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.

行为体温调节（Behavioural thermoregulation）对于动物抵御极端温度至关重要。然而，众多动物在进行体温调节时，不得不面临热逃避与食物获取之间的权衡，但目前学界仍不明确动物如何依据自身对高温和饥饿的不同耐受能力，平衡过热与饥饿两类风险。在此，我们提出一项假说，用于预测动物在行为体温调节过程中如何权衡高温与饥饿风险：饥饿风险较高的动物会优先通过承担更高热风险来降低饥饿威胁，而饥饿风险较低的动物则会优先通过承担更低热风险来缓解热应激。我们选取3种蚜虫作为研究对象，分别为麦长管蚜（Metopolophium dirhodum）、麦二叉蚜（Sitobion avenae）与禾谷缢管蚜（Schizaphis graminum）。首先，通过模拟日间环境温度的线性升高过程，我们测定了蚜虫的避热温度（heat-avoidance temperatures, HATs）与临界高温（critical thermal maximum, CTmax），以解析其体温调节行为与高温耐受能力；随后，我们测试了蚜虫定位寄主植物的耗时（time spent locating a host plant, TL）以及饥饿状态下的存活时长（survival time under starvation, TS），分别用于评估其食物可获得性与饥饿耐受能力；最后，我们结合上述实验结果，将蚜虫的热风险（CTmax减去HAT）与饥饿风险（TS减去TL）与其体温调节行为进行关联，以验证所提出的假说。我们的研究结果为该假说提供了支持性证据：饥饿风险较高的蚜虫类群会优先通过更长时间取食寄主植物、更晚逃离高温环境来降低饥饿威胁，进而承担更高的热风险；与之相反，饥饿风险较低的类群则会优先通过缩短取食时长、更早逃离高温环境来限制热应激，从而承担更低的热风险。动物或可基于各自的食物可获得性、饥饿耐受能力与高温耐受能力，采取差异化策略以降低饥饿与高温的综合风险。本研究结果凸显了动物决策行为中多重风险交互作用的复杂性，这对于提升其适合度具有重要意义。在预测气候变化影响的研究中纳入行为体温调节因素时，这类差异化行为及其潜在后果不容忽视。