Anuran amphibians as comparative models for understanding extreme dehydration tolerance: A unique negative feedback lymphatic mechanism for blood volume regulation

Abstract

Anurans are the most terrestrial order of amphibians. Couple the high driving forces for evaporative loss in terrestrial environments and their low resistance to evaporation, dehydration is an inevitable stress on their water balance. Anurans have the greatest tolerances for dehydration of any vertebrate group. Some species can tolerate evaporative losses up to 45% of their standard body mass. Anurans have remarkable capacities to regulate blood volume with hemorrhage and dehydration compared with mammals. Stabilization of blood volume is central to extending dehydration tolerance, since it avoids both the hypovolemic and hyperviscosity stresses on cardiac output and its consequential effects on aerobic capacity. Anurans, in contrast to mammals, seem incapable of generating a sufficient pressure difference, either oncotically or via interstitial compliance, to move fluid from the interstitium into the capillaries. Couple this inability to generate a sufficient pressure difference for transvascular uptake to a circulatory system with high filtration coefficients and a high rate of plasma turnover is the consequence. The novel lymphatic system of anurans is critical to a remarkable capacity for blood volume regulation. This review summarizes what is known about the anatomical and physiological specializations that are involved in explaining differential blood volume regulation and dehydration tolerance involving a true centrally mediated negative feedback of lymphatic function involving baroreceptors as sensors and lymph hearts, arginine vasotocin, pulmonary ventilation and specialized skeletal muscles as effectors.