Food limitation erodes the thermal tolerance of larvae in an ecologically influential marine herbivore.

Biologists often use organismal thermal tolerance to help explain or forecast responses of populations to climate change. Yet many studies quantify thermal tolerance under isolated laboratory conditions despite extreme events, such as heatwaves, often coinciding with other stressors such as nutrient or food limitation. These oversights may be consequential as recent theory suggests thermal tolerance itself can be fundamentally altered by food limitation. Here, we experimentally test how food limitation (500-10,000 cells mL-1) affects long-term survival, development, and growth across a present-day range of temperatures (10-20°C) in the most sensitive life stages of an important marine herbivore, purple sea urchins (Strongylocentrotus purpuratus). We show food limitation substantially erodes thermal tolerance in terms of survival, but when provided ample food, larvae exhibited robust survival across temperatures currently experienced by larvae in nature. Reductions in food however lowered optimal survival temperatures and shifted survival thresholds to those conditions observed during recent marine heatwaves. These results are consistent with the "metabolic meltdown" hypothesis-shifting optima and upper limits to cooler temperatures-and illustrate how present-day warming coupled with lower productivity may lead to substantial, unexpected declines in larval survival and recruitment. In contrast to survival, developmental rates and time to metamorphic competency, which ranged from 21 to 61 days, were driven largely by temperature with little impact of food concentration. Our findings relate to historical observations of declines in larval supply at the southern edge of the species range. Overall, these results have broad-reaching implications beyond sea urchin populations as sea urchin herbivory is known to control productivity of kelp forest communities. We provide evidence of how laboratory derived thermal reaction norms can be coupled with ecologically relevant food concentrations to inform unexpected vital rate declines of sensitive life stages in a changing climate.