Abstract
Increases in thermal variability elevate metabolic rate due to Jensen's inequality, and increased metabolic rate decreases the fitness of dormant ectotherms by increasing consumption of stored energy reserves. Theory predicts that ectotherms should respond to increased thermal variability by lowering the thermal sensitivity of metabolism, which will reduce the impact of the warm portion of thermal variability. We examined the thermal sensitivity of metabolic rate of overwintering Erynnis propertius (Lepidoptera: Hesperiidae) larvae from a stable or variable environment reared in the laboratory in a reciprocal common garden design, and used these data to model energy use during the winters of 1973–2010 using meteorological data to predict the energetic outcomes of metabolic compensation and phenological shifts. Larvae that experienced variable temperatures had decreased thermal sensitivity of metabolic rate, and were larger than those reared at stable temperatures, which could partially compensate for the increased energetic demands. Even with depressed thermal sensitivity, the variable environment was more energy-demanding than the stable, with the majority of this demand occurring in autumn. Autumn phenology changes thus had disproportionate influence on energy consumption in variable environments, and variable-reared larvae were most susceptible to overwinter energy drain. Therefore the energetic impacts of the timing of entry into winter dormancy will strongly influence ectotherm fitness in northern temperate environments. We conclude that thermal variability drives the expression of metabolic suppression in this species; that phenological shifts will have a greater impact on ectotherms in variable thermal environments; and that E. propertius will be more sensitive to shifts in phenology in autumn than in spring. This suggests that increases in overwinter thermal variability and/or extended, warm autumns, will negatively impact all non-feeding dormant ectotherms which lack the ability to suppress their overwinter metabolic thermal sensitivity.
Highlights
The intuitive outcome of warmer winter temperatures for ectotherms is a release from cold-induced stress, leading to increased survival and expansion of geographic ranges [1,2]
We show that winter metabolic rate is suppressed by variable environments, and that most of the energy used during the dormant period is consumed in the autumn
Measurements in November represent the condition of animals prior to winter, but after a variable period of post-feeding dormancy
Summary
The intuitive outcome of warmer winter temperatures for ectotherms is a release from cold-induced stress, leading to increased survival and expansion of geographic ranges [1,2]. Metabolic rate is a function of temperature in many species, such that warmer winters result in individuals emerging from dormancy in spring with decreased energy reserves [3], reducing energy available for post-winter maintenance and reproduction, thereby depressing performance and fitness [4]. We explore the impact of thermal variability on overwinter energy use in a butterfly larva in the context of climate change. It is well-appreciated that an acute increase in temperature will result in an increase in the metabolic rate of an ectotherm. Jensen’s inequality states that the mean value of metabolic rate over the accelerating portion of the curve will increase with increasing variance in temperature [8]
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