Linking environmental salinity to respiratory phenotypes and metabolic rate in fishes: a data mining and modelling approach

The gill is the primary site of ionoregulation and gas exchange in adult teleost fishes. However, those characteristics that benefit diffusive gas exchange (large, thin gills) may also enhance the passive equilibration of ions and water that threaten osmotic homeostasis. Our literature review revealed that gill surface area and thickness were similar in freshwater (FW) and seawater (SW) species; however, the diffusive oxygen (O-2) conductance (G(d)) of the gill was lower in FW species. While a lower G(d) may reduce ion losses, it also limits O-2 uptake capacity and possibly aerobic performance in situations of high O-2 demand (e.g. exercise) or low O-2 availability (e.g. environmental hypoxia). We also found that FW fishes had significantly higher haemoglobin (Hb)-O-2 binding affinities than SW species, which will increase the O-2 diffusion gradient across the gills. Therefore, we hypothesized that the higher Hb-O-2 affinity of FW fishes compensates, in part, for their lower G(d). Using a combined literature review and modelling approach, our results show that a higher Hb-2 affinity in FW fishes increases the flux of O-2 across their low-G d gills. In addition, FW and SW teleosts can achieve similar maximal rates of O-2 consumption ((M) over dot(O2,max)) and hypoxia tolerance (P-crit) through different combinations of Hb-O-2 affinity and G(d). Our combined data identified novel patterns in gill and Hb characteristics between FW and SW fishes and our modelling approach provides mechanistic insight into the relationship between aerobic performance and species distribution ranges, generating novel hypotheses at the intersection of cardiorespiratory and ionoregulatory fish physiology.

Automated summary

The gill is the primary site of ionoregulation and gas exchange in adult teleost fishes. Differences in gill characteristics and hemoglobin-O2 affinities between freshwater (FW) and seawater (SW) species affect oxygen diffusion and ion regulation, with FW fishes compensating for lower diffusive oxygen conductance with higher hemoglobin-O2 affinity. Both FW and SW teleosts can achieve similar maximal rates of oxygen consumption and hypoxia tolerance through different combinations of hemoglobin-O2 affinity and diffusive oxygen conductance. The relationship between aerobic performance and species distribution ranges is influenced by these factors, leading to novel hypotheses in fish physiology.