Stressed Overwintering Bottleneck Hypothesis: Ocean warming and acidification synergistically disrupt Arctic zooplankton overwintering

Ocean warming (OW), driven by the influx of warm Atlantic water masses, and acidification (OA) are threatening Arctic marine ecosystems. However, their potential synergistic effects are poorly understood, especially during the Polar Night when marine species are particularly vulnerable to stressors. Here, we tested our novel Stressed Overwintering Bottleneck Hypothesis (SOBH): warming will disrupt the overwintering of the keystone pan-Arctic copepod Calanus glacialis, a pivotal secondary producer, by impairing fitness-related traits underpinning survival and reproduction. We exposed C. glacialis to current and projected future OW levels (0 °C and 4 °C) and OA levels (pH 8.0 and 7.4-7.3) for 53 days during the mid-Arctic Polar Night. We assessed survival, development, and physiological and molecular mechanisms (oxygen consumption, lipid depletion, the expression of nine targeted genes related to oxidative stress and damage repair, and DNA damage). OW alone did not affect C. glacialis mortality; however, OA increased copepod survival at 0 °C. Notably, their combined effects (OWA) synergistically doubled mortality, as predicted by SOBH. Warming also accelerated moulting from copepodite stage V to adulthood in December, and increased respiration, exhausted lipid reserves entirely by early March, approximately one to four months before the spring algal bloom, further supporting SOBH. DNA damage and gene expression patterns indicated low investment in maintenance and damage repair. Collectively, these findings reveal hidden mechanisms by which OW and OA synergistically threaten overwintering Calanus copepods by drastically increasing mortality, accelerating moulting, raising metabolic rates, and causing early lipid depletion. These effects generate cross-seasonal phenological mismatches among overwintering survival, energy reserves, reproduction, and primary production. Such stressed overwintering bottlenecks in foundational secondary producers like Calanus copepods provide novel explanations for how OW and OA can constrict Arctic marine food webs. At a broader perspective, SOBH highlights how multiple stressors induced overwintering disruption could reshape pan-Arctic and global biodiversity.