Annual outbreaks of coral disease coincide with extreme seasonal warming

Abstract

Reef-building corals living in extreme environments can provide insight into the negative effects of future climate scenarios. In hot environments, coral communities experience disproportionate thermal stress as they live very near or at their upper thermal limits. This results in a high frequency of bleaching episodes, but it is unknown whether temperature-driven outbreaks of coral disease follow a similar trajectory. Here we tracked outbreaks of a white-syndrome (WS) disease over three years in the hottest region inhabited by reef-building corals, the southern Persian Gulf. From 2014 to 2016, WS affected 10 of the 16 scleractinian genera recorded at inshore and offshore sites. Intra- and inter-specific transmission of lesions was frequently observed, indicative of a single contagious disease infecting multiple coral taxa. Colonies of Acropora were the most susceptible to WS disease and were more than twice as likely to experience lesions than any other genera. Prevalence reached 42% of Acropora colonies and lesions progressed at an average rate of 1 mm day⁻¹. Platygyra colonies were the second most susceptible to WS disease, where prevalence reached 33% and lesions progressed at 0.3 mm day⁻¹. Affected colonies of both of these genera suffered considerable partial mortality that was not recovered between years, promoting the fragmentation of larger colonies into smaller size classes. Across the 3 years of our study, the onset of WS outbreaks occurred early in summer and prevalence increased exponentially with cumulative heat exposure (coral community r² = 0.55, Acropora r² = 0.72, Platygyra r² = 0.75). Peak levels of community-wide prevalence occurred in August (10% of all coral colonies) to September (14%) when preceding 4-week and 8-week average temperatures exceeded 34.5 °C and 34 °C, respectively. Outbreaks ceased following the return of cooler temperatures with prevalence remaining below 0.5% between December and June. Levels of bleaching remained relatively low (< 5% prevalence), despite exposure to daily temperatures ≥ 35 °C each summer. These findings demonstrate that thermal stress on coral reefs does not always manifest as coral bleaching and diseases can present as a primary sign of thermal stress. Consequently, temperature-driven outbreaks of coral disease are expected to become more widespread as climate warming pushes corals to be living increasingly closer to their upper thermal limits.