Seeking temporal refugia to heat stress: Increasing nocturnal activity despite predation risk

Flexibility in activity timing may enable organisms to quickly adapt to environmental changes. Under global warming, diurnally adapted endotherms may achieve a better energy balance by shifting their activity towards cooler nocturnal hours. However, this shift may expose animals to new or increased environmental challenges (e.g., increased predation risk, reduced foraging efficiency). We analysed a large dataset of activity data from 47 ibex (Capra ibex) in two protected areas, characterized by varying levels of predation risk (presence vs absence of the wolf – Canis lupus). We found that ibex increased nocturnal activity following warmer days and during brighter nights. Despite the considerable sexual dimorphism typical of this species and the consequent different predation-risk perception, males and females demonstrated consistent responses to heat in both predator-present and predator-absent areas. This supports the hypothesis that shifting activity towards nighttime may be a common strategy adopted by diurnal endotherms in response to global warming. As nowadays different pressures are pushing mammals towards nocturnality, our findings emphasize the urgent need to integrate knowledge of temporal behavioural modifications into management and conservation planning.

Methods
Activity data logging: The activity data of individual ibex (18 males and 9 females in PNGP, 12 males and 8 females in SNP, more details in the Supporting Information Table S1 and Table S2) were recorded by means of a dual-axis motion sensor (i.e., accelerometer) fitted on the collars. The accelerometer simultaneously measures along two orthogonal directions the changes in acceleration associated with the actual motion experienced by the collar. On the X-axis, the accelerometer was sensitive to acceleration events with forward/backward direction/axes, while on the Y-axis, it recorded acceleration events with a sideways and rotary direction. The accelerometer had a dynamic range of ±2g and measured activity as the change of static acceleration (gravity) and dynamic acceleration (collar) with a frequency of 4 Hz. The motion data from accelerometers, i.e., activity values, were calculated as the difference between consecutive measurements, averaged over a time interval of 4 or 5 minutes and given within a relative range between 0 (no difference between consecutive data) and 255 (difference of -2 g/+2 g), with the associated date and time. The activity data recorded were downloaded by means of a handheld terminal (Vectronic Aerospace GmbH, Berlin) and Yagi antenna.

Weather and Astronomical Data: Weather data such as hourly air temperature (°C) and hourly precipitation (i.e., the amount of rain expressed in millimetres of water) were provided by Meteorological Service of Regione Autonoma Valle d’Aosta (weather station of Pont, 45° 31′ N, 7° 12′ E; 1951 m a.s.l.) and by the Federal Office for Meteorology and Climatology (weather station of Samedan, 46° 31′ N; 9° 52′ E; 1710 m a.s.l.), for the GPNP and SNP study areas, respectively. We a priori chose to use temperature rather than radiation (which are highly correlated) because previous research suggested that air temperature was the main driver affecting ibex spatial choices (Brivio et al. 2019). Moon illumination was calculated using the suncalc package in R (Thieurmel and Elmarhraoui 2019) and was expressed as the illuminated fraction of the moon, which ranged from 0.0 (new moon) to 1.0 (full moon). Cloud cover estimates were downloaded from the NCEP/NCAR data set (Kalnay et al. 1996) by using the interpolation method “Inverse Distance Weighting” (Shepard 1968) by means of the NCEP.interp function in the RNCEP package in R (Kemp et al. 2012). Cloud cover data was expressed as the percentage of sky covered by clouds and had a spatial and temporal gridded resolution of 2.5° and 6 hours, respectively. In our analyses, only cloud cover data recorded at 00.00 AM were used.

活动时间的灵活性可帮助生物体快速适应环境变化。在全球变暖背景下，日行性恒温动物可通过将活动时段调整至更为凉爽的夜间，以获得更优的能量平衡。然而这一行为转变可能会使动物面临全新或加剧的环境挑战，例如捕食风险升高、觅食效率降低。本研究分析了来自两个保护区的47只北山羊（ibex，*Capra ibex*）的大型活动数据集，这两个保护区的捕食风险水平存在差异，即存在灰狼（Canis lupus）与无灰狼。研究发现，北山羊在气温较高的次日以及夜间光照更强的时段会增加夜间活动比例。尽管该物种存在显著的性别二态性，且由此导致雌雄个体对捕食风险的感知存在差异，但无论在有捕食者还是无捕食者的区域，雌雄个体对高温均表现出一致的响应。这一结果支持了“日行性恒温动物为应对全球变暖，或将活动时段调整至夜间作为通用策略”的假说。当前多重压力正推动哺乳动物转向夜行性，本研究结果强调，亟需将时间行为可塑性相关知识纳入野生动物管理与保护规划之中。

Methods

### 活动数据记录
研究通过项圈搭载的双轴运动传感器（加速度计，accelerometer）记录个体北山羊的活动数据：大帕拉迪索国家公园（GPNP）内18只雄性、9只雌性，斯图尔维亚自然公园（SNP）内12只雄性、8只雌性，详细信息见补充材料表S1与表S2。该加速度计可同时沿两个正交方向测量项圈所感知到的运动相关加速度变化：X轴可检测前后方向的加速度事件，Y轴则记录侧向与旋转方向的加速度事件。该加速度计的动态范围为±2g，以4Hz的频率采集静态加速度（重力）与动态加速度（项圈运动）的变化值，并将活动量计算为连续两次测量值的差值，随后在4或5分钟的时间区间内取平均，最终活动量取值范围为0（连续数据无差异）至255（差值为-2g至+2g），并同步记录关联的日期与时间。研究通过手持终端（Vectronic Aerospace GmbH，柏林）与八木天线下载采集得到的活动数据。

### 气象与天文数据
针对大帕拉迪索国家公园（GPNP）与斯图尔维亚自然公园（SNP）两个研究区域，研究分别使用瓦莱达奥斯塔自治区气象服务局（位于蓬特的气象站，45°31′N，7°12′E，海拔1951米）与瑞士联邦气象与气候局（位于萨梅丹的气象站，46°31′N，9°52′E，海拔1710米）提供的逐小时气温（℃）与逐小时降水量（以毫米水深表示的降雨量）数据。本研究预先选择气温而非辐射（二者相关性极高）作为分析变量，原因是既往研究表明气温是影响北山羊空间选择的主要驱动因子（Brivio等，2019）。
月相照度通过R语言的suncalc包计算（Thieurmel与Elmarhraoui，2019），以月球被照亮的比例表示，取值范围为0.0（新月）至1.0（满月）。云量数据通过RNCEP包（Kemp等，2012）中的NCEP.interp函数，采用“反距离加权”插值方法（Shepard，1968），从NCEP/NCAR数据集（Kalnay等，1996）中获取。云量以天空被云覆盖的百分比表示，空间与时间格点分辨率分别为2.5°与6小时。本研究仅采用每日00:00记录的云量数据用于后续分析。