Thermal Variability Increases the Impact of Autumnal Warming and Drives Metabolic Depression in an Overwintering Butterfly

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

Comparison of pre-winter thermal sensitivity of CO₂ production by <i>Erynnis propertius</i> among treatment groups.

<p>All models use the general form of Model 5 (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0034470#pone-0034470-t002" target="_blank">Table 2</a>). An overall scaling factor (S) and minimum life-supporting metabolic rate (L_met) were estimated from Model 5, while temperature-scaling (T_s) was estimated for the experimental groups separately or together. GNME: Generalized nonlinear Mixed Effects model (with T_s and S as fixed effects). GN: Generalized Nonlinear model. AIC: Akaike's Information criterion. df: degrees of freedom. The model with the lowest AIC is in bold type, and coefficients from this model were used in subsequent analyses. Different superscript letters indicate generalized nonlinear models that significantly differ in explanatory power (p<0.05). Coefficient p-value is the probability that T_s differs significantly from 0.</p

The predicted impact of phenological shifts on overwinter energy use by <i>Erynnis propertius</i>.

<p>The sensitivity of overwintering energy use of <i>E. propertius</i> 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 <i>E. propertius</i> (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0034470#pone-0034470-t002" target="_blank">Table 2</a>), 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.</p

Effects of thermal variability on the estimated coefficient of thermal sensitivity (Ts) in <i>Erynnis propertius</i>.

<p>Group-specific coefficients for thermal sensitivity (Ts) from the best-fit generalized nonlinear model (<i>CO₂ = S×T^Ts+L_met</i>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0034470#pone-0034470-t002" target="_blank">Tables 2</a> & <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0034470#pone-0034470-t003" target="_blank">3</a>) relating <i>E. propertius</i> CO₂ production rate to body temperature, in individuals from a stable environment reared at stable temperatures (BC stable) or individuals originating from a variable environment and/or reared at variable temperatures (all other rearing×source). Value indicated is mean ± SE.</p

Generalized nonlinear models relating measured <i>E. propertius</i> CO₂ production rate to measured body temperature.

<p>All models provided a better fit than a linear model (<i>CO2 = S×T</i>; log-likelihood test, p<0.05 in all cases). Model 5 was selected because there was no significant difference in explanatory power between Models 4 and 5 (likelihood ratio test, L = 3.06, p = 0.08) and Model 5 has fewer terms. A power of the mean model for variance was used in all models. Empirical input: CO₂: CO₂ production rate, ml·min⁻¹; T: Temperature, °C; M: body mass, mg. Coefficients estimated by maximum likelihood: S: an overall scaling factor; M_s: a mass scaling factor; T_s: a temperature scaling factor (i.e. thermal sensitivity). L_met: theoretical minimum life-supporting metabolic rate. AIC: Akaike's Information Criterion; df: degrees of freedom.</p

Temperature records from Vancouver Island and Oregon.

<p>Hourly meteorological data from (a) Victoria International airport, BC, 1973–2010; (b) Victoria International airport, BC, 1998–1999; (c) Rogue Valley International-Medford, OR, 1973–2009; (d) Rogue Valley International-Medford, OR, 1998–1999; (e) normal-based incubator temperature regimes, with timing of experimental events indicated.</p

Predicted overwinter energy use of <i>Erynnis propertius</i> from Oregon and Vancouver Island.

<p>(a) Predicted overwinter energy use from 1973–2010 in Oregon for larvae expressing high (dark squares) or low (light circles) thermal sensitivity. (b) Predicted energy use in their natal environment for larvae expressing high (BC, dark grey squares) or low (OR, light grey circles) thermal sensitivity, based on either hourly (solid lines, filled symbols) or monthly mean (dotted lines, open symbols) temperatures.</p

Collection sites and the geographic range of <i>Erynnis propertius</i>.

<p>Butterflies were collected from southern Vancouver Island, British Columbia and the vicinity of Medford, Oregon, overall distribution of this species is shaded in grey. Circles indicate the sampling locales and stars the location of the climate stations from which meteorological data were obtained. <i>E. propertius</i> has also been reported from Baja California Norte, Mexico (not shown). Data from Opler PA, Lotts K, Naberhaus T (coordinators) (2011) <i>Butterflies and Moths of North America</i>. <a href="http://www.butterfliesandmoths.org/" target="_blank">http://www.butterfliesandmoths.org/</a>; and Royal British Columbia Museum Entomology Collection, Canadian National Collection (CNC) of Insects, Arachnids and Nematodes, Lyman Entomological Museum, Nova Scotia Museum of Natural History, Halifax, NS, Canada, Lepidopterists Society Season Summaries 1973–1997, Crispin S. Guppy Collection, Royal Ontario Museum: Entomology, and the Spencer Entomological Museum (accessed through GBIF Data Portal, <a href="http://data.gbif.org" target="_blank">data.gbif.org</a>).</p

The predicted energetic cost of thermal variability for overwintering <i>Erynnis propertius</i>.

<p>Predicted extra lipid used overwinter by <i>E. propertius</i> larvae above that predicted by mean temperatures as a function of daily thermal amplitude in a given winter in OR or BC. Dark symbols: larvae with high thermal sensitivity in BC; light symbols: larvae with low thermal sensitivity in OR.</p