Persistent changes in coral-microalgal symbioses with climate change-amplified heat stress

Date

2025

Authors

Buzzoni, Daisy

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Abstract

Climate change-amplified marine heatwaves pose the greatest threat globally to the future of coral reefs. The algal symbionts (family Symbiodiniaceae) hosted by corals are intimately linked to host physiology and as such the composition of corals’ symbiont assemblages can have dramatic consequences for their survival under stress and resilience through bleaching events. This dissertation addresses persistent changes in symbiont assemblages using empirical datasets from study sites characterising exposure to globally relevant stressors. The island of Kiritimati (central Pacific) harbours reefs across a gradient of local human disturbance and was the epicentre for the 2015-2016 tropical Pacific marine heatwave, whilst the reefs of Palau (Micronesia) have experienced consistent local differences in historical marine heatwave exposure. Prior to analysing datasets from these study sites, I review evidence of the effects of climate change on the interactions between eukaryotic hosts and their microbial symbionts from a range of ecosystems to better inform hypotheses involving coral-Symbiodiniaceae responses: I summarise ongoing shifts in diversity, flexibility, and degree of parasitism in terrestrial and aquatic symbioses and reveal a pervasive lack of longitudinal data tracking long-term symbiotic changes or stability. Then, using ITS2 DNA metabarcoding to characterise Symbiodiniaceae in coral tissue samples from Kiritimati collected from 2014 to 2019 and spanning the 2015-16 marine heatwave, I reveal greater temporal and spatial flexibility in the symbiont taxa hosted by coral species that inherit their symbionts horizontally (from their environment) compared to those that inherit symbionts vertically (from their parents). The heatwave-induced changes detected over 5 years within corals’ symbiont assemblages were smaller with increasing human disturbance in corals with horizontal symbiont inheritance and greater in those with vertical symbiont inheritance, exposing contrasting effects of multiple stressor exposure on symbioses for these two coral life histories. I then report findings from a decade-long time series which revealed factors shaping the recovery trajectories of heatwave-transformed coral-Symbiodiniaceae associations for one coral species on Kiritimati. The extreme intensity of acute heat stress exposure disrupted reversion to pre-heatwave symbiont assemblages, promoting the dominance of stress-tolerant generalist symbionts, with differential local disturbance exposure shaping the succession of recovered assemblages through intermediary symbiont community compositions. Finally, in a coral species with comparatively more specific symbiont associations in Palau, I uncover increased symbiont diversity at fine taxonomic scales associated with increased historical heat stress exposure spanning more than 20 years. Experimental heat exposure revealed that the symbiont taxa driving this increased diversity were linked to low heatwave tolerance in corals from historically more heat-stressed reefs, but not in corals from historically less heat-stressed reefs, reflecting a putative interaction between symbiont function and chronic heat stress. This dissertation addresses uncertainty surrounding the fate of climate change-transformed symbioses by assessing the long-term changes in other symbiotic study systems, the spatial and temporal flexibility in coral-symbiont associations over multiple years, the persistence of heatwave-transformed symbiont assemblages, and the links between chronic historical heat stress, Symbiodiniaceae, and heatwave tolerance. This research has applicability to coral reef conservation through improved understanding of the mechanisms driving natural variation in bleaching resilience and addresses foundational questions in symbiosis ecology under climate change and human disturbance, with relevance to other symbiotic systems.

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Keywords

Climate change, Coral, Coral bleaching, Marine heatwave, Symbiosis, Symbiodiniaceae

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