Oxygen uptake in bullfrog tadpoles (Rana catesbeiana)

Abstract

Weight-specific rates of aquatic oxygen consumption (VO2, microliter O2 g-1 h-1) at 23 degrees C were determined for water-breathing (e.g., forcibly submerged) bullfrog tadpoles as functions of stage of development and O2 tension (PO2). The VO2 at an O2 tension near that of air-saturated water (PO2 approximately 154 mmHg) was independent of stage of development throughout the premetamorphic stages (I-XIX). Aquatic VO2 increased by approximately 24%, relative to the average of the preceding stages, during the first metamorphic stage (XX) and thereafter decreased steadily with developmental stage. The decline in aquatic VO2 resulted in a shift from facultative air-breathing to obligate air-breathing at about stage XXII. Changes with developmental stage of the critical O2 tension (Pc) corresponded to changes in aquatic VO2. The Pc was low and relatively constant at 29-36 mmHg through stage XVI, started to increase (to 51 mmHg) during the final premetamorphic stages (XVII-XIX), reached a value near air saturation (159 mmHg) at stage XXII, and was in excess of air saturation for stages XXIII-XXV. The ability to survive continuous submergence paralleled the changes in Pc, as tadpoles could survive in air-saturated water without access to air through stages XXII-XXIII, when they drowned. Whole-body lactate concentrations of tadpoles in normoxic water with access to air averaged 0.56 mg/g through stage XX, comparable to that of froglets (stage XXV, 0.67 mg/g) in shallow water. Animals in anoxic water with access to air exhibited an approximate doubling (1.05 mg/g) of lactate concentration for all stages, as did metamorphic stages XXI-XXV in normoxic water with air access. Recently, metamorphosed frogs (stage XXV) could survive continuous submergence for up to 200 h without accumulating lactate if the water was hyperoxic (600-700 mmHg), suggesting that cutaneous O2 exchange in normoxic water is diffusion-limited. Stages I-XXI in normoxic water breathed air regularly but infrequently (0.4-6.2 surfacings/h), with earlier stages breathing more frequently than later stages. While not required for oxygen uptake during these stages, air-breathing may serve to promote lung development, to prevent lung collapse, or to prevent accumulation of fluid in the lungs. Surfacing rates increased as the PO2 of the water decreased, but we could discern no clear relationship between the Pc for surfacing and developmental stage. Stages XXII-XXV spent most of their time floating. The changes in aquatic VO2, Pc, surfacing behavior, and survivorship when forcibly submerged, all suggest that stage XXII is a critical developmental stage during which bullfrog tadpoles switch from a primarily aquatic to a primarily terrestrial mode of existence. When provided with a choice of being in or out of water, early stages abruptly change from a preference for water (e.g., 92.5% of stage XXI) to a preference for land by stage XXII (74%), further indicating the transitional nature of the latter stage.