Rapid adjustments in thermal tolerance and the metabolome to daily environmental changes – a field study on the Arctic seed bug Nysius groenlandicus

Laboratory investigations on terrestrial model-species, typically of temperate origin, have demonstrated that terrestrial ectotherms can cope with daily temperature variations by rapid heat or cold hardening. However, few studies have investigated this ability and its physiological basis in the field. This is even more true in the polar regions, where temporal and spatial temperature variations can be extreme, e.g. during the arctic summer. We examined adjustments in heat and cold tolerance in the Greenlandic seed bug Nysius groenlandicus to daily changes in microhabitat temperatures by collecting individuals for thermal assessment at different time points within and across days. Secondly, we assessed underlying metabolomic fingerprints using GC-MS metabolomics in a subset of individuals collected during days with either low or high temperature variation. We found a significant correlation between observed heat or cold tolerance and the ambient microhabitat temperatures at the time of capture, indicating that N. groenlandicus continuously and within short time-windows respond physiologically to thermal changes in their microhabitats. Concentrations of some metabolites varied significantly with time of collection and temperature. For instance, we detected elevated sugar levels in animals caught at the lowest daily field temperatures. Polyol concentrations were lower in individuals collected at the time points with the coldest temperatures and higher at the warmest temperatures. Additionally, changes in concentrations of metabolites associated with energetic metabolism was observed across collection times. Our findings suggest that hardening responses under natural conditions are marked and likely play a crucial role for coping with microhabitat temperature variation on a daily scale, and that metabolite levels are actively altered on a daily basis. Such results provide interesting new knowledge on the thermal biology of a common insect from the Arctic region, and contribute to our understanding of responses and robustness of arthropods to environmental changes in fragile and thermally variable ecosystems.针对通常起源于温带的陆生模式物种开展的实验室研究已证实，陆生变温动物（terrestrial ectotherms）可通过快速热硬化与冷硬化应对每日温度波动。然而，鲜有研究在野外环境中探究此类适应能力及其生理基础。这一情况在极地地区尤为突出——该区域的温度时空波动幅度可达到极端水平，例如北极夏季时段。我们以格陵兰籽蝽（Nysius groenlandicus）为研究对象，通过在单日及跨日的不同时间点采集个体进行热耐受性评估，探究其对微生境温度日变化的耐热与耐寒适应性调节机制。其次，我们针对在温度波动幅度较低或较高的日期采集的部分个体，采用气相色谱-质谱联用（GC-MS）代谢组学技术分析其潜在代谢指纹图谱。研究发现，观测到的耐热与耐寒耐受性与个体采集时的微生境环境温度存在显著相关性，表明格陵兰籽蝽可在短时间窗口内持续对微生境的温度变化产生生理性响应。部分代谢物的浓度会随采集时间与环境温度发生显著变化：例如，在每日野外最低温度时段采集的个体中，我们检测到糖类水平升高；而在最冷时段采集的个体中，多元醇浓度较低，在最暖时段采集的个体中则浓度更高。此外，我们还观测到与能量代谢相关的代谢物浓度在不同采集时间点间存在变化。我们的研究结果表明，自然条件下的硬化响应特征显著，且可能在日常尺度上应对微生境温度波动中发挥关键作用，同时代谢物水平会以日为周期发生主动调控。此类研究结果为北极地区常见昆虫的热生物学特性研究提供了新颖的见解，也有助于加深我们对脆弱且温度多变的生态系统中，节肢动物应对环境变化的响应机制与抗逆能力的理解。