Temperature and UV-B insensitive performance in tadpoles of the Ornate burrowing frog: an ephemeral pond specialist

Abstract

Animals may overcome the challenges of temperature instability through behavioural and physiological mechanisms in response to short-and long-term temperature changes. When ectotherms face the challenge of large diel temperature fluctuations, one strategy may be to reduce the thermal sensitivity of key traits in order to maintain performance across the range of temperatures experienced. Additional stressors may limit the ability of animals to respond to these thermally challenging environments through changes to energy partitioning or interactive effects. Ornate burrowing frog (Platyplectrum ornatum) tadpoles develop in shallow ephemeral pools that experience high diel thermal variability (>20°C) and can be exposed to high levels of UV-B radiation. Here, we investigated how development in fluctuating versus stable temperature conditions in the presence of high or low UV-B radiation influences thermal tolerance and thermal sensitivity of performance traits of P. ornatum tadpoles. Tadpoles developed in either stable (24°C) or fluctuating temperatures (18-32°C) under high or low UV-B conditions. Tadpoles were tested for upper critical thermal limits, thermal dependence of resting metabolic rate and maximum burst swimming performance. We hypothesised that developmental responses to thermal fluctuations would increase thermal tolerance and reduce thermal dependence of physiological traits, and that trade-offs in the allocation of metabolic resources towards repairing UV-B-induced damage may limit the ability to maintain performance over the full range of temperatures experienced. We found that P. ornatum tadpoles were thermally insensitive for both burst swimming performance, across the range of temperatures tested, and resting metabolic rate at high temperatures independent of developmental conditions. Maintenance of performance led to a trade-off for growth under fluctuating temperatures and UV-B exposure. Temperature treatment and UV-B exposure had an interactive effect on upper critical thermal limits possibly due to the upregulation of the cellular stress response. Thermal independence of key traits may allow P. ornatum tadpoles to maintain performance in the thermal variability inherent in their environment.

Physiological responses of ectotherms to daily temperature variation

“…Acclimation allows animals to overcome (to varying degrees) the challenges associated with mean temperature change (Wilson and Franklin, 1999;Seebacher and Grigaltchik, 2014). Many ectotherms, however, appear to lack the capacity to physiologically respond to DTFs in a way that allows them to prevent increased metabolic demands associated with peak environmental temperatures (Henry and Houston, 1984;Kingsolver et al, 2009;Niehaus et al, 2011;Kjörsgaard et al, 2013;Kern et al, 2014). In this study, DTFs increased upper thermal limits, which may buffer tadpoles from the lethal consequences of temperature extremes.…”

“…High DTFs in the environment could mask stable temperature cues and reduce environmentally induced plasticity, leading instead to selection of a broad performance curve (Huey and Hertz, 1984). This may be true for P. ornatum, which has thermally insensitive swimming performance and RMR (Kern et al, 2014) which may enable this species to maintain performance and buffer metabolic demands from DTFs inherent in their environment.…”

“…All three species are from the subfamily Limnodynastinae (Pyron and Wiens, 2011), which are characterised by building foam nests. Platyplectrum ornatum inhabit dry environments and breed after heavy rain in highly ephemeral water bodies characterised by large DTFs (>20°C; Anstis, 2002;Kern et al, 2014). The tadpoles of this species have low thermal sensitivity for burst swimming performance (Kern et al, 2014).…”

“…Platyplectrum ornatum inhabit dry environments and breed after heavy rain in highly ephemeral water bodies characterised by large DTFs (>20°C; Anstis, 2002;Kern et al, 2014). The tadpoles of this species have low thermal sensitivity for burst swimming performance (Kern et al, 2014). Limnodynastes peronii and L. tasmaniensis are usually associated with permanent and semi-permanent water bodies that experience smaller DTFs (Fig.…”

“…In response to DTFs, individuals can also increase thermal tolerance, reducing damage caused by temperature extremes (Feldmeth et al, 1974;Schaefer and Ryan, 2006). However, some species show no change in thermal sensitivity in response to DTFs (Niehaus et al, 2011;Kern et al, 2014).…”