The mechanics of air-breathing in gray tree frog tadpoles, Hyla versicolor LeConte, 1825 (Anura: Hylidae)

Abstract

We describe air-breathing mechanics in gray tree frog tadpoles (Hyla versicolor). We found that H. versicolor tadpoles breathe by 'bubble-sucking', a breathing mode typically employed by tadpoles too small to break the water's surface tension, in which a bubble is drawn into the buccal cavity and compressed into the lungs. In most tadpoles, bubble-sucking is replaced by breach breathing (breaking the surface to access air) at larger body sizes. In contrast, H. versicolor tadpoles bubble-suck throughout the larval period, despite reaching body sizes at which breaching is possible. Hyla versicolor tadpoles exhibit two bubble-sucking behaviors: 'single bubble-sucking', previously described in other tadpole species, is characterized by a single suction event followed by a compression phase to fill the lungs; 'double bubble-sucking' is a novel, apparently derived form of bubble-sucking that adds a second suction event. Hyla versicolor tadpoles transition from single bubble-sucking to double bubble-sucking at approximately 5.7 mm snout-vent length (SVL), which corresponds to a period of rapid lung maturation when they transition from low to high vascularization (6.0 mm SVL). Functional, behavioral and morphological evidence suggests that double bubble-sucking increases the efficiency of pulmonary gas exchange by separating expired, deoxygenated air from freshly inspired air to prevent mixing. Hyla versicolor, and possibly other hylid tadpoles, may have specialized for bubble-sucking in order to take advantage of this increased efficiency. Single and double bubblesucking represent two-and four-stroke ventilation systems, which we discuss in the context of other anamniote air-breathing mechanisms.

Circumventing surface tension: tadpoles suck bubbles to breathe air

“…R. Soc. B 287: 20192704 until sometime later in development [18] and this may be true for other species, as well. As such, air-breathing/lung filling at very early stages may be non-respiratory.…”

“…Tadpoles of the two hylid species examined exhibited a variant form of bubble-sucking at larger body sizes characterized by a second suction event immediately following the first. We treat this phenomenon in a separate paper [18]. Here, we restrict our attention to 'single bubble-sucks', the form of bubble-sucking that occurred in all species.…”

“…Like virtually all other anamniotes, tadpoles use a buccal pump to force air into the lungs [18]. Diving and hydrostatic pressure do not drive lung filling (contra [20]).…”

The case for studying tadpole autecology, with comments on strategies to study other small,fast‐movinganimals in nature

“…Such differences are indiscernible to the naked eye, but with the help of a high-speed camera and a macro lens, important changes in the air-breathing biology of tadpoles could be observed. Phillips et al (2020Phillips et al ( , 2022 went on to show that in some species, air-breathing kinematics change predictably with lung morphology, demarking a clear shift from non-respiratory air-breathing for buoyancy regulation to respiratory air-breathing.…”

Air–breathing behavior underlies the cell death in limbs of Rana pirica tadpoles

“…Next, we examined whether pulmonary respiration occurs during hindlimb development stages of R. pirica tadpoles. The lungs of X. laevis tadpoles are inflated beginning at stage 46 (before hindlimb bud initiation) and are filled with air by stage 58 (when hindlimb morphogenesis is complete), the latter visualized by the presence of air bubbles [19,32,33]. Of the 11 lungs dissected from stage 31-35 R. pirica tadpoles, 45% contained air bubbles.…”