Changing climates are driving population declines in diverse animals worldwide. Winter conditions may play an important role in these declines but are often overlooked. Animals must not only survive winter but also preserve body condition, a key determinant of growing season success. We hypothesized that ectotherms overwintering in soil face a trade-off between risks of cold damage (including freezing) near the surface and elevated energy use at deeper depths. To test this hypothesis, we developed landscapes of mortality risk across depth for overwintering bumble bee queens. These critical pollinators are in decline in part because of climate change, but little is known about how climate affects overwintering mortality. We developed a mechanistic modeling approach combining measurements of freezing points and the temperature dependence of metabolic rates with soil temperatures from across the United States to estimate mortality risk across depth under historic conditions and under several climate change scenarios. Under current conditions, overwintering queens face a Goldilocks effect: temperatures can be too cold at shallow depths because of substantial freezing risk but too hot at deep depths where they risk prematurely exhausting lipid stores. Models suggest that increases in mean temperatures and in seasonal and daily temperature variation will increase risk of overwinter mortality. Better predictions of effects of changing climate on dormant ectotherms require more measurements of physiological responses to temperature during dormancy across diverse taxa.

Winter is a key driver of individual performance, community composition, and ecological interactions in terrestrial habitats. Although climate change research tends to focus on performance in the growing season, climate change is also modifying winter conditions rapidly. Changes to winter temperatures, the variability of winter conditions, and winter snow cover can interact to induce cold injury, alter energy and water balance, advance or retard phenology, and modify community interactions. Species vary in their susceptibility to these winter drivers, hampering efforts to predict biological responses to climate change. Existing frameworks for predicting the impacts of climate change do not incorporate the complexity of organismal responses to winter. Here, we synthesise organismal responses to winter climate change, and use this synthesis to build a framework to predict exposure and sensitivity to negative impacts. This framework can be used to estimate the vulnerability of species to winter climate change. We describe the importance of relationships between winter conditions and performance during the growing season in determining fitness, and demonstrate how summer and winter processes are linked. Incorporating winter into current models will require concerted effort from theoreticians and empiricists, and the expansion of current growing-season studies to incorporate winter.