Temperature variation makes ectotherms more sensitive to climate change

Abstract

Ectotherms are considered to be particularly vulnerable to climate warming. Descriptions of habitat temperatures and predicted changes in climate usually consider mean monthly, seasonal or annual conditions. Ectotherms, however, do not simply experience mean conditions, but are exposed to daily fluctuations in habitat temperatures. Here, we highlight how temperature fluctuation can generate 'realized' thermal reaction (fitness) norms that differ from the 'fundamental' norms derived under standard constant temperatures. Using a mosquito as a model organism, we find that temperature fluctuation reduces rate processes such as development under warm conditions, increases processes under cool conditions, and reduces both the optimum and the critical maximum temperature. Generalizing these effects for a range of terrestrial insects reveals that prevailing daily fluctuations in temperature should alter the sensitivity of species to climate warming by reducing 'thermal safety margins'. Such effects of daily temperature dynamics have generally been ignored in the climate change literature.

Keywords: Anopheles stephensi; Jensen's inequality; climate change; conservation; diurnal temperature fluctuation; ectotherm fitness; thermal fitness curve; thermal reaction norm.

Figure 1

Effect of daily temperature variation on ectotherm fitness. Fundamental performance curve (relative fitness; black line) under constant temperature conditions and realized performance when appropriate daily temperature variation is considered (grey line) for the temperate terrestrial insect Muscidifurax zaraptor. Gray data point and horizontal grey line represent the mean habitat temperature (T_h) and the average habitat temperature range, respectively. CT_min, critical minimum temperature; (r)T_o, (realized) optimum temperature; (r)CT_max, (realized) critical maximum temperature; and (r)TSM, (realized) thermal safety margin.

Figure 2

Impact of constant and variable temperatures on insect life-history traits. (a, b) Fundamental thermal reaction norm for (a) daily development rate and (b) survival of Anopheles stephensi mosquito immatures measured at 11 constant temperatures. (c, d) Effects of fluctuation at different points on the fundamental curve: Estimated marginal mean (c) development rate and (d) survival at mean temperatures of 18, 26, or 32 °C, combined with daily temperature ranges (DTRs) of 0, 8, or 12 °C. (e, f) Effects of temperature variation on the temperature optimum: Estimated marginal mean (e) development rate and (f) survival at mean temperatures of 28, 30 or 32 °C, combined with DTRs of 0 or 12 °C. The vertical error bars in all panels represent the standard error of the mean.

Figure 3

Impact of variable temperatures on the critical maximum temperature. Survival of Anopheles stephensi mosquito immatures at various mean temperatures (x-axis) and daily temperature ranges (DTRs) of (a) 8 °C, (b) 12 °C, or (c) 16 °C. Note that rCT_max is lower than the fundamental CT_max of 36 °C in a constant environment (Fig. 2b). (d) Effect of smaller DTRs around a mean temperature of 35 °C. Vertical error bars represent the standard error of the mean.

Figure 4

Effects of daily temperature variation and climate warming on thermal safety margins across latitude. Thermal safety margins for 29 terrestrial insect across latitude, as estimated for (a) the period 1960–1990 or (b) the period 2080. Open gray circles represent estimates based on the mean habitat temperature, black solid circles estimates based on the average habitat temperature range. The gray area represents the tropics.