Winter metabolic compensation endangers woodland salamanders under climate change

Understanding the mechanisms that shape species geographic distributions is essential for predicting responses to climate change, particularly under winter conditions, which are warming more rapidly than summer conditions in many temperate ecosystems. Woodland salamanders, which constitute many of the species in the global hotspot of salamander diversity located in the southern Appalachian Mountains of North America, are thought to cope with harsh winters through dormancy and metabolic suppression. We used a field-based experiment to investigate the winter physiology and energetics of a woodland salamander (Plethodon metcalfi). Despite showing histological signs of dormancy, salamanders exhibited higher metabolic rates during winter than the active season when measured at low temperatures associated with winter, consistent with metabolic compensation. High-elevation salamanders also exhibited elevated metabolic rates at cold temperatures compared to low-elevation salamanders, indicative of countergradient metabolic compensation. When integrated into a biophysical species distribution model, depletion of energy stores estimated from winter metabolic rates under current climates accurately predicted the geographic range limits of our focal species. Under future warming scenarios, incorporating winter physiology indicated that 77% of the species range would experience local extinction due to depletion of energy stores. These findings challenge assumptions about winter energetics, reveal metabolic limits on cold-season survival, and highlight metabolic demands during dormancy as a key constraint on responses to climate change.