Striped marsh frog (Limnodynastes peronii) tadpoles do not acclimate metabolic performance to thermal variability

Abstract

SUMMARYHuman-induced climate change is predicted to affect not only the mean temperature of the environment but also the variability and frequency of extreme climatic events. Variability in an organism's developmental environment has the potential to markedly affect an individual's growth trajectory and physiological function, leading to impacts on individual fitness and population dynamics. Thus, it is important to consider the consequences of thermal variability on developing organisms and understand their capacity to respond to such increased variation. We investigated the capacity of larval striped marsh frogs (Limnodynastes peronii) to initiate a response to increases in the thermal variability of their developmental environment by reducing the sensitivity of their physiological rate functions to changes in temperature. In variable environments, we expected the thermal sensitivity of rate functions to decrease and their performance breadth to widen so as to buffer the effect of thermal variability. We raised larvae in stable (24°C), narrowly variable (22-26°C; mean 24°C) and widely variable (14-34°C; mean 24°C) thermal environments and measured the thermal sensitivity of their locomotor performance, heart rate, oxygen consumption and activities of two metabolic enzymes, lactate dehydrogenase and cytochrome c oxidase. We found that the temperature-dependent relationships of these physiological functions did not differ between tadpoles raised in stable or variable thermal conditions. Furthermore, the Q 10 values of each response variable were virtually unaffected by treatment when measured over the entire thermal range. Our results reveal that larval amphibians exhibit little plasticity in metabolic traits to thermal variability. This lack of plasticity may have important implications for the growth and population dynamics of organisms in environments that are beginning to experience increased thermal variability.

Temperature during embryonic development has persistent effects on metabolic enzymes in the muscle of zebrafish

“…The activity of this enzyme varied little across temperatures, differing by at most 30% across a 14°C range of assay temperatures and generally peaking between 27 and 32°C (Figs 3, 9). Similar patterns have been observed in some fish, amphibian and reptile species (Godiksen and Jessen, 2001;Glanville and Seebacher, 2006;Niehaus et al, 2011), but not in others (Caldwell, 1969;Blier and Lemieux, 2001). Furthermore, there were clear differences in thermal optima between the 22°C T E group (T opt of 27°C) and the 32°C T E group (T opt of 32°C).…”

Predicting the physiological performance of ectotherms in fluctuating thermal environments

“…Indeed, previous studies confirmed that thermal sensitivities of locomotor performance acclimate during larval development to constant thermal environments (Wilson and Franklin, 1999). Because constant environments are more likely to promote acclimation (Niehaus et al, 2011a), our ability to predict phenotypes in fluctuating environments should decrease as the magnitude of environmental variation increases (i.e. as the environment of interest differs more from a constant one).…”

“…We set the critical thermal minimum equal to 8°C for the growth of larvae, 15°C for the growth of embryos, and 15°C for the development of all stages (R.S.W., unpublished data) (Rogers et al, 2004). The critical thermal maximum for the growth and development of all stages was set equal to 34°C; this temperature A. C. Niehaus and others not only causes certain mortality during prolonged exposures but also approximates the upper thermal limit of aerobic scope (Niehaus et al, 2011a). These constraints were imposed by augmenting observed data with artificial data at the critical thermal limits; the number of artificial data for the thermal limits equalled the number of real data in each thermal treatment (e.g.…”

“…Nevertheless, our general conclusions about our hypotheses would have been the same for this scenario. Furthermore, tadpoles were unlikely to have developed at temperatures as high as 38°C given that they have no scope for aerobic metabolism at temperatures above 34°C (Niehaus et al, 2011a).…”

“…Dramatic fluctuations in temperature occur daily in many environments, including ephemeral pools (Johns et al, 1981;Dadour et al, 2001;Niehaus et al, 2006), shallow soils (Shine and Elphick, 2001;Ashmore and Janzen, 2003;Georges et al, 2005) and tidal waters (Stillman and Somero, 2000;Podrabsky and Somero, 2004). Despite the ubiquity of thermal change, studies of development at constant temperatures greatly outnumber studies of development at fluctuating temperatures [for examples of the latter, see the following references (Siddiqui and Barlow, 1972;Qualls and Shine, 1998;Loeschcke et al, 1999;Pétavy et al, 2004;Niehaus et al, 2011a;Niehaus et al, 2011b)]. Instead, impacts of thermal fluctuations are usually inferred from a reaction norm, which describes the relationship between temperature and the phenotype.…”