Separating the contributions of vascular anatomy and blood viscosity to peripheral resistance and the physiological implications of interspecific resistance variation in amphibians

Abstract

Amphibian pulmonary and systemic vascular circuits are arranged in parallel, with potentially important consequences for resistance (R) to blood flow. The contribution of the parallel anatomic arrangement to total vascular R (R T), independent of blood viscosity, is unknown. We measured pulmonary (R P) and systemic (R S) vascular R with an in situ Ringer's solution perfusion technique using anesthetized anuran and urodele species to determine: (1) relative contributions of vascular anatomy and blood viscosity to R T; (2) distensibility index (%Δ flow kPa(-1)) of the pulmonary and systemic vascular circuits; and (3) interspecific correlates of variation in these parameters with red blood cell size, cardiac power output, and aerobic capacities. R P was lower than R S in anurans, while R P of the urodeles was greater than R S and significantly greater than anuran R P. Anuran R T was lowest and did not vary interspecifically, whereas urodele R T was significantly greater than anuran, and varied interspecifically. Pulmonary and systemic circuit distensibility differences may explain cardiac shunt patterns in toads with changes in cardiac output from rest to activity. When blood viscosity was taken into account, vascular resistance accounted for about 25 % of R T while blood viscosity accounted for the remaining 75 %. Owing to lower R T, terrestrial anuran species required lower cardiac power outputs when moving fluid through their vasculature compared to aquatic species. These results indicate that physical characteristics of the vasculature can account for interspecific differences in cardiovascular physiology and suggest a co-evolution of cardiac and vascular anatomy among amphibians.

Net cardiac shunts in anuran amphibians: physiology or physics?

“…In our recent study (Kohl et al, 2013), we measured the passive physical characteristics of the vascular circuits for cane toads, Rhinella marina (Linnaeus 1758) (formerly Bufo marinus). The effect of variation in flow rate on the input pressure and conductances was quantified in situ for the pulmonary and systemic vasculature in anesthetized, cranially pithed toads that eliminated autonomic regulation of the vasculature.…”

“…There are three studies that report in vivo data describing net cardiac shunt flow in R. marina, and we have re-analysed the data from these studies in light of the passive physical characteristics of the pulmonary and systemic vascular circuits described in our 2013 study (Kohl et al, 2013). Hedrick et al quantified in vivo variation in Q pul and Q sys at rest and during exercise at temperatures ranging from 10 to 30°C.…”

“…This protocol eliminated the possibility of direct autonomic regulation of tonus on the vasculature either through direct innervation or via humoral agents. Our analysis compares in vivo data for net cardiac shunts in cane toads from the literature with the results of our previous study (Kohl et al, 2013).…”

“…In particular, regulation of pulmonary conductance by vagal (parasympathetic) innervation of the pulmonary artery has received considerable attention (West and Burggren, 1984;Gamperl et al, 1999). The second entails the passive properties of the vascular beds to perfusion pressures resulting from variation in cardiac output (West and Smits, 1994;Kohl et al, 2013). In this case, the physical characteristics of the systemic and respiratory vascular beds determine the conductance of, and flow through, each circuit.…”

“…We suggest that differences in Q pul and Q sys are not sufficient to define direct autonomic regulation of the net cardiac shunt in amphibians unless it can be demonstrated that the differences are distinct from the physical characteristics of the indirect passive pressure-mediated effects on conductance in the two circuits. Our recent study examined the in situ physical characteristics of the pulmonary and systemic circuits in a variety of amphibians that were anesthetized and cranially pithed and perfused with only Ringers solution (Kohl et al, 2013). This protocol eliminated the possibility of direct autonomic regulation of tonus on the vasculature either through direct innervation or via humoral agents.…”