Reviews and syntheses: Biological indicators of low-oxygen stress in marine water-breathing animals

Abstract

Anthropogenic warming and nutrient over-enrichment of our oceans have resulted in significant, and often catastrophic, reductions in dissolved oxygen (deoxygenation). Stress on water-breathing animals from this deoxygenation has been shown to occur at all levels of biological organization: cellular, organ, individual, species, population, community, and ecosystem. Most climate forecasts predict increases in ocean deoxygenation; thus, it is essential to develop reliable biological indicators of low-oxygen stress that can be used by regional and global oxygen monitoring efforts to detect and assess the impacts of deoxygenation on ocean life. This review focuses on responses to low-oxygen stress that are manifest at different levels of biological organization and at a variety of spatial and temporal scales. We compare particular attributes of these biological indicators to the dissolved oxygen threshold of response, timescales of response, sensitive life stages and taxa, and the ability to scale the response to oxygen stress across levels of organization. Where there is available evidence, we discuss the interactions of other biological and abiotic stressors on the biological indicators of low-oxygen stress. We address the utility, confounding effects, and implementation of the biological indicators of oxygen stress for research and societal applications. Our hope is that further refinement and dissemination of these oxygen stress indicators will provide more direct support for environmental managers, fisheries and mariculture scientists, conservation professionals, and policymakers to confront the challenges of ocean deoxygenation. An improved understanding of the sensitivity of different ocean species, communities, and ecosystems to low-oxygen stress will empower efforts to design monitoring programs, assess ecosystem health, develop management guidelines, track conditions, and detect low-oxygen events.