Pan-Caribbean emergence and persistence of Durusdinium spp. driven by bleaching stress

The increasing severity and frequency of mass bleaching events has placed shallow water tropical coral reefs at risk of significant decline in the coming decades. The association of endosymbiotic dinoflagellates (Family: Symbiodiniaceae) with corals is regulated by local environmental conditions along with evolutionary history, and plays a leading role in bleaching sensitivity and recovery. Resolving temporal and spatial dynamics of coral-Symbiodiniaceae association is therefore essential for accurate bleaching risk predictions. Here, we investigate temporal patterns in dominant Symbiodiniaceae across the Greater Caribbean region – which is heavily impacted by human activities, disease and climate change. Using records derived from genetic databases, we consider Symbiodiniaceae dominance from 1994-2009, with a particular focus on and around the 2005 mass bleaching event. From the four Symbiodiniaceae genera recorded (Symbiodinium, Breviolum, Cladocopium and Durusdinium spp.), we identified genera-specific responses to ocean heating and bleaching stress. Generalist symbiont representatives were dominant only during periods of sustained environmental stability. In contrast, during and immediately after bleaching saw the emergence and subsequent persistence of Durusdinium spp. – an invasive genus in the Caribbean with high thermal tolerance but induces negative impacts on coral physiology and calcification. In post-bleaching recovery years, a regional-scale bet-hedging strategy was adopted allowing thermal tolerance to be maintained, but with poise for a more physiologically-beneficial symbiosis if / when environmental conditions become favourable. Our regional-scale, multi-year perspective gives support for local / colony-scale tuning of coral-Symbiodiniaceae relationships, and highlights how continued warming and bleaching stress will enable Durusdinium spp. invasion to persist, with knock-on implications for future coral reef development.

大规模珊瑚白化事件的严重程度与发生频率持续攀升，已使浅水热带珊瑚礁在未来数十年面临大幅衰退的风险。珊瑚与内共生甲藻（Symbiodiniaceae科）的共生关系，受局地环境条件与演化历史共同调控，同时在珊瑚白化敏感性及恢复过程中发挥核心作用。因此，厘清珊瑚-虫黄藻共生关系的时空动态，对精准预测白化风险至关重要。本研究聚焦受人类活动、病害与气候变化严重影响的大加勒比海区，对该区域内占优势地位的虫黄藻（Symbiodiniaceae）的时间分布模式展开调查。研究利用遗传数据库中的记录，分析了1994年至2009年间虫黄藻的优势类群分布，并重点关注2005年大规模白化事件及其前后时段。在记录到的4个虫黄藻属（Symbiodinium、Breviolum、Cladocopium及Durusdinium spp.）中，本研究发现了各属对海洋升温与白化胁迫的特异性响应：泛化共生体类群仅在环境持续稳定的时期占据优势地位。与之形成鲜明对比的是，在白化发生期间及白化后即刻，Durusdinium spp.类群会大量出现并持续存在——该属是加勒比海区的入侵类群，虽耐热性极强，但会对珊瑚的生理机能与钙化过程产生负面影响。在白化后的恢复年份中，该区域采取了一种区域尺度的风险对冲共生策略：既维持了耐热性，又能在环境条件适宜时，灵活转向更具生理收益的共生关系。本研究的区域尺度、多年观测视角，为珊瑚-虫黄藻共生关系的局地/珊瑚群体尺度调控提供了支撑，并揭示了持续升温与白化胁迫将如何让Durusdinium spp.的入侵态势得以延续，进而对未来珊瑚礁的发育产生连锁影响。