CO 2 -metabolism in early tetrapods revisited: inferences from osteological correlates of gills, skin and lung ventilation in the fossil record

Abstract

One of the most important physiological changes during the conquest of land by vertebrates was the increasing reliance on lung breathing, with the concomitant decrease in importance of gill breathing. The main problem involved here was to cope with the excessive accumulation of CO2 in the body and to avoid respiratory acidosis. In the past, several often mutually contradicting hypotheses of CO2-elimination via skin, lungs and gills in early tetrapods have been proposed, based on theoretical physiological considerations and comparison with extant air-breathing fishes and amphibians. This study proposes a revised scenario of CO2-elimination in early tetrapods based on fossil evidence, that is recently identified osteological correlates of gills, skin structure and mode of lung ventilation. In stem tetrapods of the Devonian and Carboniferous, O2-uptake via the lungs by buccal pumping was decoupled from CO2-release via internal gills, and the rather gas-impermeable skin played a minor role in gaseous exchange. The two main lineages of crown-group tetrapods, the amphibian and amniote lineage, used different strategies of CO2-elimination. As in stem tetrapods, O2-uptake and CO2-release remained always largely decoupled in temnospondyls, which ventilated their lungs via buccal pumping and relied mainly on their internal gills for CO2-release. Temnospondyls were not able to reduce their internal gills before their skin became more gas permeable and their body size was reduced, to shift from internal gills to the skin as the major site of CO2-elimination, a pattern that is retained in most lissamphibians. In contrast, internal gills were lost very early in stem amniote evolution. This was associated with the evolution of the more effective aspiration pump that allowed the elimination of the bulk of CO2 via the lungs, leading to a coupled O2-uptake and CO2-loss in stem amniotes and later in amniotes.