Diel oxygen fluctuation drives the thermal response and metabolic performance of coastal marine ectotherms

Abstract

Coastal marine systems are characterized by high levels of primary production that result in diel oxygen fluctuations from undersaturation to supersaturation. Constant normoxia, or 100% oxygen saturation, is therefore rare. Since the thermal sensitivity of invertebrates is directly linked to oxygen availability, we hypothesized that (i) the metabolic response of coastal marine invertebrates would be more sensitive to thermal stress when exposed to oxygen supersaturation rather than 100% oxygen saturation and (ii) natural diel fluctuation in oxygen availability rather than constant 100% oxygen saturation is a main driver of the thermal response. We tested the effects of oxygen regime on the metabolic rate, and haemocyanin and lactate levels, of velvet crabs ( Necora puber ) and blue mussels ( Mytilus edulis ), under rising temperatures (up to 24°C) in the laboratory. Oxygen supersaturation and photosynthetically induced diel oxygen fluctuation amplified animal metabolic thermal response significantly in both species, demonstrating that the natural variability of oxygen in coastal environments can provide considerable physiological benefits under ocean warming. Our study highlights the significance of integrating ecologically relevant oxygen variability into experimental assessments of animal physiology and thermal response, and predictions of metabolic performance under climate warming. Given the escalating intensity and frequency of climate anomalies, oxygen variation caused by coastal vegetation will likely become increasingly important in mitigating the effects of higher temperatures on coastal fauna.

The relationship between size and metabolic rate of juvenile crown of thorns starfish

“…Studies of whole‐body metabolic rate are used to understand how physiological performance adjusts to changes in environmental conditions and the capacity of organisms to cope with stress (Monaco et al, 2014; Propp et al, 1983; Wilson et al, 2013). Metabolic response data are used to model organism resilience and vulnerability to changing environmental conditions such as food levels, oxygen availability, and salinity, as well as ocean acidification and warming (Agüera & Byrne, 2018; Booth et al, 2021; Christensen et al, 2011; Harianto et al, 2018; McGaw & Twitchit, 2012; Peck et al, 2008). Change in the metabolism of organisms as they grow has important implications for food webs and trophic dynamics (Brown et al, 2004).…”

Experimental hyperoxia (O 2 supersaturation) reveals a gill diffusion limitation of maximum aerobic performance in fish

“…Increasingly, naturally occurring hyperoxia is being touted as an environmental phenomenon that can improve the resilience of aquatic ectotherms, including fish, to extreme heat waves associated with climate change [4,26,27]. Moreover, there is growing interest in using hyperoxia as an experimental tool to examine whether O 2 capacity limitations set constraints on whole animal performance in fish facing environmental warming [4,28].…”

“…The severe blood acidosis following exhaustive exercise in fish and potentially associated reductions in HbO 2 binding affinity due to Root and Bohr effects [6], for example, could amplify the extent to which hyperoxia increases M ̇O2max . Increasingly, naturally occurring hyperoxia is being touted as an environmental phenomenon that can improve the resilience of aquatic ectotherms, including fish, to extreme heat waves associated with climate change [4,26,27]. Moreover, there is growing interest in using hyperoxia as an experimental tool to examine whether O 2 capacity limitations set constraints on whole animal performance in fish facing environmental warming [4,28].…”

Editorial: Fluctuating Habitats: Ecological Relevance of Environmental Variability and Predictability on Species, Communities, and Ecosystems

“…Although most of the models of species adaptation consider the biological response to one or few relevant environmental factors, such as temperature in climate change models, there are growing evidences that the cumulative effect of the variability of abiotic factors has to be considered. For instance, fluctuating conditions can mitigate the net impact of the corresponding stressor, increasing physiological tolerance and promoting adaptation to novel environmental conditions at all biological levels (Booth et al, 2021;Fusi et al, 2021). For microorganisms, in addition to spatial patterns, environmental fluctuations can determine localized spatial jackpot events that ensure persistence of strains across environmental dynamic conditions (Ciccarese et al, 2022).…”