Neurometabolic rewiring in squid (Sepioteuthis lessoniana) optic lobes drives behavioral plasticity and visual integration under environmental acidification

Abstract

Ocean acidification's impacts on marine animal behavior have substantial implications for ecosystem stability. Understanding how key predators respond to acidification is crucial for predicting future ocean food web dynamics, yet the underlying neural mechanisms remain poorly understood. Here, we show that prolonged exposure to projected year 2100 acidification conditions substantially impairs predatory behavior in bigfin reef squid (Sepioteuthis lessoniana), a key invertebrate predator. Chronic acidification exposure reduces expression of acetylcholine receptors in optic lobes and alters systemic HCO3- levels and metabolic rates. Using custom electroretinogram recordings, we find that while basic visual processing remains intact, behavioral impairments likely stem from changes in downstream neural integration pathways. Transcriptomic expression analysis reveals broad reductions in energy metabolism and synaptic signaling under acute exposure, while chronic exposure induces compensatory upregulation of cellular maintenance pathways. Our findings demonstrate that while squids maintain visual capabilities through adaptive mechanisms, the energy-intensive processes of neural integration and behavioral execution are compromised. These results highlight the complex physiological trade-offs marine predators face under ocean acidification, with implications for understanding future shifts in marine ecosystem structure and function.