Dissolved Oxygen in Heterogeneous Environments Dictates the Metabolic Rate and Thermal Sensitivity of a Tropical Aquatic Crab

Abstract

Oxygen availability, together with water temperature, greatly varies in coastal habitats, especially in those characterized by elevated primary production. In this study, we investigate the combined role of dissolved oxygen and temperature on the thermal physiological response of the mud crab Thalamita crenata living in an equatorial system of coastal habitats. We sampled temperature, oxygen and salinity in T. crenata habitats, mangrove creeks and fringes and seagrass meadows, at Gazi Bay (Kenya). We found that seagrass meadows exhibited higher temperature and oxygen saturation than the mangrove habitats during the day, creating conditions of oxygen supersaturation. By investigating the effect of different levels of oxygen saturation on the thermal response of T. crenata, we demonstrated that the respiratory physiology of this ectotherm has a pronounced resistance to heat, directly influenced by the amount of dissolved oxygen in the water. Under low oxygen saturation levels, the mud crab significantly reduced its metabolism, becoming temperature-independent. This result shows that aquatic species can modulate their thermal response in a stringent dependency with water oxygen saturation, corroborating previous findings on the thermal response of T. crenata under supersaturation. This contribution provides further support for the need to adopt an ecologically-relevant approach to forecast the effect of climate change on marine ectothermal species.

Ideas and perspectives: The fluctuating nature of oxygen shapes the ecology of aquatic habitats and their biogeochemical cycles – the aquatic oxyscape

“…However, unexpected oxygen profiles have also been reported in several specific habitats and at different timescales, suggesting that different abiotic and biotic drivers modulate oxygen dynamics (Craig and Hayward, 1983). For instance, the alternation of oxygen biological production and consumption determines a massive fluctuation in oxygen availability in highly productive aquatic habitats, such as mangrove forests, salt marshes, coral reefs (Giomi et al, 2019;Fusi et al, 2021;Booth et al, 2021), kelp forests (Krause-Jensen et al, 2016), plankton blooms in pelagic systems (Riser and Johnson, 2008;Benoiston et al, 2017), freshwater lakes (Andersen et al, 2017), or even agricultural drainage channels (Booth et al, 2023a). The seasonal variation in diel oxygen fluctuations is increasingly reported at all latitudes and habitats, and it occurs in a vast range of water bodies independently of the scale, the hydrological features, and the local biotic components (Fig.…”

Ideas and perspectives. The fluctuating nature of oxygen shapes the ecology of aquatic habitats and their biogeochemical cycles: the aquatic oxyscape

“…However, unexpected oxygen profiles have also been reported in several specific habitats and at different time scales suggesting that different abiotic and biotic drivers modulate oxygen dynamics (Craig and Hayward, 1983). For instance, the alternation of oxygen biological production and consumption determines massive fluctuation of its availability in highly productive aquatic habitats, such as mangrove forests, salt marshes, coral reefs (Giomi et al, 2019;Fusi et al, 2021;Booth et al, 2021), kelp forests (Krause-Jensen et al, 2016), plankton blooms in the open oceans (Riser and Johnson, 2008;Benoiston et al, 2017), freshwater lakes (Andersen et al, 2017) or even in agricultural drainage channels (Booth et al, 2023). Stochastic variation of oxygen availability principally depends upon abiotic factors and may determine extensive conditions of uneven oxygenation on small and large spatial and temporal scales.…”

“…Hyperoxia benefits the metabolic performance of fishes and invertebrates, especially under acute warming that may be very intense in tidal ponds or shallow coastal habitats (Fusi et al, 2021;Booth et al, 2021;Giomi et al, 2019;McArley et al, 2020;Booth et al, 2023). It extends the upper thermal tolerance of aquatic animals during acute events of daily warming and their survival to anomalous heat waves (McArley et al, 2022).…”

“…Within the current trend of climate change, the beneficial effect of hyperoxia against extreme heating events can have underestimated positive consequences on the survival of the animals. For instance, an important consequence of exposure to the hyperoxic conditions experienced during the daytime under high heating regimes is the enhanced capability to extract oxygen from the poorly oxygenated water during the night and endure hypoxic or even anoxic periods (Giomi et al, 2019;Booth et al, 2021).…”

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).…”