Marginal coral communities increasingly experience intense winter cooling events, yet the extent to which heterotrophic feeding enhances cold-stress resilience, bleaching threshold and defines the threshold of thermal compensation remains poorly resolved. Here, we conducted a long-term mesocosm experiment using three cold-tolerant coral species, Dipsastraea speciosa, Duncanopsammia peltata, and Cyphastrea serailia, originated from the thermally extreme marginal reefs of Dongshan Bay, southern China. We demonstrated that marginal reef corals withstand prolonged winter cooling through metabolic suppression rather than energetic collapse, maintaining a positive autotrophic carbon balance (CZAR > 100%) after two months at 7–10 °C below ambient conditions. Symbionts exhibited greater metabolic impairment than the coral host, identifying them as the primary site of cold-induced stress. Cold bleaching disrupted PSII activity, reduced rETR and Fv/Fm, increased excitation pressure and NPQ, and caused severe symbiont loss and tissue paling. Heterotrophic feeding enhanced cold tolerance under moderate cooling (15 °C; CHAR +23 to -9 %), but this compensatory pathway collapsed under extreme cold stress (12 °C; CHAR -96%), forcing near complete autotrophic dependence despite symbiont losses of up to 93%. The persistence of autotrophic carbon fixation under severe symbiont depletion suggesting compensatory holobiont carbon cycling, likely supported by microbial primary production, distinct from heat bleaching. Feeding increased cold-bleaching thresholds in D. peltata and C. serailia, but not in D. speciosa, indicating species-specific nutritional dependence likely linked to symbiont genotype. However, heterotrophic buffering failed under extreme cold, highlighting metabolic suppression as a key survival strategy and suggesting potential shift coral communities toward intrinsically cold-tolerant species.
 

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