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.

Improved cardiac filling facilitates the postprandial elevation of stroke volume inPython regius

“…The V b determined for both fasting and digesting pythons resemble the 4-7% of body mass previously reported for other species of snakes and other terrestrial vertebrates (Hillman et al, 2010;Lillywhite and Smith, 1981;Lillywhite and Smits, 1984;Smits and Lillywhite, 1985;Thorson, 1968). We determined V b in awake snakes, while our haemodynamic measurements were performed with anaesthetized animals.…”

“…However, given the short duration of the experimental protocol during anaesthesia and the sessile nature of the awake snakes during V b measurements, V b is unlikely to have been altered before the initial measurements of MCFP and blood flows were concluded (Lillywhite and Smith, 1981;Lillywhite and Smits, 1984). Some studies incubate EB with native plasma before injection to ensure binding to plasma proteins and alleviate wash-out from the capillaries (Hillman et al, 2010), whereas we and others injected EB directly into the circulation (Baustian, 1988;Thorson, 1964), which could overestimate the calculated V b . However, the V b of 3% in our study is lower than previous measurements in other snake species (Lillywhite and Smits, 1984).…”

Posterior lymph heart function in two species of anurans: analysis based on both in vivo pressure–volume relationships by conductance manometry and ultrasound

“…All lymph flow must pass through the four lymph hearts, so the combined output is the total lymphatic flow. Recent estimates indicate that flow for all four lymph hearts ranges from 0.9 to 5mlkg -1 min -1 (Baustian, 1988;Baldwin et al, 1993;Malvin et al, 1995;Jones et al, 1997;Hillman et al, 2010). The magnitude of this flux is remarkable when compared with mammalian values of 0.083mlkg -1 min -1 in adult sheep (Brace and Power, 1981).…”

“…One hypothesis to explain differential tolerance to dehydration is that anurans have differing abilities to compensate for low blood volume and maintain systemic oxygen transport during dehydration. Blood volumes are greater and better maintained in dehydration-tolerant species (Shoemaker, 1964;Hillman, 1978;Hillman, 1980;Hillman et al, 1987;Hillman and Withers, 1988;Hillman et al, 2010), supporting differential ability to maintain blood volume as a potential mechanism for differential dehydration tolerance. Interstitial fluid can replace dehydrational plasma volume loss in terrestrial species.…”

“…Interstitial fluid can replace dehydrational plasma volume loss in terrestrial species. The mobilization of this fluid reserve into the cardiovascular system is dependent upon a functioning lymphatic system (Zwemer and Foglia, 1943;Baustian, 1988) and appears to be independent of Starling Law-based transcapillary fluid mobilizing mechanisms in anurans Hillman et al, 2010).…”