Episodic ventilation lowers the efficiency of pulmonary CO₂excretion

Abstract

The ventilation pattern of many ectothermic vertebrates, as well as hibernating and diving endotherms, is episodic where breaths are clustered in bouts interspersed among apneas of varying duration. Using mechanically ventilated, anesthetized freshwater turtles (Trachemys scripta), a species that normally exhibits this episodic ventilation pattern, we investigated whether episodic ventilation affects pulmonary gas exchange compared with evenly spaced breaths. In two separate series of experiments (a noninvasive and an invasive), ventilation pattern was switched from a steady state, with evenly spaced breaths, to episodic ventilation while maintaining overall minute ventilation (30 ml·min(-1)·kg(-1)). On switching to an episodic ventilation pattern of 10 clustered breaths, mean CO2 excretion rate was reduced by 6 ± 5% (noninvasive protocol) or 20 ± 8% (invasive protocol) in the first ventilation pattern cycle, along with a reduction in the respiratory exchange ratio. O2 uptake was either not affected or increased in the first ventilation pattern cycle, while neither heart rate nor overall pulmonary blood flow was significantly affected by the ventilation patterns. The results confirm that, for a given minute ventilation, episodic ventilation is intrinsically less efficient for CO2 excretion, thereby indicating an increase in the total bodily CO2 store in the protocol. Despite the apparent CO2 retention, mean arterial Pco2 only increased 1 Torr during the episodic ventilation pattern, which was concomitant with a possible reduction of respiratory quotient. This would indicate a shift in metabolism such that less CO2 is produced when the efficiency of excretion is reduced.

The Evolution of Unidirectional Pulmonary Airflow

“…Minimizing the number of breaths needed for washout could facilitate crypsis, reduce the overall energetic cost of ventilation, lower rates of respiratory evaporative water loss, and lower rates of cooling due to the heat of vaporization. Unidirectional flow may furthermore be important to ectotherms because episodic ventilation decreases the efficiency of CO 2 excretion, independent of changes in cardiac output (52). During periods of apnea, CO 2 is primarily stored in the tissues and must be rapidly delivered to the lung during short periods of ventilation.…”

Effects of overground locomotor training on the ventilatory response to volitional treadmill walking in individuals with incomplete spinal cord injury: a pilot study

“…12 Phase II is characterized by an exponential rise toward steady-state ventilation, and is often determined by a time constant of~60-70 s. 12,13 Phase III begins at steady-state ventilation when there is no further rise in the V E during CWR exercise below the anaerobic threshold, and is typically achieved by the 4th minute of CWR exercise. 12 In contrast to healthy individuals, impaired pulmonary function contributes to discrepancies in matching internal and external respiration, 14 leading to blood gas abnormalities 15,16 and potentially resulting in subsequent peripheral muscle fatigue. 17,18 In individuals with SCI, altered pulmonary mechanics 19,20 and alveolar hypoventilation 14 have been observed; however, the degree to which our current understanding of a phasic model of exercise hyperpnea can be applied to individuals with iSCI is unknown.…”

Effects of environmental hypoxia and hypercarbia on ventilation and gas exchange in Testudines

“…Vitalis & Milsom (1986a) consider episodic breathing an adaptive mechanism that decreases the energetic cost of ventilation in ectotherms, and Randall et al (1981) consider such a breathing behavior advantageous for aquatic species, since it reduces the energetic cost to surface and also reduces the exposure time at the surface, possibly lessening risks of predation. Since episodic breathing with long non-ventilatory periods leads to a significant change in arterial blood gases, decreasing P a O 2 and pH and increasing P a CO 2 ( Glass, Burggren & Johansen, 1978 ), as well as decreasing the efficiency of pulmonary CO 2 excretion ( Malte, Malte & Wang, 2013 ), it should be more advantageous for a terrestrial species to ventilate regularly and thereby maintain homeostasis of arterial blood gases. It is therefore interesting to ask why the terrestrial C. carbonarius employs episodic breathing under normoxic conditions, thereby possibly increasing variation in arterial blood gases instead of maintaining a regular breathing pattern, such as seen in this species only under severe levels of hypoxia or hypercarbia ( Fig.…”