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Untangling the roles of microclimate, behavior and physiological polymorphism in governing vulnerability of intertidal snails to heat stress
Updated on2017-5-10      Visits314

Abstract: Biogeographic distributions are driven by cumulative effects of smaller scale processes. Thus, vulnerability of animals to thermal stress is the result of physiological sensitivities to body temperature (Tb), microclimatic conditions, and behavioural thermoregulation. To understand interactions among these variables, we analysed the thermal tolerances of three species of intertidal snails from different latitudes along the Chinese coast, and estimated potential Tb in different microhabitats at each site. We then empirically determined the temperatures at which heart rate decreased sharply with rising temperature (Arrhenius breakpoint temperature, ABT) and at which it fell to zero (flat line temperature, FLT) to calculate thermal safety margins (TSM). Regular exceedance of FLT in sun-exposed microhabitats, a lethal effect, was predicted for only one mid-latitude site. However, ABTs of some individuals were exceeded at sun-exposed microhabitats in most sites, suggesting physiological impairment for snails with poor behavioural thermoregulation and revealing inter-individual variations (physiological polymorphism) of thermal limits. An autocorrelation analysis of Tb showed that predictability of extreme temperatures was lowest at the hottest sites, indicating that the effectiveness of behavioural thermoregulation is potentially lowest at these sites. These results illustrate the critical roles of mechanistic studies at small spatial scales when predicting effects of climate change.


Figure 1. Relationship between cardiac performance (ABT, FLT) and TSM. (a) Heart rate increases with temperature until the Arrhenius Breakpoint Temperature (ABT) is reached and then decreases rapidly to zero (black circles and the red curve following left y-axis). ABT was calculated by linear regression (blue lines) using data on Arrhenius plots (gray circles following the right y-axis) that lay either above or below the temperature at which the highest heart rate occurred. The temperature at which these two lines intersected was taken as the ABT. FLT is the temperature where heart beat ceases. TSM is defined as the difference between an organism’s critical thermal maximum (ABT (nonlethal) or FLT (lethal)) and the highest body temperature that an organism is likely to experience in nature (TSMABT = ABT – Tbmax, TSMFLT = FLT - Tbmax). Due to the physiological polymorphism and microhabitat heterogeneity, TSM varies among (b) individuals and (c) microhabitats.


Figure 2. High inter-individual, inter-population and interspecific variability in cardiac performance curves. (a) Variation within a population: dashed lines depict individual heart rates and the solid line depicts the curve for all individuals of L. sinensis from the Xiamen population (n = 10). (b) Variation among populations: dashed lines depict heart rate curves generated for each population and the solid line depicts the curve for all individuals of L. sinensis from all populations (n = 70). (c) Interspecific comparisons: the solid, dashed and dotted lines depict the heart rate curves of L. sinensis, L. brevicula and N. yoldii, respectively.


Figure 3. Phase diagrams of heat-tolerance limits and maximum operative temperatures in sun-exposed (a, c) and shaded habitats (b, d). The white region shows where species have a physiological thermal-safety margin for ABT and FLT; the shaded region shows where species are threatened by temperatures above either ABT (c, d) or FLT (a, b) thermal stress.


Figure 4. Thermal safety margin (TSM) of three gastropods with latitude. Solid lines show linear regressions for TSM with latitude and dotted lines show 95% confidence intervals. TSM was calculated for the FLT (a, b) and the ABT (c, d) in sun-exposed (a, c) and shaded habitats (b, d).

Citation: Dong Yun-wei, Li Xiao-xu, Choi FMP, Williams GA, Somero GN, Helmuth B. 2017 Untangling the roles of microclimate, behaviour and physiological polymorphism in governing vulnerability of intertidal snails to heat stress. Proceedings of Royal Society B 284: 20162367.

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