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On the temperature-dependence of hæmoglobin-oxygenation and blood-oxygen transport in regionally heterothermic teleosts and sharks

University of British Columbia

Hæmoglobin (Hb)-O2 affinity in most vertebrates typically decreases with increasing blood temperature because the oxygenation enthalpy (ΔH') is usually exothermic. However, in regionally heterothermic fishes, such as tunas and some sharks, ΔH' is commonly low or even endothermic, causing a very reduced or reversed effect of temperature on Hb-O₂ affinity. Regionally heterothermic fishes conserve metabolic heat with vascular heat exchangers that prevent circulatory heat loss and establish internal temperature gradients. My objective was to investigate the functional significance of reduced and reverse temperature-dependent Hb-O₂ affinity in regionally heterothermic fishes. I hypothesized that temperature-independent Hb-O₂ affinity conserves heat energy and matches O₂ supply to O₂ demand despite large internal temperature gradients, so I expected this trait to be shared by all regionally heterothermic fishes. I investigated this by (1) examining the effect of temperature on Hb-O₂ affinity in three regionally heterothermic species whose Hb has not been well studied (swordfish, opah, and common thresher shark), and (2) mathematical modelling of O₂ transport to quantitatively assess the relative contributions of Hb concentration and Hb-O₂ affinity to O₂ and heat transport. I found that opah Hb-O₂ affinity is temperature-independent, the temperature-dependence of swordfish Hb-O₂ affinity is pH dependent, becoming temperature-independent at low pH, and common thresher shark Hb-O₂ affinity is temperature-independent. I also found that Hb from bigeye thresher shark, a suspected regional heterotherm, is temperature-independent below 50% Hb-O₂ saturation. Using a mathematical model of O₂ transport I demonstrated that Hb concentration and Hb-O₂ affinity are relatively more important than other factors of O₂ transport in determining maximum O₂ consumption in yellowfin tuna, a regional heterotherm with a iv “high-energy demand.” I also showed that Hb with a reversed temperature-dependence diminishes temperature induced changes to blood O₂ tension and prevents Hb-heat loss, as much as 13% of metabolic heat production. These results provide insight into the functional significance of reduced and reversed temperature-dependent Hb-O₂ affinity in regionally heterothermic fishes. All known lineages of regionally heterothermic fishes have Hb with a low ΔH', and increases to ΔH' have convergently evolved by different molecular mechanisms with underlying dependence on different allosteric effectors.

Text

2020-12-16

Attribution-NonCommercial-NoDerivatives 4.0 International

http://hdl.handle.net/2429/76826

Zoology

University of British Columbia

UBCV

http://creativecommons.org/licenses/by-nc-nd/4.0/