Dynamic symbioses reveal pathways to coral survival through prolonged heatwaves

Climate change has increased the frequency, intensity, and duration of marine heatwaves that cause coral bleaching by disrupting coral–Symbiodiniaceae symbioses. While brief thermal exposure can sometimes induce tolerance, prolonged anomalies typically lead to mass mortality. Management efforts have focused on reducing local stressors to enhance resilience, but evidence for benefits during heatwaves is mixed, and some argue tolerance to heat may correlate with tolerance to other stressors. Assisted evolution approaches aim to exploit Symbiodiniaceae diversity to boost thermal tolerance, yet most studies involve short thermal events that may not represent future prolonged heatwaves. With most reefs experiencing local anthropogenic disturbance, understanding how heatwaves interact with coral symbioses under multiple stressors is critical. This study tests how symbiont identity and chronic human disturbance influence bleaching, recovery, and survival of tagged corals through an unprecedented 2015–2016 heatwave at Kiritimati, evaluating whether heat-sensitive versus heat-tolerant symbiont associations confer resistance or alternative recovery pathways during extended thermal stress.

Prior work shows: (1) Marine heatwaves are increasing globally and have driven catastrophic coral loss. (2) Corals hosting heat-tolerant Symbiodiniaceae, especially Durusdinium, often exhibit elevated bleaching resistance (≈1–1.5 °C increase in tolerance) compared to Cladocopium-dominated corals. (3) Post-bleaching symbiont shifts can increase heat tolerance, but most experimental and field studies evaluated relatively short heat stress. (4) The efficacy of mitigating local stressors to improve bleaching resilience is equivocal, and a ‘protection paradox’ may exist whereby thermal tolerance correlates with tolerance to other stressors. (5) Background, low-abundance heat-tolerant symbionts may be functionally important for recovery in some cases, though other studies suggested they are transient with limited functional significance. The literature leaves open whether these paradigms hold under prolonged heatwaves and how chronic human disturbance modulates symbiont composition and outcomes.

Study system: Kiritimati (Christmas Island), central equatorial Pacific (01°52′N, 157°24′W), spanning a strong spatial gradient of chronic human disturbance (population density within 2 km and fishing pressure). Sites were categorized (very low to very high disturbance) and also analyzed with disturbance as a continuous, square-root transformed metric. Oceanographic covariates (exposure, salinity, pH, dissolved oxygen, wave energy, primary productivity) were quantified to assess potential confounding. Thermal context: In situ temperature loggers (10–12 m depth) and satellite data characterized the 2015–2016 El Niño heatwave. Degree heating weeks (DHW) were computed using local bleaching thresholds. The heatwave reached 31.6 °C-weeks and persisted for ~10 months. Design and sampling: Two massive coral species were studied: Platygyra ryukyuensis and Favites pentagona. A total of 141 tagged colonies were followed at 15 fore reef sites (10–12 m) across expeditions before (Aug 2014; Jan–Feb 2015; Apr–May 2015), during (Jul 2015; Mar 2016), and after (Nov 2016; Jul 2017) the heatwave. Each colony was photographed to assess bleaching and fate (survived/died). Not all sites were visited every season; some colonies were lost (unknown outcome) due to reef degradation. Symbiont identification and abundance: ITS2 metabarcoding (Illumina MiSeq 2×300 bp) characterized Symbiodiniaceae communities for 363 samples from 141 colonies (mean 2.6 time points per colony). Bioinformatics used DADA2 (ASVs) and SymPortal (ITS2-type profiles), with filtering thresholds (≥1000 reads for ASV, ≥250 reads for ITS2-type profiles). Quantitative PCR assays measured symbiont-to-host (S:H) cell ratios and dominant symbiont identity for P. ryukyuensis (n=57 colonies; n=146 samples; analysis subset n=48 colonies, n=131 samples) using actin targets for Cladocopium and Durusdinium and a new coral host PaxC assay. Benthic community: Photoquadrats (1 m²) at 24–30 points along 60 m transects (n=1389 photos) quantified coral cover pre- and post-bleaching; additional photos assessed bleaching at selected times/sites. Statistical analyses: Constrained ordination (CAP) with weighted UniFrac distances tested effects of disturbance and exposure on symbiont communities; significance via permutation tests and model building (vegan). Logistic regressions (bayesglm) examined (i) Durusdinium prevalence vs disturbance (pre-heatwave), (ii) early bleaching probability vs Durusdinium proportion (July 2015), and (iii) survival vs pre-heatwave Durusdinium proportion. Linear mixed-effects models (lme4) analyzed S:H ratios across time with coral ID as random effect and field season as fixed effect; Tukey-corrected post hoc comparisons (emmeans). Sensitivity analyses assessed mortality assumptions.

- Disturbance shapes symbioses pre-heatwave: Human disturbance strongly influenced symbiont identity (P<0.001), more than measured environmental variables. Highly disturbed sites had Durusdinium-dominated corals, while less disturbed sites were Cladocopium-dominated. - Prolonged extreme heatwave: DHW reached 31.6 °C-weeks with ~10 months of elevated temperatures around the atoll. - Bleaching resistance: Two months into the heatwave, Durusdinium-dominated colonies were significantly less likely to have bleached than Cladocopium-dominated colonies (P. ryukyuensis: P=0.020; F. pentagona: P=0.009). - Survival outcomes reversed expectations: By late heatwave, P. ryukyuensis hosting Durusdinium had much lower survival (25%) than those initially hosting Cladocopium (82%) (logistic regression P<0.001). For F. pentagona, a similar trend was non-significant (Durusdinium 46% survival vs Cladocopium 61%; P=0.231). Overall across species with known starting genus, Cladocopium: 73% survived; Durusdinium: 36% survived. - Recovery at elevated temperatures: Many colonies that initially bleached recovered pigmentation and symbiont densities while temperatures were still above bleaching thresholds. Recovery was associated with increases in Durusdinium dominance. - Quantified symbiont dynamics (P. ryukyuensis): Mean S:H ratio before bleaching 0.037±0.010 (time iii) dropped to 0.009±0.003 during early bleaching (time iv; LME F=18, P<0.001), then returned to and slightly exceeded pre-bleaching levels by late-March 2016 (time vi: 0.045±0.006), remaining stable into 2017. - Symbiont shifts: At less disturbed sites, Durusdinium ITS2 profiles increased from rare to dominant during recovery (P. ryukyuensis: 8.96±3.89% to 90.42±3.34%; F. pentagona: 0.07±0.01% to 83.07±5.30%). - Disturbance interaction: The recovery pathway (bleach then recover with Durusdinium during the heatwave) was observed at sites without very high local disturbance. At very high disturbance sites, P. ryukyuensis declines were greater, and initial Durusdinium dominance did not confer a survival advantage. - Trade-off indication: Despite initial bleaching resistance, Durusdinium-dominated colonies (especially P. ryukyuensis) exhibited poorer survival through prolonged stress, consistent with energetic costs of hosting Durusdinium. For P. ryukyuensis, survival with Durusdinium was ~3.3 times lower than with Cladocopium (25% vs 82%).

Findings reveal multiple, symbiont-mediated pathways to survive prolonged heatwaves: (1) resistance via Durusdinium dominance reduces early bleaching risk; and (2) recovery, wherein Cladocopium-dominated corals bleach early but subsequently recover at still-elevated temperatures through proliferation of Durusdinium to densities supporting pigmentation and function. The prolonged nature of the 2015–2016 event allowed observation of recovery above typical thermal thresholds, challenging the paradigm that temperatures must return to normal for recovery to occur. Chronic local disturbance modulated these outcomes: in highly disturbed areas, corals were more often Durusdinium-dominated pre-heatwave, resisted early bleaching, but for P. ryukyuensis suffered lower ultimate survival—likely reflecting trade-offs such as reduced energy delivery from Durusdinium, compromised homeostasis or immunity, and additive local stressors (e.g., turbidity, nutrients, elevated DOC and microbial activity). Approximately two-thirds of surviving colonies that were sampled early had already bleached, underscoring the predominance of recovery over resistance under extended heat stress. These results suggest that management and forecasting must consider variable bleaching and recovery thresholds across host–symbiont pairings and the interaction with local stressors, rather than assuming uniform thresholds.

This natural experiment demonstrates that coral survival through prolonged heatwaves can proceed via distinct pathways mediated by symbiont identity and local disturbance. Although Durusdinium dominance increases initial bleaching resistance, it did not improve, and in P. ryukyuensis reduced, survival through an extended heatwave. Conversely, corals initially hosting Cladocopium often bleached but recovered at elevated temperatures by shifting to Durusdinium, a previously undocumented recovery pathway during ongoing heat stress. These insights reframe bleaching paradigms and highlight that local disturbance can alter symbiont composition and trade-offs, linking local management with climate resilience. Future research should use manipulative experiments to test mechanisms and fitness trade-offs across host–symbiont combinations under varying disturbance regimes, quantify energetic and immune consequences, and incorporate multiple, symbiont-specific bleaching and recovery thresholds into predictive models. While targeted interventions may enhance survival, long-term persistence of reefs depends on rapid mitigation of greenhouse gas emissions.

- Observational natural experiment focused on two massive coral species at one atoll; generalizability to other taxa and regions may be limited. - Incomplete temporal and spatial coverage: not all sites were visited each season; some colonies were lost between surveys, yielding unknown outcomes; some samples failed sequencing. - qPCR-based symbiont density and identity time series were available primarily for Platygyra ryukyuensis, limiting direct quantitative corroboration for Favites pentagona. - Disturbance was quantified using proxies (population density within 2 km and fishing pressure), and while multiple environmental covariates were assessed, unmeasured factors could contribute. - Timing of within-heatwave recovery is inferred between discrete sampling points; exact onset of recovery likely preceded late-March 2016 sampling.