Trade-off between overheating and fasting: how animals minimize heat vs. starvation risk during behavioural thermoregulation

Behavioural thermoregulation is critical for animals to buffer against thermal extremes. However, many animals have to face a trade-off between heat escape and food acquisition during thermoregulation, but how animals balance overheating vs. starvation risk based on their different resistance to heat and starvation currently remains unclear. Here, we proposed a hypothesis for predicting how animals reduce heat vs. starvation risk during behavioural thermoregulation. Animals with higher starvation risk give priority to reducing starvation by taking a higher heat risk, whereas animals with lower starvation risk give priority to reducing heat stress by taking a lower heat risk. We used three aphid species (Metopolophium dirhodum, Sitobion avenae, Schizaphis graminum) as focal animals. First, by simulating linearly increasing ambient temperatures during the daytime, we measured the heat-avoidance temperatures (HATs) and critical thermal maximum (CTmax) values to understand their thermoregulatory behaviour and heat tolerance. Then, we tested the time spent locating a host plant (TL) and the survival time under starvation (TS) of the aphids to assess their food accessibility and starvation tolerance, respectively. Finally, we combined these results by linking the aphids’ heat risk (CTmax minus HAT) and starvation risk (TS minus TL) with their thermoregulatory behaviour to test our hypothesis. Our results provide evidence to support our hypothesis. The species with higher starvation risk gave priority to reducing starvation by spending more time feeding on the host plant and escaping from heat later and thus taking a higher heat risk. In contrast, the species with lower starvation risk gave priority to limiting heat stress by spending less time on feeding and escaping from heat earlier and thus taking a lower heat risk. Animals may adopt different strategies to reduce the integrative risks of starvation and heat based on their respective food accessibility, starvation resistance and heat tolerance. Our findings highlight the complexity of the interactions among multiple risks in animal decision-making behaviour to increase their fitness. Such different behaviours and their potential consequences matter when taking behavioural thermoregulation into account in predicting the impacts of climate change