The mechanics of air breathing in African clawed frog tadpoles, Xenopus laevis (Anura: Pipidae)

Abstract

ABSTRACT Frog larvae (tadpoles) undergo many physiological, morphological and behavioral transformations throughout development before metamorphosing into their adult form. The surface tension of water prevents small tadpoles from breaching the surface to breathe air (including those of Xenopus laevis), forcing them to acquire air using a form of breathing called bubble sucking. With growth, tadpoles typically make a behavioral/biomechanical transition from bubble sucking to breaching. Xenopus laevis tadpoles have also been shown to transition physiologically from conforming passively to ambient oxygen levels to actively regulating their blood oxygen. However, it is unknown whether these mechanical and physiological breathing transitions are temporally or functionally linked, or how both transitions relate to lung maturation and gas exchange competency. If these transitions are linked, it could mean that one biomechanical breathing mode (breaching) is more physiologically proficient at acquiring gaseous oxygen than the other. Here, we describe the mechanics and development of air breathing and the ontogeny of lung morphology in X. laevis throughout the larval stage and examine our findings considering previous physiological work. We found that the transitions from bubble sucking to breaching and from oxygen conforming to oxygen regulation co-occur in X. laevis tadpoles at the same larval stage (Nieuwkoop–Faber stages 53–56 and 54–57, respectively), but that the lungs do not increase significantly in vascularization until metamorphosis, suggesting that lung maturation, alone, is not sufficient to account for increased pulmonary capacity earlier in development. Although breach breathing may confer a respiratory advantage, we remain unaware of a mechanistic explanation to account for this possibility. At present, the transition from bubble sucking to breaching appears simply to be a consequence of growth. Finally, we consider our results in the context of comparative air-breathing mechanics across vertebrates.