An analysis of the transport and interaction of oxygen and carbon dioxide in fish
Creators: name: Brauner, Colin J.
Publisher: name: University of British Columbia
Year: 2009

description: Many teleost fish haemoglobins (Hbs) exhibit a Root effect, a large Haldane effect and a low buffer capacity. This combination of characteristics influences the interaction between movements of oxygen (O₂) and carbon dioxide (CO₂) in the red cell, in the respiratory epithelium, and in the tissues. For example in rainbow trout, oxygenation of the blood at constant Pco₂ in vitro, induces a large acidosis (0.21 pH units) in the red cell. This acidosis results from the release of a large number of protons during Hb oxygenation (Haldane effect) in the presence of a Hb with a low buffer capacity. It can be hypothesized, that oxygen uptake in the absence of CO₂ removal, could limit oxygen binding to Hb at the gills by as much as 50% due to the presence of the Root effect (where an acidosis reduces blood oxygen carrying capacity). Arapaima gigas is an obligate air breathing teleost fish from the Amazon. It possesses two respiratory surfaces for gas exchange: gills and a highly vascularized swimbladder which acts as an air-breathing organ (ABO). The movements of O₂ and CO₂ are spatially uncoupled in normoxia. That is, 78 % of the O₂ consumed was from the air and 85 % of the CO₂ excreted was into the water. Therefore, a large proportion of the oxygen uptake across the ABO occurred in the absence of CO₂ removal. The Hb in this species possessed a large Root effect and therefore, an acidosis induced by Hb oxygenation in the absence of CO₂ removal, could impair O₂ uptake as hypothesized above in rainbow trout. The Haldane effect in this Hb, however, was small preventing an acidosis during Hb oxygenation. Interestingly, the Hb buffer capacity was also low relative to that in rainbow trout, seemingly maladaptive for CO₂ excretion. Thus, Hb characteristics appear to be modified to prevent impairment of O₂ uptake in the absence of CO₂ removal in A. gigas; however, the effect of these changes on CO₂ excretion is less clear. A quantitative analysis of O₂ and CO₂ transport was conducted in resting and exercising rainbow trout, and these data were used to quantify the magnitude of coupling between O₂ and CO₂ exchange, in vivo. In resting rainbow trout exposed to normoxia and two levels of hypoxia, or in fish during sustained exercise, 60% of the total CO₂ excreted was dependent upon HCO₃⁻/Cl⁻ exchange during red cell transit through the gills. This is of significance to CO₂ excretion because HCO₃⁻/Cl⁻ exchange is thought to be the rate limiting step. In both arterial and mixed-venous blood of trout, an acid-base disequilibrium was observed in resting fish exposed to normoxia and two levels of hypoxia, indicating that the blood pH and Pco₂ probably never reach equilibrium in vivo. However, inclusion of the acid-base disequlibrium in an analysis of partitioning of CO₂ excretion, did not result in a significant difference from a similar analysis using steady state values. Oxygenation of whole blood from trout resulted in a non-linear release of protons (Bohr protons) over the Hb-O₂ equilibrium curve in vitro. That is, the majority of Bohr protons were released between 60 and 100% of Hb oxygen saturation (So₂). Rapid oxygenation of the blood over this region of the Hb-O₂ equilibrium curve elevated the HCO₃⁻ flux rate across the HCO₃⁻/Cl⁻ exchanger on the red cell by about 30% during CO₂ excretion in vitro. Oxygenation of the Hb between 0 and 60% So₂ did not elevate CO₂ excretion rate in vitro. The non-linear release of Bohr protons over the Hb-O₂ equilibrium curve was also observed in vivo, in trout subjected to different levels of sustained exercise. At low swimming speeds, when venous blood O₂ content (C[sub v]o2) was high, there was a small acidosis as blood passed through the gills, indicating more protons were released during oxygenation of Hb than were consumed during HCCy dehydration. At higher swimming speeds, when C[sub v]o2) was low, there was a significant alkalosis in the arterial blood relative to the venous blood, indicating fewer protons were released upon oxygenation than HCCy ions were dehydrated to CO₂. Haldane coefficients (moles of protons released per mole of O₂ which binds to Hb), calculated from steady state arterial and mixed-venous parameters, revealed that under resting conditions 100% of CO₂ excreted was stoichiometrically related to O₂ uptake through the release of Bohr protons during Hb oxygenation. The magnitude of coupling between CO₂ excretion and O₂ uptake decreased from 100% to less than 50% at the maximal swimming velocity when the largest region of the Hb-O₂ equilibrium curve was used for gas exchange. The non-linear release of Bohr protons over the range of Hb-O₂ saturation in the blood limits HCO₃⁻ dehydration at the gills during greater work loads, conserving the HCO₃⁻ buffer capacity of the blood and tissues.