Anatomical adaptations for peripheral oxygen transport at high and low temperatures

Abstract

On acute cold exposure most animals show a reduction in cardiac output and increased blood viscosity that may seriously impair oxygen supply to peripheral tissue. The apparent increase in capillarisation in response to chronic low temperature may be accompanied by significant muscle atrophy in hibernating mammals, and a rise in capillary density (CD) may then simply reflect a reduced fibre diameter. When hamsters were exposed to reduced temperature and photoperiod, capillary to fibre ratio (C:F) of the tibialis anterior muscle was unchanged (at 2.7) and CD increased by 30% (to 1538 mm⁻²) following a similar decrease in fibre size. A measure of local C:F decreased around glycolytic fibres, but increased around both oxidative fibre types. When corrected for changes in fibre size, local CD increased around all fibre types in the cold. Fishes are particularly sensitive to fluctuations in environmental temperature, but in contrast to mammals often maintain activity and undergo muscle hypertrophy. Slow (aerobic) muscle from striped bass and goldfish held for eight weeks at seasonal extremes of 5 and 25°C had a higher C:F in cold vs. warm animals. However, increased fibre size meant that the functional capacity of the microcirculation was maintained rather than increased. Seasonal acclimatisation of trout induced an inverse relationship between environmental temperature and C:F, increasing 40% from summer (18°C) to winter (4°C). However, extensive hypertrophy at 4°C meant that the size of the capillary bed was maximal at 11°C, corresponding to the point of highest muscle blood flow and greatest scope for aerobic swimming, reflecting an optimised aerobic performance at intermediate temperatures. The consequence of altered fibre composition and capillarisation is calculated as an increase in mean fibre PO₂ from 1.9 to 4.6 kPa, and in minimum PO₂ from 0.6 to 4.2 kPa in 25° v. 5°C-acclimated striped bass, respectively. However, the most dramatic effect on intracellular oxygenation results from an altered capillary supply with the capillary supply becoming increasingly inadequate at high temperatures.