Neurometabolic rewiring in optic lobes of squid drives behavioral plasticity and visual integration under environmental acidification

Ocean acidification's impacts on marine animal behavior have significant implications for ecosystem stability. We demonstrate that prolonged exposure to the projected year 2100 acidification conditions significantly impairs predatory behavior in bigfin reef squid (Sepioteuthis lessoniana), a key invertebrate predator. Chronic exposure resulted in reduced acetylcholine receptor expression in optic lobes, coupled with altered hemolymph HCO3- levels and metabolic rates. Using a custom electroretinogram (ERG) recording method, we found that while basic visual processing remained intact, behavioral impairments likely stem from changes in downstream neural pathways. Transcriptomic analysis revealed broad reductions in energy metabolism and synaptic activities under acute exposure, while chronic exposure induced compensatory upregulation of cellular maintenance pathways. Our findings suggest that while squids maintain visual capabilities through adaptive mechanisms, the energy-intensive processes of neural integration and behavioral execution are compromised, highlighting the complex physiological trade-offs marine predators face under ocean acidification.