Publication Date

2013-12-10

Availability

Embargoed

Embargo Period

2015-12-10

Degree Type

Dissertation

Degree Name

Doctor of Philosophy (PHD)

Department

Marine Biology and Fisheries (Marine)

Date of Defense

2013-11-08

First Committee Member

Andrew C. Baker

Second Committee Member

Douglas L. Crawford

Third Committee Member

Peter W. Glynn

Fourth Committee Member

Diego Lirman

Fifth Committee Member

Rebecca L. Vega Thurber

Abstract

The continued growth and survival of reef-building corals is essential to sustain the goods and services provided by coral reefs, worth billions of dollars annually. However, warming oceans are causing more frequent and severe episodes of coral bleaching, the breakdown of symbiosis between corals and their algal symbionts (Symbiodinium spp.), which threatens corals’ survival unless they can adapt or acclimatize. One way that corals may increase their thermal tolerance is by associating with different Symbiodinium types. Changes in partner abundance may also have functional consequences, but these symbiont dynamics are poorly understood. This dissertation aims to provide a clearer understanding of Symbiodinium community dynamics in corals by investigating changes in both partner identity and abundance over time, the factors driving these changes, and their functional consequences. First, I developed methods to analyze Symbiodinium community structure based on quantitative PCR, overcoming limitations of other techniques while providing a more physiologically relevant metric of symbiont density – the symbiont to host cell ratio. I then applied these techniques to simultaneously assay symbiont identity and abundance in corals under fluctuating environmental conditions. I show that naturally-variable symbiont densities converged under constant conditions to clade-specific equilibria and readjusted to new equilibria when conditions change. To explain these patterns, I used a mathematical  model to show that corals maintain an “optimal” symbiont abundance in a given environment that maximizes the net benefit of the symbiosis, suggesting that partner density regulation facilitates coral acclimatization in a dynamic environment. While symbiont abundance in the Pacific coral Pocillopora damicornis increased under warmer temperatures, corals with more symbionts were more susceptible to thermal bleaching, establishing a quantitative mechanistic link between symbiont abundance and the molecular basis for coral bleaching. Higher symbiont abundance also caused more severe bleaching in the Caribbean corals Orbicella faveolata and Siderastraea siderea, confirming the generality of this phenomenon and indicating that environmental conditions that increase symbiont densities, such as nutrient pollution, may exacerbate climate change-induced coral bleaching. However, corals may resist bleaching by increasing the relative proportion of thermally tolerant symbionts, which I show is more likely to occur when corals bleach more severely and recover at higher temperatures. These findings reconcile conflicting reports over whether corals change their symbionts in response to environmental stress by showing that the magnitude of symbiont shuffling is determined within an ecological framework by disturbance, niche differentiation, and competition among symbiont types. However, species-specific influences also determine symbiont community trajectories, evidenced by greater shifts to thermally tolerant communities in S. siderea compared to O. faveolata. To investigate potential tradeoffs associated with thermally tolerant symbionts, I measured growth rates of P. damicornis with different symbionts at three temperatures and found that while thermally tolerant symbionts reduced coral growth at cool temperatures, this disadvantage was ameliorated by warming, suggesting that in warmer oceans, these symbionts will benefit reefs by enhancing coral survival at no cost to growth. Finally, a survey of thermally tolerant symbionts in different Pocillopora lineages revealed common associations across host taxa, indicating the widespread relevance of symbiont community variation and dynamics. In summary, this dissertation illustrates that coral performance and stress- tolerance are influenced by both symbiont identity and abundance, which are highly dynamic and change in accordance with principles of community ecology. These findings illustrate the importance of symbiotic dynamism in adaptation and acclimatization in diverse biological systems, while highlighting the major role that Symbiodinium community ecology may play in determining the future of coral reefs.

Keywords

coral reefs; coral; Symbiodinium; symbiosis; climate change

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