Body mass and cell size shape the tolerance of fishes to low oxygen in a temperature‐dependent manner

• Published in: Global change biology Vol. 28; no. 19; pp. 5695 - 5707
• Main Authors: Verberk, Wilco C. E. P., Sandker, Jeroen F., Pol, Iris L. E., Urbina, Mauricio A., Wilson, Rod W., McKenzie, David J., Leiva, Félix P.
• Format: Journal Article
• Language: English
• Published: Oxford Blackwell Publishing Ltd 01.10.2022; Wiley
• Subjects: Aquatic habitats; ATP; Biodiversity and Ecology; Body mass; Body size; Body temperature; Boundary layers; Cell size; climate change; Dissolved oxygen; Divergence; Energy budget; Energy metabolism; Environmental Sciences; Fish; Freshwater; Freshwater environments; Freshwater fish; Freshwater fishes; genome size; Gills; Global Changes; Hypoxia; Inland water environment; marine; Marine fish; Mass; Metabolic rate; metabolic scaling; Metabolism; Oxygen; Oxygen consumption; Oxygen requirement; Oxygen uptake; Phylogenetics; Phylogeny; Temperature; Temperature dependence; Temperature requirements; Temperature tolerance; Thickness; Uptake; Viscosity
• DOI: 10.1111/gcb.16319
• ISSN: 1354-1013

Aerobic metabolism generates 15–20 times more energy (ATP) than anaerobic metabolism, which is crucial in maintaining energy budgets in animals, fueling metabolism, activity, growth and reproduction. For ectothermic water‐breathers such as fishes, low dissolved oxygen may limit oxygen uptake and hence aerobic metabolism. Here, we assess, within a phylogenetic context, how abiotic and biotic drivers explain the variation in hypoxia tolerance observed in fishes. To do so, we assembled a database of hypoxia tolerance, measured as critical oxygen tensions (Pcrit) for 195 fish species. Overall, we found that hypoxia tolerance has a clear phylogenetic signal and is further modulated by temperature, body mass, cell size, salinity and metabolic rate. Marine fishes were more susceptible to hypoxia than freshwater fishes. This pattern is consistent with greater fluctuations in oxygen and temperature in freshwater habitats. Fishes with higher oxygen requirements (e.g. a high metabolic rate relative to body mass) also were more susceptible to hypoxia. We also found evidence that hypoxia and warming can act synergistically, as hypoxia tolerance was generally lower in warmer waters. However, we found significant interactions between temperature and the body and cell size of a fish. Constraints in oxygen uptake related to cellular surface area to volume ratios and effects of viscosity on the thickness of the boundary layers enveloping the gills could explain these thermal dependencies. The lower hypoxia tolerance in warmer waters was particularly pronounced for fishes with larger bodies and larger cell sizes. Previous studies have found a wide diversity in the direction and strength of relationships between Pcrit and body mass. By including interactions with temperature, our study may help resolve these divergent findings, explaining the size dependency of hypoxia tolerance in fish. Whether fish can tolerate low levels of dissolved oxygen is shown here to depend on characteristics of both the fish (body mass, genome size and metabolism) and the water (temperature and salinity). These effects did not act in isolation: In warmer waters, small fishes with small genomes were more tolerant than large fishes with large genomes. We also observed a greater tolerance in freshwater fishes, compared to marine fishes. These findings can help to (i) resolve the scientific debate about oxygen limitation and (ii) predict the impacts of climate change on global fish populations and fisheries.