The differential effects of increasing frequency and magnitude of extreme events on coral populations.

Extreme events, which have profound ecological consequences, are changing in both frequency and magnitude with climate change. Because extreme temperatures induce coral bleaching, we can explore the relative impacts of changes in frequency and magnitude of high temperature events on coral reefs. Here, we combined climate projections and a dynamic population model to determine how changing bleaching regimes influence coral persistence. We additionally explored how coral traits and competition with macroalgae mediate changes in bleaching regimes. Our results predict that severe bleaching events reduce coral persistence more than frequent bleaching. Corals with low adult mortality and high growth rates are successful when bleaching is mild, but bleaching resistance is necessary to persist when bleaching is severe, regardless of frequency. The existence of macroalgae-dominated stable states reduces coral persistence and changes the relative importance of coral traits. Building on previous studies, our results predict that management efforts may need to prioritize protection of "weaker" corals with high adult mortality when bleaching is mild, and protection of "stronger" corals with high bleaching resistance when bleaching is severe. In summary, future reef projections and conservation targets depend on both local bleaching regimes and biodiversity.

Response diversity can increase ecological resilience to disturbance in coral reefs.

Community-level resilience depends on the interaction between multiple populations that vary in individual responses to disturbance. For example, in tropical reefs, some corals can survive higher stress (resistance) while others exhibit faster recovery (engineering resilience) following disturbances such as thermal stress. While each type will negatively affect the other through competition, each might also benefit the other by reducing the potential for an additional competitor such as macroalgae to invade after a disturbance. To determine how community composition affects ecological resilience, we modeled coral-macroalgae interactions given either a resistant coral, a resilient coral, or both together. Having both coral types (i.e., response diversity) can lead to observable enhanced ecological resilience if (1) the resilient coral is not a superior competitor and (2) disturbance levels are high enough such that the resilient coral would collapse when considered alone. This enhanced resilience occurs through competitor-enabled rescue where each coral increases the potential for the other to recover from disturbance through external recruitment, such that both corals benefit from the presence of each other in terms of total cover and resilience. Therefore, conservation management aimed at protecting resilience under global change requires consideration of both diversity and connectivity between sites experiencing differential disturbance.

Symbiotic specificity, association patterns, and function determine community responses to global changes: defining critical research areas for coral-Symbiodinium symbioses.

Climate change-driven stressors threaten the persistence of coral reefs worldwide. Symbiotic relationships between scleractinian corals and photosynthetic endosymbionts (genus Symbiodinium) are the foundation of reef ecosystems, and these associations are differentially impacted by stress. Here, we couple empirical data from the coral reefs of Moorea, French Polynesia, and a network theoretic modeling approach to evaluate how patterns in coral-Symbiodinium associations influence community stability under climate change. To introduce the effect of climate perturbations, we simulate local 'extinctions' that represent either the loss of coral species or the ability to engage in symbiotic interactions. Community stability is measured by determining the duration and number of species that persist through the simulated extinctions. Our results suggest that four factors greatly increase coral-Symbiodinium community stability in response to global changes: (i) the survival of generalist hosts and symbionts maximizes potential symbiotic unions; (ii) elevated symbiont diversity provides redundant or complementary symbiotic functions; (iii) compatible symbiotic assemblages create the potential for local recolonization; and (iv) the persistence of certain traits associate with symbiotic diversity and redundancy. Symbiodinium may facilitate coral persistence through novel environmental regimes, but this capacity is mediated by symbiotic specificity, association patterns, and the functional performance of the symbionts. Our model-based approach identifies general trends and testable hypotheses in coral-Symbiodinium community responses. Future studies should consider similar methods when community size and/or environmental complexity preclude experimental approaches.

Persistence and change in community composition of reef corals through present, past, and future climates.

The reduction in coral cover on many contemporary tropical reefs suggests a different set of coral community assemblages will dominate future reefs. To evaluate the capacity of reef corals to persist over various time scales, we examined coral community dynamics in contemporary, fossil, and simulated future coral reef ecosystems. Based on studies between 1987 and 2012 at two locations in the Caribbean, and between 1981 and 2013 at five locations in the Indo-Pacific, we show that many coral genera declined in abundance, some showed no change in abundance, and a few coral genera increased in abundance. Whether the abundance of a genus declined, increased, or was conserved, was independent of coral family. An analysis of fossil-reef communities in the Caribbean revealed changes in numerical dominance and relative abundances of coral genera, and demonstrated that neither dominance nor taxon was associated with persistence. As coral family was a poor predictor of performance on contemporary reefs, a trait-based, dynamic, multi-patch model was developed to explore the phenotypic basis of ecological performance in a warmer future. Sensitivity analyses revealed that upon exposure to thermal stress, thermal tolerance, growth rate, and longevity were the most important predictors of coral persistence. Together, our results underscore the high variation in the rates and direction of change in coral abundances on contemporary and fossil reefs. Given this variation, it remains possible that coral reefs will be populated by a subset of the present coral fauna in a future that is warmer than the recent past.

Evolution of plant-pollinator mutualisms in response to climate change.

Climate change has the potential to desynchronize the phenologies of interdependent species, with potentially catastrophic effects on mutualist populations. Phenologies can evolve, but the role of evolution in the response of mutualisms to climate change is poorly understood. We developed a model that explicitly considers both the evolution and the population dynamics of a plant-pollinator mutualism under climate change. How the populations evolve, and thus whether the populations and the mutualism persist, depends not only on the rate of climate change but also on the densities and phenologies of other species in the community. Abundant alternative mutualist partners with broad temporal distributions can make a mutualism more robust to climate change, while abundant alternative partners with narrow temporal distributions can make a mutualism less robust. How community composition and the rate of climate change affect the persistence of mutualisms is mediated by two-species Allee thresholds. Understanding these thresholds will help researchers to identify those mutualisms at highest risk owing to climate change.

Transmission mode predicts specificity and interaction patterns in coral-Symbiodinium networks.

Most reef-building corals in the order Scleractinia depend on endosymbiotic algae in the genus Symbiodinium for energy and survival. Significant levels of taxonomic diversity in both partners result in numerous possible combinations of coral-Symbiodinium associations with unique functional characteristics. We created and analyzed the first coral-Symbiodinium networks utilizing a global dataset of interaction records from coral reefs in the tropical Indo-Pacific and Atlantic Oceans for 1991 to 2010. Our meta-analysis reveals that the majority of coral species and Symbiodinium types are specialists, but failed to detect any one-to-one obligate relationships. Symbiont specificity is correlated with a host's transmission mode, with horizontally transmitting corals being more likely to interact with generalist symbionts. Globally, Symbiodinium types tend to interact with only vertically or horizontally transmitting corals, and only a few generalist types are found with both. Our results demonstrate a strong correlation between symbiont specificity, symbiont transmission mode, and community partitioning. The structure and dynamics of these network interactions underlie the fundamental biological partnership that determines the condition and resilience of coral reef ecosystems.