Ventilation in Amia calva : a comparison with water-breathing fish
Creators: name: McKenzie, David J.
Publisher: name: University of British Columbia
Year: 2011

description: Aspects of ventilation and ventilatory control were investigated in an air-breathing fish, Amia calva, to determine the extent to which Amia is similar to water-breathing fish. The possibility that Amia uses the air-breathing organ to maintain gas-exchange during periods of aestivation was tested. During gradual air-exposure, Amia showed no reduction in oxygen consumption, no increase in plasma urea levels or in urea excretion. Arterial blood pH (pHa) remained constant, and arterial plasma total carbon dioxide (TaCO₂) and carbon dioxide partial pressure (PaCO₂) increased. Arterial plasma total ammonia (Tamm) and NH₃ concentrations rose significantly. Exposure to elevated total ammonia concentrations in the water did not elicit an increase in urea production or air-breathing. Aquatic hypoxia without access to air did not cause a reduction in aerobic metabolism and moderate levels were fatal. These results indicate that Amia are incapable of aestivation, due to an inability to reduce metabolism and detoxify ammonia to urea, and die following three to five days of air-exposure. The air-breathing organ is used to maintain aerobic metabolism under aquatic conditions of hypoxia or raised temperature. The characteristics of air-breathing and gill ventilatory responses to internal acid-base disturbances were investigated in Amia. Acid infusions lowered pHa and arterial blood oxygen content (CaO₂), raised PaCO₂, and stimulated air-breathing and gill ventilation. Ammonium bicarbonate infusions did not change pHa or CaO₂, raised PaCO₂, and did not stimulate any ventilatory responses. Acid infusions during aquatic hyperoxia lowered pHa and raised PaCO₂. Arterial blood O₂ content declined but remained above normoxic levels. There were no ventilatory responses. These results indicate that air-breathing and gill ventilation responses in Amia are most closely correlated with blood O₂ status, not pHa or PaCO₂. Air-breathing and gill ventilation responses following acid infusion were associated with a release of catecholamines into circulation. Catecholamine infusion stimulated gill ventilation but not air-breathing in Amia, suggesting that endogenous catecholamine release may have mediated gill ventilatory responses to hypoxaemia. These ventilatory reflex responses to acid-base disturbance, and the correlation between gill ventilation responses and catecholamine release are similar to observations made on water-breathing fish. Ventilatory responses to increases in TaCO₂ and Tamm were investigated in rainbow trout, and compared with responses by Amia. In trout, infusion of NaHCO₃ raised pHa and TaCO₂, did not change PaCO₂ or CaO₂, and stimulated ventilation. Infusion of NH₄HCO₃ did not change pHa or CaO₂, raised TaCO₂, PaCO₂ and Tamm, and stimulated ventilation. Infusion of NH₄Cl lowered pHa, raised Tamm, and stimulated ventilation. Infusion of HCl lowered pHa, TaCO₂ and CaO₂, and stimulated ventilation. Infusion of NaOH raised pHa but did not stimulate ventilation until twenty minutes post-infusion. Infusion of NaCl had little or no effect on pHa, CaO₂, TaCO₂ or Tamm, and no effect on ventilation. These results indicate that trout show a ventilatory response to increases in TaCO₂, increases in Tamm and decreases in pHa and CaO₂, but not to increases in pHa. Following HCl and NaHCO₃ infusion, there was a significant increase in the level of circulating catecholamines, indicating that the ventilatory responses to reductions in pHa and CaO₂ and increases in TaCO₂ may be Immorally mediated by catecholamine release. The ventilatory responses to increases in Tamm were not associated with a catecholamine release. Unlike trout, Amia do not show a ventilatory response to infusion of NH₄HCO₃, i.e. to increases in TaCO₂ and Tamm. Sites and afferent pathways for ventilatory reflex responses to blood and water O₂ status were determined in Amia. Air-breathing and gill ventilatory reflex responses to hypoxia, sodium cyanide (NaCN), hypoxaemia and catecholamines were investigated in intact Amia, and compared with responses in animals following section of branchial branches of cranial nerves IX and X, and extirpation of the pseudobranch. In intact, sham-operated animals, hypoxia stimulated an increase in air-breathing and gill ventilation. Following denervation, the air-breathing response was abolished, and the gill ventilation response significantly attenuated. In sham-operated animals, NaCN in the water flowing over the gills stimulated air-breathing and gill ventilation, and NaCN given in the dorsal aorta stimulated gill ventilation. These responses were abolished following denervation. In intact animals, HC1 infusion stimulated air-breathing and gill ventilation, but following denervation, the air-breathing response was abolished. The ventilatory response to catecholamines was significantly attenuated in denervated animals as compared with shams. These results indicate that air-breathing and gill ventilation reflex responses are controlled by oxygen-sensitive receptors in the gills and pseudobranch, innervated by cranial nerves VII, IX and X. These sites and afferent pathways are similar to receptors controlling hypoxic reflex responses in water-breathing fish. The effects of catecholamines on gill ventilation are mainly exerted via stimulation of receptors in the gills, which are separate from those controlling air-breathing. The gill ventilatory responses to hypoxia, hypoxaemia and acidosis following denervation may be mediated by central effects of circulating catecholamines, or by an extrabranchial oxygen or pH receptor. In conclusion, Amia is an entirely aquatic animal with the primary ventilatory control mechanisms of water-breathing fish intact, but with the added ability to breathe air at the surface.