The Importance of the Rare: The Role of Background Symbiodinium in the Response of Reef Corals to Environmental Change

• Main Author: Silverstein, Rachel N.
• Other Authors: Andrew Baker, Danielle McDonald, Michael Schmale, Diego Lirman, Rebecca Vega-Thurber
• Format: Other/Unknown Material
• Language: unknown
• Published: Scholarly Repository 2012
• Subjects: coral reefs; Symbiodinium; climate change; symbiosis; resilience; qPCR; Ocean acidification
• Online Access: https://scholarlyrepository.miami.edu/oa_dissertations/910; https://scholarlyrepository.miami.edu/cgi/viewcontent.cgi?article=1917&context=oa_dissertations

Reef ecosystems throughout much of the tropics are predicted to decline in coral cover and diversity as a result of ongoing climate change (ocean acidification, temperature increases, sea level rise), disease, pollution, and overfishing. Corals may be able to respond to some of these stressors by associating with diverse algal symbionts (Symbiodinium spp.) which vary in their physiological traits and therefore expand corals’ realized niche space. This dissertation used high-sensitivity molecular techniques to investigate the presence and functional role of "background" or "rare" Symbiodinium, which occur at low abundance, and therefore may not be detected using standard molecular methods. First, in order to determine the prevalence of mixed-clade symbiont communities (including potentially low-abundance populations), I used a highly-sensitive, real-time PCR assay to analyze archived DNA from a collection of geographically and phylogenetically diverse corals. I found that mixed-clade Symbiodinium communities were common, and that clades C and D were present in all 39 coral species examined. These findings provide strong evidence that no coral species is restricted to hosting only a single symbiont type. I then investigated the functional role of low-abundance symbionts through a series of bleaching and recovery experiments involving the Caribbean coral Montastraea cavernosa. I monitored changes in symbiont community structure using newly-designed quantitative PCR assays, and monitored symbiont community function using chlorophyll fluorometry. Corals hosted only clade C symbionts before bleaching (except for 2 of 139 cores which hosted trace amounts of clade D as well). All bleached colonies (both herbicide-bleached and heat-bleached) recovered with dominant communities of clade D symbionts at both 24oC and 29oC recovery temperatures. Therefore, low-abundance (or even undetectable) symbionts became dominant in corals after disturbance. Increased temperatures, without acute disturbance, underwent less-dramatic, slower symbiont community changes. Corals that bleached, but which were not exposed to heat either during bleaching or during recovery, recovered with fewer D1a symbionts than corals bleached by heat or acclimated to higher temperatures. During a third experiment, I used these same corals to investigate how changes in symbiont clade, past thermal history, and host genotype, affect coral thermotolerance during a second heat stress exposure. I found that, during heat stress, previously-bleached corals hosting D1a symbionts lost fewer symbionts and exhibited less photochemical damage than corals hosting C3 symbionts. Prior heat exposure, either during bleaching or during recovery, did not increase coral thermotolerance, unless it was also associated with symbiont community shifts to D1a-dominance. This demonstrates that rare (or even undetectable symbionts) can become dominant, and can eventually play a critical role in coral bleaching response. Finally, a two-part experiment investigated the effect of incremental warming and cooling on these corals. D1a symbionts in corals that were incrementally heated to 33oC had higher photochemical efficiency than cores containing C3 symbionts, and experienced less symbiont loss. During cooling, however, the photochemical efficiency of D1a was either equal to, or lower than C3. Despite this, fewer D1a symbionts were still lost compared to C3. This suggests that photochemical efficiency and symbiont loss may be decoupled from one another during stress, and that D1a symbionts may be generally more resistant to expulsion, regardless of their performance in hospite. This study also shows that M. cavernosa corals hosting D1a can expand their realized thermal niches wider corals hosting C3 symbionts, reinforcing the importance of functional redundancy in dynamic environments. Together, these studies show that mixed algal symbiont communities can increase both the resistance and resilience of corals to stress and disturbance. These findings have indicate that symbiont community shifts have the potential to allow reef corals to rapidly adapt or acclimatize to environmental change.