Reef‐building corals are at risk of extinction from ocean warming. While some corals can enhance their thermal limits by associating with dinoflagellate photosymbionts of superior stress tolerance, the extent to which symbiont communities will reorganize under increased warming pressure remains unclear. Here we show that corals in the hottest reefs in the world in the Persian Gulf maintain associations with the same symbionts across 1.5 years despite extreme seasonal warming and acute heat stress (≥35°C). Persian Gulf corals predominantly associated with Cladocopium (clade C) and most also hosted Symbiodinium (clade A) and/or Durusdinium (clade D). This is in contrast to the neighbouring and milder Oman Sea, where corals associated with Durusdinium and only a minority hosted background levels of Cladocopium. During acute heat stress, the higher prevalence of Symbiodinium and Durusdinium in bleached versus nonbleached Persian Gulf corals indicates that genotypes of these background genera did not confer bleaching resistance. Within symbiont genera, the majority of ITS2 rDNA type profiles were unique to their respective coral species, confirming the existence of host‐specific symbiont lineages. Notably, further differentiation among Persian Gulf sites demonstrates that symbiont populations are either isolated or specialized over tens to hundreds of kilometres. Thermal tolerance across coral species was associated with the prevalence of a single ITS2 intragenomic sequence variant (C3gulf), definitive of the Cladocopium thermophilum group. The abundance of C3gulf was highest in bleaching‐resistant corals and at warmer sites, potentially indicating a specific symbiont genotype (or set of genotypes) that may play a role in thermal tolerance that warrants further investigation. Together, our findings indicate that co‐evolution of host–Symbiodiniaceae partnerships favours fidelity rather than flexibility in extreme environments and under future warming.
Corals in the Persian/Arabian Gulf are the most thermally tolerant in the world, but live very near the thresholds of their thermal tolerance. Warming sea temperatures associated with climate change have resulted in numerous coral bleaching events regionally since the mid-1990s, but it has been unclear why unusually warm sea temperatures occur some years but not others. Using a combination of 5 years of observed sea-bottom temperatures at three reef sites and a meteorologically linked hydrodynamic model that extends through the past decade, we show that summer sea-bottom temperatures are tightly linked to regional wind regimes, and that strong 'shamal' wind events control the occurrence and severity of bleaching. Sea bottom temperatures were primarily controlled by latent heat flux from wind-driven surface evaporation which exceeded 300 W m −2 during shamal winds, double that of typical breeze conditions. Daily temperature change was highly correlated with wind speed, with breeze winds (<4 m s −1) resulting in increased warming, while faster winds caused cooling, with the magnitude of temperature decline increasing with wind speed. Using observed and simulated data from 2012 to 2017, we show that years with reported bleaching events (2012, 2017) were characterized by low winds speeds that resulted in temperatures persisting above coral bleaching threshold temperatures for >5 weeks, while the cooler intervening years (2013-2016) had summers with more frequent and/or strong shamal events which repeatedly cooled temperatures below bleaching thresholds for days to weeks, providing corals temporary respite from thermal stress. Using observed data from 2012 onward and simulated data from 2008 to 2011, we show that the severity of bleaching events over the past decade was linked to both the number of cumulative days above bleaching thresholds (rather than total days, which obfuscates the cooling effects of occasional brief shamal events), as well as to maxima. We show that winds of 4 m s −1 represents a critical threshold for whether or not corals cross bleaching threshold temperatures, and provide simulations to forecast sea-bottom temperature change and recovery times under a range of wind conditions. The role that wind-driven cooling may play on coral reefs globally is discussed.
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 whitesyndrome (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 Keywords Coral disease Á White syndrome Á Persian Gulf Á Arabian Gulf Á Climate warming
Coral reefs are threatened by climate change as coral-algal symbioses are currently living close to their upper thermal limits. The resilience of the algal partner plays a key role in determining the thermal tolerance of the coral holobiont and therefore, understanding the acclimatory limits of present day coral-algal symbioses is fundamental to forecasting corals’ responses to climate change. This study characterised the symbiont community in a highly variable and thermally extreme (Max = 37.5 °C, Min = 16.8 °C) lagoon located in the southern Persian/Arabian Gulf using next generation sequencing of ITS2 amplicons. Despite experiencing extreme temperatures, severe bleaching and many factors that would be expected to promote the presence of, or transition to clade D dominance, the symbiont communities of the lagoon remain dominated by the C3 variant, Symbiodinium thermophilum. The stability of this symbiosis across multiple genera with different means of symbiont transmission highlights the importance of Symbiodinium thermophilum for corals living at the acclimatory limits of modern day corals. Corals in this extreme environment did not undergo adaptive bleaching, suggesting they are living at the edge of their acclimatory potential and that this valuable source of thermally tolerant genotypes may be lost in the near future under climate change.
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