Air breathing and aquatic gas exchange during hypoxia in armoured catfish

Air breathing in fish is commonly believed to have arisen as an adaptation to aquatic hypoxia. The effectiveness of air breathing for tissue O₂ supply depends on the ability to avoid O₂ loss as oxygenated blood from the air-breathing organ passes through the gills. Here, we evaluated whether the armoured catfish (Hypostomus aff. pyreneusi)-a facultative air breather-can avoid branchial O₂ loss while air breathing in aquatic hypoxia, and we measured various other respiratory and metabolic traits important for O₂ supply and utilization. Fish were instrumented with opercular catheters to measure the O₂ tension (PO₂) of expired water, and air breathing and aquatic respiration were measured during progressive stepwise hypoxia in the water. Armoured catfish exhibited relatively low rates of O₂ consumption and gill ventilation, and gill ventilation increased in hypoxia due primarily to increases in ventilatory stroke volume. Armoured catfish began air breathing at a water PO₂ of 2.5 kPa, and both air-breathing frequency and hypoxia tolerance (as reflected by PO₂ at loss of equilibrium, LOE) was greater in individuals with a larger body mass. Branchial O₂ loss, as reflected by higher PO₂ in expired than in inspired water, was observed in a minority (4/11) of individuals as water PO₂ approached that at LOE. Armoured catfish also exhibited a gill morphology characterized by short filaments bearing short fused lamellae, large interlamellar cell masses, low surface area, and a thick epithelium that increased water-to-blood diffusion distance. Armoured catfish had a relatively low blood-O₂ binding affinity when sampled in normoxia (P₅₀ of 3.1 kPa at pH 7.4), but were able to rapidly increase binding affinity during progressive hypoxia exposure (to a P₅₀ of 1.8 kPa). Armoured catfish also had low activities of several metabolic enzymes in white muscle, liver, and brain. Therefore, low rates of metabolism and gill ventilation, and a reduction in branchial gas-exchange capacity, may help minimize branchial O₂ loss in armoured catfish while air breathing in aquatic hypoxia.