Working underground: respiratory adaptations in the blind mole rat

Abstract

Mole rats (Spalax ehrenbergi superspecies) perform the heavy work of digging their subterranean burrows in Israel under highly hypoxic/hypercapnic conditions. Unlike most other mammals, they can achieve high levels of metabolic rate under these conditions, while their metabolic rate at low work rates is depressed. We explored, by comparing mole rats with white rats, whether and how this is related to adaptations in the design of the respiratory system, which determines the transfer of O2 from the lung to muscle mitochondria. At the same body mass, mole rats were found to have a significantly smaller total skeletal muscle mass than ordinary white rats (-22%). In contrast, the fractional volume of muscle mitochondria was larger by 46%. As a consequence, both species had the same total amount of mitochondria and achieved, under normoxia, the same V(O2max). Whereas the O2 transport capacity of the blood was not different, we found a larger capillary density (+31%) in the mole rat muscle, resulting in a reduced diffusion distance to mitochondria. The structural pulmonary diffusing capacity for O2 was greater in the mole rat (+44%), thus facilitating O2 uptake in hypoxia. We conclude that structural adaptations in lung and muscle tissue improve O2 diffusion conditions and serve to maintain high metabolic rates in hypoxia but have no consequences for achieving V(O2max) under normoxic conditions.

Figure 1

Rate of O₂ consumption as function of running speed in white rats (a) and mole rats (b). Solid symbols represent normoxic measurements (Fi_O2 = 21%), and the open symbols measurements represent hypoxia. Framed values of Fi_O2 represent the lowest sustainable O₂ concentration (critical P_O2). The regressions for the white rats are reported in the mole rat graph as a dashed line.

Figure 2

Morphometric properties of skeletal musculature for mole rats (hatched bars) and white rats (open bars). M_m/M_b, relative whole body skeletal muscle mass; V_V(mt,f), mitochondrial volume density; J_V(c,f), capillary length density; MYOGLOBIN, myoglobin concentrations for mole rat and white rat tissue; mt, mitochondrial; c, capillary; and f, muscle fibers. Data are reported as mean ± SEM. ∗, Significantly different vs. white rat, P < 0.05.

Figure 3

Morphometric properties relevant to oxygen supply in the heart for mole rats (hatched bars) and white rats (open bars). M_h, mass of the heart; V_V(mt,f), mitochondrial volume density; J_V(c,f), capillary length density; MYOGLOBIN, myoglobin content in heart muscle; mt, mitochondrial; c, capillary; and f, muscle fibers. Data are reported as mean ± SEM.

Figure 4

Summary of key parameters determining oxygen uptake in the lungs in mole rats (hatched bars) compared with white rats (open bars). V_L/M_b, lung volume related to body mass; S(a)/M_b, body mass-specific alveolar surface area; S(c)/M_b, capillary surface area relative to body mass; and Dl_O2/M_b, body mass-specific pulmonary diffusing capacity for oxygen. Data are reported as mean ± SEM. ∗, Significantly different vs. white rat, P < 0.05.