Contemporary ocean acidification and marine heatwaves shape individual energetics and rates of herbivory in a dominant ecosystem engineer.

Climate change can alter ecological interactions, including herbivory, and potentially alter thresholds for ecosystem collapse. Yet how multiple stressors and dynamic conditions (i.e., variability) shape these interactions remains unclear. This question is particularly pertinent in the coastal ocean, where factors such as ocean warming (OW) and acidification (OA) shape the physiology of dominant consumers, including sea urchins that can turn kelp forests into barrens. We experimentally quantified how present-day extreme conditions (including temperatures, temperature variability, and ocean acidification) affect herbivory and herbivore energetics of barren-forming purple sea urchins (Strongylocentrotus purpuratus). Metabolic and consumption rates nearly doubled across the range of currently experienced temperatures. When combined with present-day extreme OA conditions (pCO2 = 1200 μatm) sea urchins experienced a further doubling of both metabolic and consumption rates. Despite dramatic increases in consumption rates across these conditions, animals gained little to no growth or reproductive benefits. Energetic efficiency (i.e., growth and reproductive gains per unit energy consumed) declined substantially under contemporary warming, ocean acidification and variable temperature (i.e., El Niño-like dynamics). This acceleration in per capita grazing potential and shift in herbivore fitness has the potential to exacerbate effects of climate change but also may lead to unpredictable and volatile responses at the population and community level. Such results present a mechanistic warning for how extreme climatic events and multiple stressors, such as OA and OW, can drive when and where trophic interactions can lead to collapse of primary production ecosystems experiencing environmental change.