Oxygen dependence of visual physiology and behavior in marine invertebrate larvae and its ecological implications

Many invertebrates undergo a planktonic larval stage, during which they have a deeper distribution during the day (to 80 m), and then ascend to the surface at night. Those migrating in regions with eastern boundary currents, such as the Southern California Bight, are exposed to large gradients of both oxygen and irradiance with depth in the ocean, in addition to seasonal variability. Marine larvae of visual species rely on sophisticated eyes for prey capture, predator avoidance, and vertical migration; this vision is very oxygen demanding. The critical early life stages of marine invertebrates can be vulnerable to changes in ocean conditions, and stress from oxygen loss could compromise optimal visual function, fitness, and survival. This research evaluated the effects of reduced oxygen partial pressure (pO2) on visual physiology, metabolism, and visual behavior in larvae of animals with “fast” vision, including cephalopods and arthropods, and the potential consequences for their distributions in the ocean. A decrease in pO2 from 21 kPa (surface ocean pO2) to ~ 3 kPa caused retinal function to decline by 60-100% in larvae of the market squid Doryteuthis opalescens, the two-spot octopus Octopus bimaculatus, the graceful rock crab Metacarcinus gracilis, and the tuna crab Pleuroncodes planipes. Temporal resolution was impaired at 3.8 kPa in D. opalescens but not in P. planipes. Oxygen effects on retinal function occurred at higher pO2 (22, 11.5 kPa) than the critical oxygen limit for metabolism (Pcrit) (2.47, 0.48 kPa) for D. opalescens and O. bimaculatus, respectively, indicating visual effects are dissociated from general metabolic decline. Phototaxis behavior decreased with exposure to pO2 that would cause 50% retinal function in the cephalopod larvae. To define available visual habitat for these larvae (the critical luminoxyscape), oxygen and light conditions were measured over various temporal and spatial scales using a custom-built sensor package deployed at 30 m depth in 2015-2017, and from hydrographic profiles taken between 1999 and 2017 in the Southern California Bight (CalCOFI). Oxygen and light during the seasonal upwelling periods and in the nearshore environment reached levels that alter visual function of these species. Future effects of ocean deoxygenation may manifest as impaired larval vision