Understanding ventilation and oxygen uptake of Pacific hagfish (Eptatretus stoutii), with particular emphasis on responses to ammonia and interactions with other respiratory gases

Abstract

The hagfishes are an ancient and evolutionarily important group, with breathing mechanisms and gills very different from those of other fishes. Hagfish inhale through a single nostril via a velum pump, and exhale through multiple separate gill pouches. We assessed respiratory performance in E. stoutii (31 ppt, 12 ºC, 50–120 g) by measuring total ventilatory flow ($\dot{\text V}\text{w}$) at the nostril, velar (respiratory) frequency (fr), and inspired (P_IO₂) and expired (P_EO₂) oxygen tensions at all 12 gill pouch exits plus the pharyngo-cutaneous duct (PCD) on the left side, and calculated ventilatory stroke volume (S$\dot{\text V}\text{w}$), % O₂ utilization, and oxygen consumption (ṀO₂). At rest under normoxia, spontaneous changes in $\dot{\text V}\text{w}$ ranged from apnea to > 400 ml kg⁻¹ min⁻¹, due to variations in both fr and S$\dot{\text V}\text{w}$; “normal” $\dot{\text V}\text{w}$ averaged 137 ml kg⁻¹ min⁻¹, ṀO₂ was 718 µmol kg⁻¹ h⁻¹, so the ventilatory convection requirement for O₂ was about 11 L mmol⁻¹. Relative to anterior gill pouches, lower P_EO₂ values (i.e. higher utilization) occurred in the more posterior pouches and PCD. Overall, O₂ utilization was 34% and did not change during hyperventilation but increased to > 90% during hypoventilation. Environmental hypoxia (P_IO₂ ~ 8% air saturation, 1.67 kPa, 13 Torr) caused hyperventilation, but neither acute hyperoxia (P_IO₂ ~ 275% air saturation, 57.6 kPa, 430 Torr) nor hypercapnia (P_ICO₂ ~ 1% CO₂, 1.0 kPa, 7.5 Torr) significantly altered $\dot{\text V}\text{w}$. ṀO₂ decreased in hypoxia and increased in hyperoxia but did not change in hypercapnia. Acute exposure to high environmental ammonia (HEA, 10 mM NH₄HCO₃) caused an acute decrease in $\dot{\text V}\text{w}$, in contrast to the hyperventilation of long-term HEA exposure described in a previous study. The hypoventilatory response to HEA still occurred during hypoxia and hyperoxia, but was blunted during hypercapnia. Under all treatments, ṀO₂ increased with increases in $\dot{\text V}\text{w}$. Overall, there were lower convection requirements for O₂ during hyperoxia, higher requirements during hypoxia and hypercapnia, but unchanged requirements during HEA. We conclude that this “primitive” fish operates a flexible respiratory system with considerable reserve capacity.