylaarsdam 1983, Edmunds and Gates two to four Symbiodinium clades remain present 2004). This emphasizes the importance of under- within adult scleractinian host tissues at various standing the ecology of newly settled and juvenile levels of abundance (Finney et al. 2010, Silverstein corals especially for dominant Caribbean reef et al. 2012), although usually with a particular sym- builders including Orbicella spp. biont phylotype (Rowan et al. 1997, Glynn et al. To better understand the mechanisms underpin- 2001, Goulet 2006, Kemp et al. 2008) or even iso- ning physiological differences among coral individu- clonal algal strain (Goulet and Coffroth 2003, als hosting different Symbiodinium species, analyses Baums et al. 2014) dominating within the host or of photophysiology have become common for both within a section of host tissue. In adult colonies, cultured and in-hospite Symbiodinium. Most common changes in the dominant symbiont type can is the use of pulse amplitude modulated (PAM) flu- enhance stress tolerance for the coral host (Budde- orometry to measure chlorophyll fluorescence and meier and Fautin 1993, Cunning et al. 2015, Silver- infer pathways of light-energy flow through the pho- stein et al. 2015). tosynthetic machinery. Various components of pho- Interestingly, changes in symbiont community tophysiology, particularly the rate and efficiency structure unrelated to environmental conditions with which light energy is used in photochemistry, occur during coral ontogeny, suggesting essential, can be assessed using PAM fluorometry, but, due to yet understudied, differences in the symbiosis of the complexities of photosynthesis (i.e., the conver- juveniles versus adult coral–Symbiodinium interac- sion of that light energy into fixed carbon), studies tions that could include metabolic differences and/ that employ PAM fluorometry exclusively are limited or immature endosymbiont recognition capacity. in their ability to predict the quality of a symbiont Juveniles of the octocoral Briareum asbestinum are with regard to the algae’s contribution of carbon to dominated by one clade B Symbiodinium phylotype their