Pulmonary-type surfactants in the lungs of terrestrial and aquatic amphibians

Abstract

We examined the composition and function of pulmonary surfactants in amphibians inhabiting aquatic and terrestrial habitats with particular regard to the influences of (1) variations in body temperature, (2) external hydrostatic pressure and (3) breathing pattern. Two fully aquatic salamanders, and the completely terrestrial cane toad Bufo marinus (all maintained at 21–23 °C) were selected. Whereas one of the salamanders ( Siren intermedia) possessed gills and lungs, Amphiuma tridactylum only possessed lungs. We determined the amounts of cholesterol (Chol), disaturated phospholipids (DSP) and total phospholipid (PL) in lavage of all three species, and also determined the types of phospholipids of B. marinus and A. tridactylum. DSP lowers surface tension at the air-water interface in the lung, while Chol and unsaturated phospholipids assist spreading and maintain the DSP in its disordered, liquid-crystalline state at high lung volumes. All three species had significant amounts of pulmonary-type surfactant. The two aquatic salamanders had identical ratios of both Chol/PL and DSP/PL both of which in turn were nearly twice those of B. marinus. All three species had similar Chol/DSP ratios. Aquatic salamanders sustain high external hydrostatic pressure exerted by the aquatic environment and tend to collapse their lungs during expiration. We hypothesize that these salamanders might require a DSP-rich surfactant to prevent the epithelial surfaces from adhering and large amounts of Chol to keep the DSP fluid. The terrestrial B. marinus has less DSP, suggesting a surfactant which is fluid over a large range of temperatures. Possibly, cane toads do not require a DSP rich surfactant as they either collapse their lungs on deflation, nor experience external hydrostatic pressure promoting lung collapse. The PL profile of B. marinus lavage was similar to that of other frogs and mammals, containing phosphatidylcholine (PC) as the predominant phospholipid together with substantial amounts of phosphatidyglycerol (PG). On the other hand, although A. tridactylum exhibited high levels of PC, it contained phosphatidylinositol (PI) in place of PG, a pattern typical of reptiles and birds.