Reduced Oxygen Impairs Photobehavior in Marine Invertebrate Larvae.

AbstractOrganisms in coastal waters experience naturally high oxygen variability and steep oxygen gradients with depth, in addition to ocean deoxygenation. They often undergo diel vertical migration involving a change in irradiance that initiates a visual behavior. Retinal function has been shown to be highly sensitive to oxygen loss; here we assess whether visual behavior (photobehavior) in paralarvae of the squid Doryteuthis opalescens and the octopus Octopus bimaculatus is affected by low oxygen conditions, using a novel behavioral paradigm. Larvae showed an irradiance-dependent, descending photobehavior after extinction of the light stimulus, measured through the change in vertical position of larvae in the chamber. The magnitude of photobehavior was decreased as oxygen was reduced, and the response was entirely gone at <6.4 kPa partial pressure of oxygen (<74.7 µmol kg-1 at 15.3 °C) 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. These findings suggest that variable and declining oxygen conditions in coastal upwelling areas and elsewhere will impair photobehavior and likely affect the distribution, migration behavior, and survival of highly visual marine species.

Integrative Approaches to Understanding Organismal Responses to Aquatic Deoxygenation.

AbstractOxygen bioavailability is declining in aquatic systems worldwide as a result of climate change and other anthropogenic stressors. For aquatic organisms, the consequences are poorly known but are likely to reflect both direct effects of declining oxygen bioavailability and interactions between oxygen and other stressors, including two-warming and acidification-that have received substantial attention in recent decades and that typically accompany oxygen changes. Drawing on the collected papers in this symposium volume ("An Oxygen Perspective on Climate Change"), we outline the causes and consequences of declining oxygen bioavailability. First, we discuss the scope of natural and predicted anthropogenic changes in aquatic oxygen levels. Although modern organisms are the result of long evolutionary histories during which they were exposed to natural oxygen regimes, anthropogenic change is now exposing them to more extreme conditions and novel combinations of low oxygen with other stressors. Second, we identify behavioral and physiological mechanisms that underlie the interactive effects of oxygen with other stressors, and we assess the range of potential organismal responses to oxygen limitation that occur across levels of biological organization and over multiple timescales. We argue that metabolism and energetics provide a powerful and unifying framework for understanding organism-oxygen interactions. Third, we conclude by outlining a set of approaches for maximizing the effectiveness of future work, including focusing on long-term experiments using biologically realistic variation in experimental factors and taking truly cross-disciplinary and integrative approaches to understanding and predicting future effects.

First known observations of brooding, development, and hatching of fertilized eggs for the North Pacific bigeye octopus, Octopus californicus.

The North Pacific bigeye octopus, Octopus californicus (Berry, 1911) is a cold-water, deep-sea octopod. Little is known about their biology due to difficulty accessing their natural habitat and obtaining live specimens. Although they are a frequent bycatch product in commercial bottom trawl fisheries, individuals of this species have rarely been raised in captivity and their embryonic development has not yet been documented. Considering these limitations, we were fortunate to have witnessed this process leading to successful hatching in an aquarium setting. Here, we present a brief observational account of the first-known record of brooding, development, and hatching of fertilized eggs for O. californicus. The incubation time was a maximum of 10 months at a temperature between 8-10°C and embryos hatched over a period of 2.5 months. While more detailed research is needed, this preliminary information contributes to our limited knowledge of this species and supports life history theories of prolonged embryonic development under colder temperatures.

Vision is highly sensitive to oxygen availability in marine invertebrate larvae.

For many animals, evolution has selected for complex visual systems despite the high energetic demands associated with maintaining eyes and their processing structures. Therefore, the metabolic demands of visual systems make them highly sensitive to fluctuations in available oxygen. In the marine environment, oxygen changes over daily, seasonal and inter-annual time scales, and there are large gradients of oxygen with depth. Vision is linked to survival in many marine animals, particularly among the crustaceans, cephalopods and fish, and early life stages of these groups rely on vision for prey capture, predator detection and their distribution in the water column. Using in vivo electroretinogram recordings, we show that there is a decrease in retinal sensitivity to light in marine invertebrates when exposed to reduced oxygen availability. We found a 60-100% reduction in retinal responses in the larvae of cephalopods and crustaceans: the market squid (Doryteuthis opalescens), the two-spot octopus (Octopus bimaculatus), the tuna crab (Pleuroncodes planipes) and the graceful rock crab (Metacarcinus gracilis). A decline in oxygen also decreases the temporal resolution of vision in D. opalescens These results are the first demonstration that vision in marine invertebrates is highly sensitive to oxygen availability and that the thresholds for visual impairment from reduced oxygen are species-specific. Oxygen-impaired retinal function may change the visual behaviors crucial to survival in these marine larvae. These findings may impact our understanding of species' vulnerability to ocean oxygen loss and suggest that researchers conducting electrophysiology experiments should monitor oxygen levels, as even small changes in oxygen may affect the results.

Physiological and ecological implications of ocean deoxygenation for vision in marine organisms.

Climate change has induced ocean deoxygenation and exacerbated eutrophication-driven hypoxia in recent decades, affecting the physiology, behaviour and ecology of marine organisms. The high oxygen demand of visual tissues and the known inhibitory effects of hypoxia on human vision raise the questions if and how ocean deoxygenation alters vision in marine organisms. This is particularly important given the rapid loss of oxygen and strong vertical gradients in oxygen concentration in many areas of the ocean. This review evaluates the potential effects of low oxygen (hypoxia) on visual function in marine animals and their implications for marine biota under current and future ocean deoxygenation based on evidence from terrestrial and a few marine organisms. Evolutionary history shows radiation of eye designs during a period of increasing ocean oxygenation. Physiological effects of hypoxia on photoreceptor function and light sensitivity, in combination with morphological changes that may occur throughout ontogeny, have the potential to alter visual behaviour and, subsequently, the ecology of marine organisms, particularly for fish, cephalopods and arthropods with 'fast' vision. Visual responses to hypoxia, including greater light requirements, offer an alternative hypothesis for observed habitat compression and shoaling vertical distributions in visual marine species subject to ocean deoxygenation, which merits further investigation.This article is part of the themed issue 'Ocean ventilation and deoxygenation in a warming world'.

Effects of dispersant and oil on survival and swimming activity in a marine copepod.

Knowledge of lethal and sublethal effects of crude oil and dispersants on mesozooplankton are important to understanding ecosystem impacts of oil spills in marine environments. Here we (1) establish median lethal concentrations for water accommodated fractions of Corexit EC9500A dispersant, MC-252 crude oil (WAF), and dispersed crude oil (CEWAF) for the coastal copepod Labidocera aestiva, and (2) assess acute effects on L. aestiva swimming activity. Mortality assays with L. aestiva support that copepods are more sensitive than other zooplankton taxa to dispersant toxicity, while WAF and CEWAF are generally similar in their toxicity to this copepod species and other zooplankton. Acute effects on L. aestiva activity included impaired swimming upon WAF and CEWAF exposure. These results highlight that copepods are particularly sensitive to dispersant exposure, with acute effects on survival most evident with dispersant alone, and on swimming behavior when dispersant is mixed with crude oil.

Pupil light reflex in the Atlantic brief squid, Lolliguncula brevis.

Coleoid behavioral ecology is highly visual and requires an eye capable of forming images in a variety of photic conditions. A variable pupil aperture is one feature that contributes to this visual flexibility in most coleoids, although pupil responses have yet to be quantitatively documented for squid. The pupil light reflex (PLR) of the Atlantic brief squid, Lolliguncula brevis, was analyzed by directly exposing one eye of individual squid to light stimuli of varying irradiance and imaging the reflex, while simultaneously recording from the opposite, indirectly stimulated eye to determine whether the constriction was consensual between eyes. A PLR was measured in L. brevis, with an asymmetrical constriction observed under increasing irradiance levels that was not consensual between eyes, although a response of some level was observed in both eyes. Response thresholds ranged between 12.56 and 12.66 log photons cm(-2) s(-1). The PLR was rapid and dependent upon the stimulus irradiance, achieving half-maximum constriction within 0.49-1.2 s. The spectral responsivity of the PLR was analyzed by measuring the magnitude of the reflex in the eye directly stimulated by light of equal quantal intensity at wavelengths from 410 to 632 nm. The responsivity curve showed a maximum at 500 nm, indicating the eye is especially well suited for vision at twilight. These results, when considered in the context of the ambient light characteristics, show that the PLR of L. brevis contributes to a dynamic visual system capable of adjusting to the highly variable composition of light in its estuarine habitat.