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

Abstract

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 (P crit ) 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 P crit 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.

Genomic analysis of hypoxia inducible factor alpha in ray-finned fishes reveals missing Ohnologs and evidence of widespread positive selection

“…The current results present several opportunities for future research on HIFA in fishes. For example, tolerance to hypoxia measured at the organismal level demonstrates a strong phylogenetic signal among ray-finned fishes 72 , and future research could assess whether hypoxia-tolerant lineages are associated with the specific amino acid variants in HIFα subunits reported here. Furthermore, in fishes as in other vertebrates, HIF1A has received considerably more attention than the other HIFA paralogs.…”

The role of cell size in shaping responses to oxygen and temperature in fruit flies

“…However, while small cells have a better capacity for oxygen uptake, the higher energetic costs to maintain their electrochemical gradients are a disadvantage as more energy is required to maintain the electrochemical gradients across cellular membranes (Czarnołęski et al, 2013(Czarnołęski et al, , 2015(Czarnołęski et al, , 2018Gupta et al, 1978;Kozłowski et al, 2003;Szarski, 1970Szarski, , 1983. Therefore, cell size reflects a balance between the energetic costs and the benefits for oxygen diffusion and the optimal cell size is therefore likely to be temperature dependent (Hermaniuk et al, 2021;Verberk et al, 2022;Walczyńska et al, 2015). We observed that cell size category (small, medium and Normoxia (21 kPa) large) across our six isolines modulated the effects of temperature and oxygen.…”

“…Evidence for oxygen constraints related to heat stress is stronger for aquatic ectotherms than for terrestrial ectotherms (Leiva et al, 2019;Verberk et al, 2016), likely because of the difficulties involved: water holds less oxygen, impedes oxygen diffusion and because of the higher density and viscosity of water compared to air, it takes more energy to move water across respiratory organs such as gills (Dejours, 1981;Schmidt-Nielsen, 1997). There is also evidence that whether larger animals are more prone to oxygen limitation differs between air and water breathers (Harrison et al, 2018;Verberk et al, 2022). In air breathers, larger organisms rely to a larger extent on air convection for oxygen transport, rather than air diffusion, making them less prone to oxygen limitation (Greenlee et al, 2007).…”

Systemic orchestration of cell size throughout the body: influence of sex and rapamycin exposure in Drosophila melanogaster

“…There is also direct evidence that changes in cell size are a component of plasticityand evolutionary-related changes in adult size [7,19,21,[25][26][27][28]. Undoubtedly, the number and size of the cells that make up an organism have consequences for organismal performance [29][30][31][32][33], but it is unclear whether the cellular structure of tissues is systemically organized throughout the metazoan body or whether it is arranged locally to suit tissue-specific functions. A clear answer to this fundamental question is unavailable largely because previous studies have rarely focused on cell-size variance among organisms and even then have tended to target single cell types [10,21,[34][35][36][37].…”