Award: OCE-1829623

Changing oxygen conditions are altering the physiology, behavior, and ecology of many marine animals. Many invertebrates undergo a planktonic larval stage, during which they have a deeper distribution during the day, and then ascend to the surface at night. The extent of these vertical distributions is primarily attributed to physiological tolerance and/or avoidance of visual predation. Those migrating in regions with eastern boundary currents, such as off the west coast of the United States near Southern California, are exposed to large gradients of both oxygen and irradiance with depth in the ocean, in addition to seasonal and inter-annual 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 very 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. Key Findings: 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. The temporal resolution (ability of the eye to distinguish among fast pulses of light stimuli) was impaired at 3.8 kPa in D. opalescens but not in P. planipes. Oxygen effects on retinal function occurred at much 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. To determine how physiological impairment of visual responses would affect visual behavior, we examined photobehavior (swimming response of larvae towards or away from light) in cephalopod larvae (D. opalescens and O. bimaculatus). We identified a robust, irradiance-dependent visual behavior, measured through the change in vertical position of larvae in an experimental chamber. The magnitude of the photobehavior was decreased as oxygen was reduced, and the response was entirely gone at <6.4 kPa partial pressure of oxygen (<74.7 mmol kg-1 at 15.3 ºC) in D. opalescens paralarvae. Oxygen also affected photobehavior in O. bimaculatus paralarvae. The mean vertical velocity of paralarvae was unaffected by exposure to reduced oxygen, indicating that oxygen deficits selectively affect vision prior to locomotion. We then determined how oxygen, which affects light sensitivity and generates limits for vision, might affect the distribution of animals that rely heavily on this sensory modality. We introduced the concept of a "visual luminoxyscape" to demonstrate how combinations of limiting oxygen and light could constrain the habitat of marine larvae with oxygen-demanding vision. Using the previously determined oxygen limits for visual physiology and behavior, and environmental data from the California Cooperative Oceanic Fisheries Investigations (CalCOFI) long-term oceanographic monitoring program, we calculated the visual luminoxyscape depth (below which visual and behavioral impairment would occur). The visual luminoxyscape depth (representing the lower limit of suitable visual habitat) has shoaled drastically in nearshore areas since 1986, possibly causing distributions of visual marine larvae to be impacted by oxygen and irradiance limits for visual function. The visual luminoxyscape depth is also affected by season (e.g., spring and summer upwelling), El Niño-Southern Oscillation phase, and proximity to shore. These results suggest that the visual luminoxyscape may be a more conservative measure for describing habitat suitability relative to oxygen than indices characterized by metabolic limitation. These oxygen tolerance trends can be used to inform the vulnerabilities of marine larvae to decreasing oxygen in the marine environment, and reveals the importance of considering sublethal oxygen thresholds in marine animals. The research produced during this project was presented at various national and international scientific conferences, in several public lectures for national and international audiences, during undergraduate and graduate courses, at international climate conferences (United Nations Climate Change Conference COP 25, 26, 27), and for K-12 students. Additionally, it was incorporated into an International Union for Conservation of Nature (IUCN) report, "Ocean deoxygenation: everyone's problem". It led to numerous publications, especially for students and early career researchers. It allowed for the mentorship of one doctoral student (with this research serving as their dissertation work) and their transition to a postdoctoral position, in addition to 6 undergraduates who all transitioned to graduate school. Last Modified: 12/16/2022 Submitted by: Lisa A Levin