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Thermal variability increases the impact of autumnal warming and drives metabolic depression in an overwintering butterfly.

Williams CM, Marshall KE, MacMillan HA, Dzurisin JD, Hellmann JJ, Sinclair BJ - PLoS ONE (2012)

Bottom Line: 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 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Western Ontario, London, Ontario, Canada.

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.

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The predicted impact of phenological shifts on overwinter energy use by Erynnis propertius.The sensitivity of overwintering energy use of E. propertius larvae to phenological shifts in OR (low thermal sensitivity; light grey) or BC (high thermal sensitivity; dark grey). Dates encompass the full range of start and end times of dormancy in E. propertius (Table 2), and each surface represents the average of 37 years' energy use at that location. Black dots indicate location-specific start and end dates; from the average date of dormancy onset to median date of adult flight.
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pone-0034470-g007: The predicted impact of phenological shifts on overwinter energy use by Erynnis propertius.The sensitivity of overwintering energy use of E. propertius larvae to phenological shifts in OR (low thermal sensitivity; light grey) or BC (high thermal sensitivity; dark grey). Dates encompass the full range of start and end times of dormancy in E. propertius (Table 2), and each surface represents the average of 37 years' energy use at that location. Black dots indicate location-specific start and end dates; from the average date of dormancy onset to median date of adult flight.

Mentions: We used our hourly estimates of lipid use in each location (1973–2010) to predict the energetic impact of phenological shifts at the beginning and end of the dormant period. At any given length of dormancy, overwintering in stable Vancouver Island conditions is less energetically expensive than overwintering in variable Oregon conditions (Fig. 7), despite the metabolic rate suppression expressed by OR-derived individuals. This discrepancy in energetic costs between locations increases with longer dormant periods, and phenological changes have more impact in variable conditions (Fig. 7). Using start and end dates informed by field observations to establish a ‘typical’ phenology, we predict lipid consumption in OR (27.3 mg) to be more than double that on BC (12.7 mg; Fig. 7). Our models indicate a steeper decline in energy use with delayed diapause date compared to advancing emergence date (Fig. 7), suggesting that phenological shifts will have a greater energetic impact in autumn than in spring.


Thermal variability increases the impact of autumnal warming and drives metabolic depression in an overwintering butterfly.

Williams CM, Marshall KE, MacMillan HA, Dzurisin JD, Hellmann JJ, Sinclair BJ - PLoS ONE (2012)

The predicted impact of phenological shifts on overwinter energy use by Erynnis propertius.The sensitivity of overwintering energy use of E. propertius larvae to phenological shifts in OR (low thermal sensitivity; light grey) or BC (high thermal sensitivity; dark grey). Dates encompass the full range of start and end times of dormancy in E. propertius (Table 2), and each surface represents the average of 37 years' energy use at that location. Black dots indicate location-specific start and end dates; from the average date of dormancy onset to median date of adult flight.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3316672&req=5

pone-0034470-g007: The predicted impact of phenological shifts on overwinter energy use by Erynnis propertius.The sensitivity of overwintering energy use of E. propertius larvae to phenological shifts in OR (low thermal sensitivity; light grey) or BC (high thermal sensitivity; dark grey). Dates encompass the full range of start and end times of dormancy in E. propertius (Table 2), and each surface represents the average of 37 years' energy use at that location. Black dots indicate location-specific start and end dates; from the average date of dormancy onset to median date of adult flight.
Mentions: We used our hourly estimates of lipid use in each location (1973–2010) to predict the energetic impact of phenological shifts at the beginning and end of the dormant period. At any given length of dormancy, overwintering in stable Vancouver Island conditions is less energetically expensive than overwintering in variable Oregon conditions (Fig. 7), despite the metabolic rate suppression expressed by OR-derived individuals. This discrepancy in energetic costs between locations increases with longer dormant periods, and phenological changes have more impact in variable conditions (Fig. 7). Using start and end dates informed by field observations to establish a ‘typical’ phenology, we predict lipid consumption in OR (27.3 mg) to be more than double that on BC (12.7 mg; Fig. 7). Our models indicate a steeper decline in energy use with delayed diapause date compared to advancing emergence date (Fig. 7), suggesting that phenological shifts will have a greater energetic impact in autumn than in spring.

Bottom Line: 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 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Western Ontario, London, Ontario, Canada.

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.

Show MeSH
Related in: MedlinePlus