The Role of Vascular and Interstitial Compliance and Vascular Volume in the Regulation of Blood Volume in Two Species of Anuran

Abstract

The objectives of this study were (1) to measure plasma (V(p)), blood (V(b)), extracellular (V(e)), and interstitial fluid (V(ist)) volumes using the same techniques; (2) to measure the rate of plasma turnover; and (3) to characterize the three important variables required to interpret transvascular flux at an organismal level (vascular compliance [C(vas)], interstitial compliance [C(ist)], and the whole-body transvascular filtration coefficient [F(c)]) in two species of anurans that differ in their capacity to regulate blood volume during dehydrational and hemorrhagic stress. The disappearance curve of Evans blue-labeled native plasma protein fitted a two-component exponential decay model for both species, indicating that plasma proteins exchanged quickly between two kinetically distinct compartments, V(p) and V(e). V(p) calculated using serial sampling times <10 min were 61.0 mL kg(-1) for Chaunus marinus and 40.5 mL kg(-1) for Lithobates catesbeiana. Plasma turnover rate was 3% of V(p) min(-1) (1.8 mL min(-1) kg(-1)) for C. marinus and 5.5% of V(p) min(-1) (2.2 mL min(-1) kg(-1)) for L. catesbeiana. Chaunus marinus also had significantly greater V(b) (84 to 53 mL kg(-1)), V(ist) (171 to 154 mL kg(-1)), and V(e) (232 to 195 mL kg(-1)) than L. catesbeiana. C(vas) was significantly greater in C. marinus (47.3 mL kPa(-1) kg(-1)) compared with L. catesbeiana (27.7 mL kPa(-1) kg(-1)). This difference reflects the interspecific differences in V(b) because vascular distensibilities are similar (0.5% kPa(-1)). There were no interspecific differences in the C(ist) (500 mL kPa(-1) kg(-1)) or F(c) (2.5 mL kg(-1) kPa(-1) min(-1) filtration calculation; 0.2-0.5 mL kPa(-1) kg(-1) min(-1) fit to volume change data). Functionally, these circulatory/interstitial exchange variables of both anuran species exemplify a circulatory system with high rates of filtration (lymph formation) and with no capacity for transcapillary fluid uptake, hence requiring substantial lymphatic return to maintain vascular volume. The large C(ist) of both species provides a capacity to store extravascular volume with little perturbation of vascular pressure, but the resulting low interstitial pressures would create difficulties for extravascular fluid return to the dorsally located lymph hearts. The principal interspecific differences of greater V(b), V(p), V(ist), and C(vas) for the more terrestrial species, C. marinus, would stabilize cardiac function during hypovolemia (e.g., hemorrhage) and increase resistance to dehydration. This is consistent with this species' enhanced capacity to manage dehydrational and hemorrhagic challenges to blood volume regulation compared to L. catesbeiana.