Rainfall and nest site competition delay Mountain Bluebird and Tree Swallow breeding but do not impact productivity

AbstractOptimizing breeding phenology, an important aspect of fitness, is complex for migratory species as they must make key timing decisions early, and remotely, from breeding sites. We examined the role of weather (locally and cross-seasonally), cavity availability, and competitive exclusion in determining among-year variation in breeding phenology over 17 years for two migratory, cavity-nesting birds: Mountain Bluebirds (Sialia currucoides; n = 462 nests) and Tree Swallows (Tachycineta bicolor; n  = 572) using natural tree cavities in British Columbia, Canada. We assessed weather effects within the winter and migratory range and at our study sites. We quantified competition as the proportion of cavities occupied by European Starlings (Sturnus vulgaris) (for both species) and Mountain Bluebird (for Tree Swallow only) in each year. For 229 bluebird and 177 swallow nests with known fates, we tested whether late years resulted in reduced productivity. Although the effects were small, heavy rainfall and strong diurnal westerly winds during migration were associated with breeding delays for Mountain Bluebirds. However, cavity availability (earlier breeding with increases) had a 5-8X greater effect on timing than migratory conditions. There was no evidence that starling competition delayed bluebirds. In Tree Swallows, greater local daily rainfall was associated with delayed breeding, as was starling abundance (the effect of starlings was 1.4X times smaller than that of rainfall). Neither bluebird abundance nor cavity availability changed swallow phenology. Neither species showed reduced productivity in late breeding years. In both species, individuals that bred late relative to conspecifics within-year had smaller clutches and greater probability of nest failure.  We conclude that breeding ground conditions, particularly cavity limitation and local rainfall (for swallows), are important drivers of breeding phenology for our focal species, but that the productivity cost of late years, at least for Tree Swallows, is minimal. , MethodsPlease see associated manuscript for complete methodologies (Drake and Martin 2020) Winter and migration weather data source: The NCEP/NCAR 40-Year Reanalysis Project: March, 1996 BAM; NOAA National Center for Environmental Prediction Reanalysis I Breeding site weather data source: Environment and Climate Change Canada weather station Williams Lake A (WMO ID 71104; 52.1800N, 122.0500W; elevation 939.7m; http://climate.weather.gc.ca) Field data notes: Breeding data for Mountain Bluebird and Tree Swallow were collected between 1995 and 2011 at two study sites ~38 km apart, “Riske Creek” (52.0025°N, 122.4116°W) and “Knife Creek” (52.0068°N, 121.8619°W), near Williams Lake in south-central British Columbia, Canada. This region is part of the warm and dry Interior Douglas-fir biogeoclimatic zone. In this study, the Riske Creek site consisted of 16 mixed conifer stands (Douglas-fir (Pseudotsuga menziesii var. menziesii ), lodgepole pine (Pinus contorta var. latifolia), and white and Englemann spruce hybrids (Picea glauca x engelmannii )) with trembling aspen (Populus tremuloides) within a grassland-wetland matrix. Knife Creek consisted of 11 mixed conifer stands with some deciduous riparian zone. Stands ranged from 7-32 ha in size. No nest boxes were present at either site and all nesting was done in natural tree cavities. Mountain Bluebird and Tree Swallow were two of a total of 32 cavity-nesting bird species found within the study sites over the monitoring period (Wesolowski and Martin 2018). During the 1995 to 2011 period, systematic searches were conducted between May 1 and July 31. These surveys were conducted for approximately 6–7 h/stand/week by walking the entirety of each stand and examining previously identified nest-sites and following birds (Aitken and Martin 2007). The number of stands monitored increased between 1995 and 1998, but thereafter survey effort was equivalent. The majority of nests were found in the laying or early incubation stage (Koch et al. 2012).  Active nesting cavities were identified based on adult behaviour (carrying nesting material/food or entering/exiting cavities) or the vocalizations of young (Martin et al. 2004). All cavities at the study site were given unique identifiers and their persistence and use was recorded in each year of the study. Between 1995 and 2004, we accessed active cavities up to 5.2m above the ground using ladders and mirrors to assess the stage of breeding. One hundred and twelve nests (10% of the total dataset) were inaccessible during this 10-year period. These inaccessible cavities were recorded as active based on adult behaviour or begging chicks but could not be assigned a clutch initiation date or hatch date in the field. After 2004, all nests were accessible using a video camera mounted on a pole (TreeTop Peeper; Sandpiper Technologies, Manteca, CA, USA) to identify the stage of breeding in cavities up to 15m above the ground (Edworthy et al. 2012). Nests were checked, on average, every 5 days during their active phase and, when possible, clutch initiation date was determined using observed clutch size (if nests were found during laying) or observed final clutch size and hatch date (if nests were found during incubation), combined with a 1 egg/day laying interval and a 14- or 15-day mean incubation period for Mountain Bluebird and Tree Swallow, respectively (Koch et al. 2012). Nesting attempts found after young had hatched were not assigned a clutch initiation date in the field. Nest activity periods were recorded as the first and last days that each cavity was observed as actively being used (containing fresh nesting material, eggs, or nestlings). The number of fledglings produced by each nest was recorded when fledging was observed or when chicks were old enough at the last nest check to survive out of the nest and where there was no evidence of predation within the cavity or around the nesting site when the nest was found empty at the penultimate check. The presence of adults feeding chicks in the immediate nest area was also used as an indicator of success where fledging was not directly observed., Usage notesPlease see associated manuscript for complete methodologies (Drake and Martin 2020)

摘要

优化繁殖物候（breeding phenology）——适合度（fitness）的核心组成部分——对于迁徙物种而言极具复杂性，因为它们必须早早地在远离繁殖地的位置做出关键的时间决策。本研究针对两种迁徙性树洞筑巢鸟类，基于加拿大不列颠哥伦比亚省17年的监测数据，探究了天气（局地与跨季节）、树洞可获得性以及竞争排除对繁殖物候年际变化的影响：山蓝鸲（Mountain Bluebird, Sialia currucoides；n=462个巢）与树燕（Tree Swallow, Tachycineta bicolor；n=572个巢），所有巢均为天然树洞巢。

我们分别评估了越冬与迁徙路径范围内的天气，以及研究样地的天气对繁殖物候的作用。我们以每年被欧椋鸟（European Starlings, Sturnus vulgaris，两种鸟类的竞争者）以及山蓝鸲（仅针对树燕）占据的树洞比例量化竞争程度。针对229个已知繁殖结局的山蓝鸲巢与177个已知结局的树燕巢，我们检验了繁殖延迟年份是否会降低繁殖生产力。

尽管影响幅度较小，但迁徙途中的强降雨与昼间西风与山蓝鸲的繁殖延迟相关。然而，树洞可获得性（树洞越多，繁殖越早）对繁殖时间的影响是迁徙条件的5-8倍。尚无证据表明欧椋鸟的竞争会延迟山蓝鸲的繁殖。对于树燕而言，更高的局地日降雨量与繁殖延迟相关，欧椋鸟的种群丰度同样会导致繁殖延迟（欧椋鸟的影响强度是降雨的1/1.4）。山蓝鸲的种群丰度与树洞可获得性均未改变树燕的繁殖物候。两个物种在繁殖延迟年份均未出现繁殖生产力下降的情况。在同一年份内，相较于同种个体繁殖较晚的个体，其窝卵数更少，巢失败概率更高。

综上，繁殖地条件——尤其是树洞限制与树燕面临的局地降雨——是本次研究物种繁殖物候的重要驱动因素，但至少对于树燕而言，繁殖延迟带来的生产力成本极低。

# 研究方法

完整研究方法请参见相关论文（Drake and Martin 2020）。

越冬与迁徙天气数据来源：NCEP/NCAR 40年再分析项目（The NCEP/NCAR 40-Year Reanalysis Project）：1996年3月，BAM；美国国家海洋和大气管理局（NOAA）国家环境预报中心再分析数据集I（NOAA National Center for Environmental Prediction Reanalysis I）。

繁殖样地天气数据来源：加拿大环境与气候变化部威廉姆斯湖A气象站（Environment and Climate Change Canada weather station Williams Lake A；WMO编号71104；52.1800°N，122.0500°W；海拔939.7m；http://climate.weather.gc.ca）。

野外数据说明：山蓝鸲与树燕的繁殖数据采集于1995年至2011年，位于加拿大不列颠哥伦比亚省中南部威廉姆斯湖附近的两个样地，两地相距约38公里：里斯克溪（Riske Creek；52.0025°N，122.4116°W）与奈夫溪（Knife Creek；52.0068°N，121.8619°W）。该区域属于温暖干燥的内陆道格拉斯冷杉生物气候区。

本研究中，里斯克溪样地包含16个混合针叶林林分，优势树种为道格拉斯冷杉（Pseudotsuga menziesii var. menziesii）、黑松（Pinus contorta var. latifolia）以及白云杉与恩氏云杉的杂交种（Picea glauca x engelmannii），林分内嵌有美洲山杨（Populus tremuloides），整体处于草原-湿地基质中。奈夫溪样地包含11个混合针叶林林分，附带部分落叶河岸带。林分面积介于7-32公顷之间。两个样地均未设置人工巢箱，所有筑巢行为均发生在天然树洞中。

监测期间，研究样地共记录到32种树洞筑巢鸟类，山蓝鸲与树燕为其中两种（Wesolowski and Martin 2018）。1995年至2011年间，系统调查于每年5月1日至7月31日开展。调查人员遍历每个林分，检查已确认的巢址并追踪鸟类，每周对每个林分开展约6-7小时的调查（Aitken and Martin 2007）。1995年至1998年间，监测林分数量逐步增加，此后调查投入保持一致。大多数巢在产卵期或孵化早期被发现（Koch et al. 2012）。

活跃筑巢树洞的识别依据包括成鸟行为（携带筑巢材料/食物或进出树洞）或是幼鸟的鸣叫声（Martin et al. 2004）。所有研究样地的树洞均被赋予唯一标识符，并在每年的研究中记录其留存与使用情况。1995年至2004年间，我们使用梯子与反光镜探查距离地面最高5.2米的活跃树洞，以评估繁殖阶段。这10年间共有112个巢（占总数据集的10%）无法被直接探查。这些无法探查的树洞依据成鸟行为或是幼鸟乞食声被判定为活跃巢，但无法在野外确定其产卵起始日期与出雏日期。2004年后，我们使用安装在长杆上的摄像机（TreeTop Peeper；Sandpiper Technologies，美国加利福尼亚州曼蒂卡市），可探查距离地面最高15米的树洞以确定繁殖阶段（Edworthy et al. 2012）。

繁殖活跃期内，平均每5天检查一次巢。若巢在产卵期被发现，则通过观察到的窝卵数确定产卵起始日期；若巢在孵化期被发现，则结合每日产1枚卵的产卵间隔，以及山蓝鸲与树燕分别平均14天、15天的孵化期，通过最终窝卵数与出雏日期推算产卵起始日期（Koch et al. 2012）。幼鸟出壳后才被发现的巢，无法在野外确定其产卵起始日期。巢活动周期记录为每次观察到树洞被活跃使用的首日与末日（巢内存在新鲜筑巢材料、卵或雏鸟）。

每个巢的出飞幼鸟数量，通过直接观察出飞情况，或是在倒数第二次巢检查时发现巢空且无捕食证据的前提下，结合最后一次巢检查时雏鸟的日龄（已足够离巢存活），以及成鸟在巢区附近喂食雏鸟的行为（未直接观察到出飞时的判定依据）进行记录。

# 使用说明

完整研究方法请参见相关论文（Drake and Martin 2020）