'Active' regulation of cutaneous gas exchange by capillary recruitment in amphibians: experimental evidence and a revised model for skin respiration.

Oxygen uptake, carbon dioxide elimination, cutaneous and systemic blood flows (measured by microsphere technique) and the number of perfused capillaries in the hind foot web have been measured at 25 degrees C in unanaesthetized bullfrogs (Rana catesbeiana) both while breathing air as they float in water and while resting totally out of water in humidified air. The gas exchange ratio, approximately 1 while breathing with both water and air, fell to 0.5 or lower during 4 h of complete air exposure. A concomitant decrease occurred in both cutaneous blood flow and the proportion of perfused to non-perfused capillaries in the hind foot web. Upon returning to floating at the water surface, cutaneous blood flow and capillary recruitment increased again and the gas exchange ratio increased to above 2 for several hours. These data suggest that a partial inhibition of CO2 excretion is linked with a decrease in the extent and pattern of blood flow through the skin, which is the major site of CO2 elimination. Conventional models for cutaneous CO2 elimination in amphibians reveal major diffusion limitations but minor, even insignificant, perfusion limitations. Consequently, CO2 elimination is regarded as highly responsive to changes in blood PCO2, but nearly insensitive to changes in blood flow. Importantly, however, such models have treated the skin as a single blood compartment (i.e., single 'capillary'), through which blood flow is varied. We propose a multi-capillary model which incorporates changes in capillary recruitment, and thus changes in the surface area across which CO2 elimination from the blood can occur. In such a model, changes in the number of perfused capillaries cause major changes in CO2 elimination. Experimental data on CO2 elimination agrees well with predicted changes using this new multi-capillary model.