Reduced quality and synchronous collapse of forage species disrupts trophic transfer during a prolonged marine heatwave

Abstract

The Gulf of Alaska forage fish community includes a few key species that differ markedly in their timing of spawning, somatic growth and lipid storage, and in their migration behavior. This diversity in life history strategies facilitates resilience in marine food webs because it buffers predators against the naturally high variance in abundance of pelagic forage fish populations by decreasing the likelihood that all species will be scarce at the same time. During the prolonged North Pacific marine heatwave of 2014-2016, the availability and quality of at least three key forage species with different life history strategies were reduced simultaneously in the system. Capelin and sand lance occurrence in predator diets declined abruptly, and Prince William Sound herring spawning biomass declined to historically low levels. Biomass of euphausiids was also reduced, in part due to the loss of a cold-water species. Changes in age structure, growth, and energy content of capelin, sand lance, and herring were also associated with warming during the heatwave, but not all species responded in the same way. For example, spawning capelin grew faster and matured at a younger age but were shorter in length than usual, while sand lance in Prince William Sound experienced anomalously low growth rates and lipid storage in 2015-2016. Changes in forage fish populations had immediate impacts on predator populations in 2015-2016, when seabirds and marine mammals experienced shifts in distribution, mass mortality, and reproductive failures in the Gulf of Alaska. In contrast, copepod abundance increased on the shelf and in some coastal regions during the heatwave, suggesting that food availability was not a primary factor limiting forage fish populations at this time. The reduced quality and collapse of multiple forage fish populations reduced the efficiency of energy transfer through the middle trophic level of pelagic food webs, disrupting energy flow to piscivorous pelagic predators and causing abrupt and extreme reductions in their numbers and productivity.