Circumventing surface tension: tadpoles suck bubbles to breathe air

Abstract

The surface tension of water provides a thin, elastic membrane upon which many tiny animals are adapted to live and move. We show that it may be equally important to the minute animals living beneath it by examining air-breathing mechanics in five species (three families) of anuran (frog) tadpoles. Air-breathing is essential for survival and development in most tadpoles, yet we found that all tadpoles at small body sizes were unable to break through the water's surface to access air. Nevertheless, by 3 days post-hatch and only 3 mm body length, all began to breathe air and fill the lungs. High-speed macrovideography revealed that surface tension was circumvented by a novel behaviour we call ‘bubble-sucking’: mouth attachment to the water's undersurface, the surface drawn into the mouth by suction, a bubble ‘pinched off’ within the mouth, then compressed and forced into the lungs. Growing tadpoles transitioned to air-breathing via typical surface breaching. Salamander larvae and pulmonate snails were also discovered to ‘bubble-suck’, and two insects used other means of circumvention, suggesting that surface tension may have a broader impact on animal phenotypes than hitherto appreciated.

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

“…Visualization is particularly difficult in small tadpoles (those performing SBS), because the lungs are very small and do not bulge externally, as they do when full in larger individuals. However, we believe that lung emptying often occurs during the suction phase of SBS because the lungs in tadpoles of other frog species, as well as in adult frogs, empty at a comparable phase of air breathing (Schwenk and Phillips, 2020;de Jongh and Gans, 1969;Gans et al, 1969;Gnanamuthu, 1936;Jones, 1982;Macintyre and Toews, 1976;Vitalis and Shelton, 1990;West and Jones, 1974a,b). Alternatively, it has been suggested that tadpole lungs might empty passively via diffusion into surrounding tissues (Ultsch et al, 1999).…”

“…breathing (Schwenk and Phillips, 2020). Because of these mechanical differences, we expect that DBS is functionally more efficient for gas exchange than SBS.…”

“…Among the five species studied by Schwenk and Phillips (2020), the tadpoles of one species never transitioned to breach breathing. Gray tree frog [Hyla versicolor LeConte 1825 (Hylidae)] tadpoles continued to bubble-suck throughout the larval period and well into metamorphic climax, despite growing large and fast enough to breach the surface.…”

“…Just as it is now understood that lungs preceded the transition to terrestrial life in tetrapods, it is now widely known that the development of lungs in many tadpoles occurs well before metamorphosis (Weisz, 1945;Feder, 1984;Ultsch et al, 1999;Wells, 2007). Indeed, a recent study of five species representing three families found that air-breathing behavior and lung inflation occurred within a few days of hatching (Schwenk and Phillips, 2020).…”

“…With the exception of one study (Wassersug and Yamashita, 2000), the mechanics of air breathing have been virtually unstudied. Recently, however, Schwenk and Phillips (2020) examined air-breathing mechanics in tadpoles of five frog species. They found that small size and weak swimming prevented young tadpoles from breaking through the water's surface tension to breathe air.…”