Fossorial Damaraland mole rats do not exhibit a blunted hypercapnic ventilatory response

Abstract

Damaraland mole rats (DMRs, Fukomys damarensis) are a eusocial fossorial species that spend the majority of their life in densely populated underground burrows, in which they likely experience intermittent periods of elevated CO₂ (i.e. hypercapnia). The primary physiological response to hypercapnia in most mammals is to increase depth and rate of breathing (i.e. hyperpnoea), but this response is often blunted in species that inhabit hypercapnic environments. In their natural habitat, DMRs putatively experience a gaseous environment ranging from normocapnic (0.1% CO₂) to hypercapnic (6.0% CO₂) conditions (Roper et al. 2001 J. Zool. 254, 101-107). As such, we hypothesized that DMRs would exhibit blunted hypercapnic ventilatory and metabolic responses, relative to those of non-fossorial rodent species. To test this hypothesis, we exposed awake, freely behaving DMRs to normoxic normocapnia (21% O₂, 0% CO₂, balance N₂) or graded normoxic hypercapnia (21% O₂, 0, 2, 5, 7 and 10% CO₂, balance N₂), and measured ventilation and metabolism using whole-body plethysmography and indirect calorimetry, respectively. We found that ventilation and metabolism were unchanged during prolonged normocapnia, whereas during graded hypercapnia, ventilation was elevated at 2% CO₂ and above. As a result, O₂ extraction efficiency at the lungs decreased with increasing hyperpnoea. Conversely, metabolic rate did not increase until 10% CO₂, presumably due to the metabolic cost of hyperpnoea. Taken together, our results suggest that despite their fossorial lifestyle, DMRs do not exhibit adaptations in their ventilatory or metabolic responses to environmental hypercapnia.

Keywords: hypercapnic metabolic response; hypercapnic ventilatory response; hyperpnoea.

Figure 1.

The Damaraland mole rat hypercapnic ventilatory response is not blunted. (a–c) Average minute ventilation (${\dot{V}}_{\mathrm{E}}$, a), breathing frequency (f_R; b), and tidal volume (V_T; c), were measured from Damaraland mole rats during either 5 h normocapnia (0% CO₂; black circles, solid lines), or 1-h consecutive step-wise increases in CO₂ concentration (0, 2, 5, 7 and 10%; open circles, dashed lines). All data are presented as mean ± s.e.m. from n = 9 Damaraland mole rats per group. Significance was assessed with a two-way repeated measures ANOVA. Asterisks (*) indicate a significant difference from the corresponding time point during normocapnic trials (p < 0.05).

Figure 2.

Damaraland mole rats offset hypercapnic hyperventilation with an increase in metabolic rate. (a–f) Average O₂ consumption ($\dot{V}{\mathrm{O}}_2$; a), average rate of CO₂ production ($\dot{V}\mathrm{C}{\mathrm{O}}_2$; b), air convection requirement of O₂ (ACR_VO2; c), air convection requirement of CO₂ (ACR_VCO2; d), respiratory exchange ratio (RER; e), and extraction efficiency of O₂ (eO₂; f) were measured from Damaraland mole rats during either 5 h normocapnia (0% CO₂; black circles, solid lines), or 1-h consecutive step-wise increases in CO₂ concentration (0, 2, 5, 7 and 10%; open circles, dashed lines). Due to equipment limitations, $\dot{V}\mathrm{C}{\mathrm{O}}_2$, RER, and ACR_VCO2 data were not collected during the 10% CO₂ stage. All data are presented as mean ± s.e.m. from n = 9 Damaraland mole rats per group. Significance was assessed with a two-way repeated measures ANOVA. Asterisks (*) indicate a significant difference from the corresponding time point during normocapnic trials (p < 0.05).