Award: OCE-1130786

Coral species richness and abundance are in decline worldwide, due in large part, to anthropogenic impacts such as global climate change, eutrophication, and reductions in fish biodiversity and abundance. In the Caribbean, important drivers of coral declines have been algal competition and outbreaks of coral disease, underscoring the importance of understanding the role of algae-mediated shifts in microbial communities on reef systems. Our experiments represented novel field examinations of the impacts of multiple stressors on corals and their microbial associates on coral reefs in the Florida Keys, USA. Our experiments have confirmed some important hypotheses in the field that, to date, have only been supported by correlative data or have had no actual empirical support. For example, we have shown that long-term nutrient enrichment can increase the prevalence and severity of some coral diseases. Further, long-term enrichment also lowers some corals? thermal thresholds and increases their susceptibility to coral bleaching with increasing sea surface temperatures. Yet, we have also shown that reducing nutrient loading helps to reverse the trend in disease and bleaching prevalence. These patterns suggest that local actions such as better wastewater management and reductions in terrestrial runoff near local reef systems could help protect corals from global-scale stressors such as climate change. We used an ambitious 3-year field experiment that simulated overfishing and nutrient pollution and traced their cascading effects on benthic communities and coral microbiomes across a series of naturally occurring thermal anomalies. Our results clearly show that removal of herbivorous fishes, and to some extent increasing nutrient pollution, radically disrupts reef communities at all levels of biological organization, from parrotfish and algae to corals and coral microbes. Removing herbivores increases algal abundance results in direct overgrowth of corals, but also dramatically changes the coral microbiome, making it more variable and increasing visible coral disease. Disruption of the coral microbiome was linked to declines in coral health and increases in coral mortality. In addition to algae-mediated effects, we surprisingly found that nutrient pollution alters the outcome of a key species interaction supporting reef ecosystem function. While parrotfish often prey on corals as part of their diet, this predation typically causes negligible mortality (0% in control corals). With simulated nutrient pollution, parrotfish predation induced 60% mortality in Porites corals, turning a coral ally into an agent of coral decline. In combination, these effects of local stressors caused coral mortality rates to rise from 5% in control plots to almost 40% in treatments. Further, these local stressors interacted with warm thermal anomalies to drive coral mortality, with ~80% of coral mortality occurring during the warmest parts of the year. Control corals suffered virtually no mortality during these warm events. We document that these thermal anomalies further disrupted the coral microbiome of unhealthy corals, providing a likely mechanism by which thermal stress exacerbates the negative effects of algal competition on the health of corals and their microbiome. Our work provides fundamental insight into the dynamics of and challenges to coral reefs, one of the world?s most charismatic ecosystems, and will be important for coral management and conservation. Ultimately, we demonstrate that local overfishing or nutrient pollution can combine with climate change to cause a cascade of negative interactions that fundamental reorganize reef communities down to the microbial level. Our grant integrated 3 postdoctoral scholars, 9 graduate students, and 30+ undergraduate students into the projects on our grant. Our grant has directly produced 2 PhD dissertations and 1 M.S. thesis. We have had over twenty undergraduate students volunteer as lab technicians working on the project with 75% of these being underrepresented minorities (e.g. Hispanic, black, female). These students have received a broad introduction to our science that expands their horizons as to what marine biology actually is. We made significant effort to engage local communities in South Florida as well as produce widely distributed videos that outline the threats to coral reefs and how our research addresses those threats. We started a regional science café called "Eat, Think, and Be Merry!" to provide a casual environment for the public to come together with local scientists to learn about and discuss science and conservation topics with a specific focus on marine biology and the ecosystems of South Florida. During 2013-2015 we held sixteen events that brought in speakers from both academia and non-governmental organizations. The topics ranged from climate change and tropical forests to the potential effects of sea level rise. Our attendance ranged from 20-35 people from both the local community and from nearby universities. We were very pleased with the level of discourse and the insightfulness of many of the questions from the lay audience. Our project is listed on the BCO-DMO website to facilitate sharing our water column nutrient, temperature, benthic community composition data, and microibla 16S community data. The URL for the BCO-DMO project is http://www.bco-dmo.org/project/529590. Last Modified: 12/05/2016 Submitted by: Deron E Burkepile