Nesting White Ibis prey use in Everglades National Park in 2017 and 2018

As avian reproductive success is generally prey limited, identifying important prey types or sizes, and understanding mechanisms governing prey availability are important objectives for avian conservation ecology. Irruptive White Ibis (Eudocimus albus) nesting at coastal colonies in the southern Everglades numbered over 100,000 nests in the 1930s. A century of drainage and altered hydrologic patterns reduced aquatic prey availability and eliminated large nesting events; nesting activity in recent decades has been typically <5% of historical peaks. Hydrologic restoration is expected to increase ibis nesting activity, but which prey types will support high nesting effort is less clear. In 2017 and 2018 we collected food boluses from White Ibis chicks at coastal colonies in Everglades National Park. We also monitored regional nesting activity from 1999-2018. In 2017 the region had 1,075 nests, typical of the past several decades, but in 2018 there were 30,420 nests, representing the highest recorded nesting activity in 87 years. Prey composition varied between years; estuarine crabs dominated nestling boluses in 2017 while crayfish and fish were dominant prey in 2018. Crayfish, especially Procambarus alleni, were heavily exploited by ibis early in the 2018 breeding season while fish were used more at the end. Crayfish abundances in wetlands near the colonies were higher prior to 2018, and more crayfish-producing short-hydroperiod wetlands remained available for ibis foraging in 2018. Our results support previous studies indicating that crayfish are important prey for breeding ibises and suggest that unprecedented, extensive flooding of seasonal wetlands promoted crayfish production and initiated the irruptive breeding in 2018. Our observations indicate re-hydration of the southern Everglades could restore ibis nesting activity at coastal colonies, but further investigations of hydrologic variation, crayfish production, and ibis foraging and nesting activity will be helpful to understand these dynamics and the importance of short-hydroperiod wetlands.

Methods
Prey composition of White Ibis nesting in Everglades National Park in 2017 and 2018 

We quantified prey use of ibises nesting in the ecotone of Everglades National Park in 2017 and 2018 by examining the contents of regurgitated food boluses collected from nestlings. We collected boluses weekly for ~5 weeks each year during the peak provisioning period when chicks are between 12 and 28 days old. Most boluses (~90%) were collected from the ground or nesting substrates following voluntary regurgitation and the rest were collected via esophageal massage.Each bolus was picked through twice, and all useful prey parts were recorded, counted, and sorted into vials of 70% ethanol similar to methods used in previous diet studies (Boyle et al. 2014). We measured lengths of prey parts and back-calculated dry masses of fish and most invertebrates with regressions developed for previous assessments of ibis diets (Boyle et al. 2014).

White Ibis nesting activity

We conducted aerial surveys of nesting ibis at seven historical colonies in the ecotone of Everglades National Park from 1999 and 2018. We monitored active nesting colonies monthly from January through June using fixed-winged aircraft and helicopters flown at an altitude of 150-250 meters above ground level. During each flight, we took photos of the entire colony using a high-resolution DSLR camera and telephoto lens. We examined the photos to determine the stage of nesting and number of nests. We counted nests during the incubation stage, when the white incubating adult could be detected against the darker background of the nesting colony; we assumed each horizontally sitting (incubating) adult equated to one nest. We estimated total nest counts by rounding the number of nests up to the nearest 5, 50, or 100 nests for colonies with <100, 100-1000, and >1000 nests, respectively. We used the total nest count for each colony as a measure of colony-level nesting effort. We summed total nest counts for all colonies in the ecotone each year to examine temporal trends of total nesting effort in the coastal ecotone of Everglades National Park.

Crayfish Production

We quantified wet-season crayfish (Procambarus alleni and P. fallax, combined) catch rates at five spatially-fixed sampling sites in marl prairies and sloughs east of the colonies in each October preceding the 2017 and 2018 dry seasons (i.e. October 2016 and 2017). At each of the five sites we set six non-baited minnow traps (three 3.0 mm and three 6.4 mm wire mesh traps) for 22-24 hr. We considered the aggregate catch of six traps at each site a single effort. Crayfish were identified to species and measured (mm carapace length), and dry weights were calculated using length-weight regressions (Boyle et al. 2014). We compared mean crayfish catch rates (crayfish effort−1) and biomass (g dry mass effort−1) between 2016 and 2017 with paired one-tailed t-tests. Crayfish biomasses were natural log transformed to help meet assumptions of the analyses.

由于鸟类繁殖成功率通常受猎物资源限制，识别关键猎物类型与体型，以及理解调控猎物可获得性的机制，是鸟类保护生态学的重要研究目标。曾在大沼泽地南部沿海筑巢群落繁殖的美洲白鹮（White Ibis，*Eudocimus albus*），在1930年代的筑巢数量超过10万巢。一个世纪以来的排水工程与水文格局改变，大幅降低了水生猎物可获得性，彻底终止了大规模筑巢事件；近数十年的筑巢活动通常仅为历史峰值的5%以下。尽管水文修复有望提升美洲白鹮的筑巢活动，但何种猎物能够支撑高强度筑巢努力仍不明确。

2017与2018年，我们在大沼泽地国家公园（Everglades National Park）的沿海群落中，从美洲白鹮雏鸟体内收集反刍食团（regurgitated food boluses）。同时我们于1999-2018年监测了区域筑巢活动。2017年该区域筑巢数量为1075巢，与过去数十年的水平一致；但2018年筑巢数量达到30420巢，为87年来有记录以来的最高筑巢活动水平。两年间猎物组成存在显著差异：2017年雏鸟食团以河口蟹类为主，而2018年的优势猎物为螯虾与鱼类。2018年繁殖季早期，美洲白鹮大量捕食螯虾（尤以佛罗里达螯虾*Procambarus alleni*为甚），繁殖季后期则更多依赖鱼类。筑巢点附近湿地的螯虾丰度在2018年之前较高，且2018年可供白鹮觅食的短水文周期螯虾生产湿地留存更多。

我们的研究结果支持此前的结论，即螯虾是繁殖期美洲白鹮的重要猎物，同时表明季节性湿地前所未有的大规模淹水促进了螯虾种群繁殖，并触发了2018年的爆发式繁殖（irruptive breeding）。本研究结果显示，大沼泽地南部的水文恢复有望恢复沿海群落的美洲白鹮筑巢活动，但未来仍需进一步研究水文变化、螯虾种群繁殖，以及美洲白鹮的觅食与筑巢活动，以深入理解这些动态过程与短水文周期湿地的重要性。

## 方法

### 2017与2018年大沼泽地国家公园美洲白鹮筑巢的猎物组成
我们通过分析从雏鸟身上收集的反刍食团内容物，量化了2017与2018年大沼泽地生态交错带筑巢美洲白鹮的猎物利用情况。在雏鸟12至28日龄的核心育雏期，我们每年每周收集食团，持续约5周。多数食团（约90%）为雏鸟自愿反刍后从地面或筑巢基质上收集，剩余食团通过食道按摩（esophageal massage）获取。每份食团经两次分拣，记录并计数所有可识别的猎物部位，随后装入70%乙醇溶液的样本瓶中，该方法参考了此前美洲白鹮食性研究的流程（Boyle等，2014）。我们测量了猎物部位的长度，并通过此前针对美洲白鹮食性评估建立的回归方程，反推得到鱼类与多数无脊椎动物的干重（dry mass，Boyle等，2014）。

### 美洲白鹮筑巢活动监测
我们于1999至2018年，对大沼泽地生态交错带的7处历史筑巢群落开展航空调查。每年1月至6月，我们使用固定翼飞机与直升机，在海拔150-250米的高度每月监测活跃筑巢群落。每次飞行中，我们使用高分辨率数码单反相机与长焦镜头拍摄整个群落的全貌。通过分析照片确定筑巢阶段与巢的数量：在孵化期，白色的孵卵成鸟可与筑巢群落深色背景形成鲜明对比，此时我们计数巢的数量，并假设每只水平趴卧（孵卵）的成鸟对应1个巢。对于巢数<100、100-1000、>1000的群落，我们分别将巢数向上取整至最接近的5、50或100。我们以每个群落的总巢数作为群落水平筑巢努力的衡量指标，每年将所有群落的总巢数求和，以分析大沼泽地沿海交错带总筑巢努力的时间变化趋势。

### 螯虾种群繁殖量评估
我们分别在2017与2018年旱季之前的10月（即2016与2017年10月），在筑巢点东侧的泥灰岩草原（marl prairies）与滞水沼泽（sloughs）的5个固定采样点，量化了湿季螯虾（佛罗里达螯虾*Procambarus alleni*与光滑螯虾*Procambarus fallax*合并统计）的捕获率。在每个采样点，我们放置6个无诱饵的小鱼诱捕笼（minnow traps，3个网孔直径3.0mm、3个6.4mm的金属网诱捕笼），放置时长为22-24小时。我们将每个采样点6个诱捕笼的总捕获量视为单次采样 effort。螯虾鉴定至物种水平，测量其甲壳长度（carapace length，mm），并通过体长-体重回归方程计算干重（Boyle等，2014）。我们使用配对单尾t检验（paired one-tailed t-tests），比较2016与2017年的平均螯虾捕获率（单位effort的螯虾数量）与生物量（单位effort的干重克数）；为满足分析假设，我们对螯虾生物量数据进行了自然对数转换（natural log transformed）。