城市化对当地生态系统的结构、功能和物种组成等产生了严重影响, 并对生物多样性形成了巨大威胁(Wang et al, 2012; Nilon et al, 2017)。为了满足城市建设和居民需求, 城市地区的自然生境逐渐被人工设施取代, 通常会导致生物多样性的降低(Whitford et al, 2001; Grimm et al, 2008)。生物多样性是人类赖以生存的基本条件(侯东敏等, 2023), 影响着居民生活质量和社会经济发展(Dearborn & Kark, 2010; Fontana et al, 2011)。随着城市人口的增长, 人类对生态系统服务产生越来越大的需求(Grimm et al, 2008), 保护、恢复和提高城市生物多样性受到社会各界的重视(Savard et al, 2000)。鸟类是城市中最常见的野生动物(Shwartz et al, 2014), 也是对环境变化最敏感和最易受干扰的类群之一(Sulaiman et al, 2013), 可以作为评价城市环境质量和生物多样性的指示类群(张征恺和黄甘霖, 2018)。鸟类对栖息地组成和结构的变化非常敏感(Clergeau et al, 1998; Chace & Walsh, 2006), 城市化过程中栖息地的改变是鸟类种群数量下降的主要原因(Kemp, 2004)。园林植物是城市鸟类栖息地的重要组成部分, 为其提供了城市环境下的生存条件, 其合理配置有助于保护城市鸟类多样性, 提高城市生态环境质量(Sulaiman et al, 2013; Threlfall et al, 2016; Aronson et al, 2017)。
本土植物(native plants)是指在新石器时代之前就分布在该地区的植物, 或是新石器时代之后通过完全独立于人类活动的方法到达该地区的植物; 外来植物(alien plants)是指新石器时代及之后由于人类或家畜的活动而到达该地区的植物(Webb, 1985; Pyšek, 1998), 即在原分布范围以外栽植、直接或间接引进、或没有人类活动就不能定殖的物种。城市环境的高度异质性以及外来植物的引入在一定程度上提高了植物的密度和物种丰富度, 并塑造了城市植物的多样性(Grimm et al, 2008; Wang et al, 2012)。在城市化过程中, 本土植物经常被移除或被外来植物所取代(Blair, 1996; Millard, 2008; Szlavecz et al, 2011), 外来植物在几乎所有城市中均占有相当大的比例(Zhao et al, 2010; Potgieter et al, 2017), 其种类与数量随着城市化的加剧明显增多(Pyšek, 1998; Williams et al, 2009)。为了改善城市环境、提高居民生活质量、促进社会经济发展, 许多外来植物被引入城市, 在营造城市生态环境中发挥了重要作用(Dwyer et al, 1992; Wang et al, 2012; Potgieter et al, 2017), 同时为城市鸟类提供了重要的栖息环境。但是, 在城市园林建设过程中, 许多园林绿化工程只注重视觉效果, 未考虑鸟类对栖息环境的需求(王绪平等, 2007)。如何改善城市鸟类栖息环境, 提高鸟类多样性, 已成为城市园林建设中关注的重要问题(Fontana et al, 2011)。北京在城市化和园林建设过程中, 本土植物不断减少, 外来植物逐渐占据主导地位(Liang et al, 2008), 全部园林植物中近一半为外来物种(Wang GM et al, 2007; 赵娟娟等, 2009; Wang HF et al, 2012)。研究北京城市鸟类对园林植物的利用, 有助于全面了解城市鸟类的栖息环境, 对城市生物多样性的保护至关重要(Jirinec et al, 2016; Moraes et al, 2018; Pei et al, 2018)。
夜栖地(night roosting site)是动物夜间栖息的场所, 也是动物栖息地的重要组成部分(原宝东等, 2012)。城市生态系统中, 园林植物为许多鸟类提供了夜栖环境, 种植适合鸟类夜栖的园林植物对于保障鸟类安全夜栖至关重要(Buttemer, 1985; Watts et al, 2021)。目前国内外已有一些关于鸟类夜栖地的报道, 如黑颈鹤(Grus nigricollis)①( ① 孙喜娇 (2018) 草海湿地黑颈鹤越冬期夜栖行为与夜栖地生境选择研究. 硕士学位论文, 贵州大学, 贵州.)、白冠长尾雉(Syrmaticus reevesii) (孙全辉等, 2002)、北美金翅雀(Carduelis tristis) (Buttemer, 1985)、黑腹滨鹬(Calidris alpina pacifica) (Conklin & Colwell, 2007)等, 但大多集中在非城市环境栖息的单一物种上(Mitchell & Clarke, 2019), 大型城市中在群落水平上对鸟类夜栖地的研究非常缺乏。本研究将探究城市夜栖鸟类对北京市本土植物和外来植物的利用差异, 以期为华北地区城市鸟类的夜栖环境建设提供参考依据。
1 研究地点与研究方法
1.1 研究地点
公园绿地和大学校园均为城市鸟类的主要栖息地, 是开展鸟类研究的理想场所(杨刚等, 2015; 郝晟等, 2021)。本研究选取植物种类丰富、鸟类多样性较高的奥林匹克森林公园和北京林业大学为研究地点(图1)。奥林匹克森林公园占地约680 ha, 为北京市最大的公共公园(胡洁等, 2006)。园内植物多样性较高, 种数超过北京城区的一半, 共有75科203属295种, 其中本土植物179种, 外来植物116种(余琦殷等, 2012)。北京林业大学植物种类丰富, 曾被评为“全国绿化先进单位” (胡楠等, 2018), 共有植物59科134属267种(
图1
图1
北京林业大学(A)及奥林匹克森林公园(B)夜栖植物分布图
Fig. 1
Distribution of night roosting plants in Beijing Forestry University (A) and Olympic Forest Park (B)
1.2 数据收集
2021年4月至2022年3月, 对研究地点的夜栖鸟类进行观察记录。调查于日落2小时后开始, 每次调查2-4 h, 每周调查1-2次。使用艾睿E2n红外热成像仪搜寻调查地点的乔木和灌丛。发现夜栖鸟类后, 使用沃尔森H9002手电筒和沃尔森X50 T6变焦手电筒照射并通过博冠乐观8 × 42双筒望远镜观察, 确定物种及数量。使用徕卡D3a激光测距仪和胸径尺测量乔木的胸径、树高、冠幅, 灌木的长度、宽度、高度, 鸟类的栖枝高度。使用手持GPS记录夜栖植物的经纬度并对其进行编号。沿调查轨迹记录两侧20 m内植物的种类和数量, 并依据Wang等(2012)对北京城市植物来源的划分, 将园林植物分为本土植物与外来植物。根据每种夜栖鸟类个体数量占总数量的比例, 将鸟类划分为优势种(> 10%)和非优势种(< 10%)。
1.3 数据分析
采用Shannon-Wiener多样性指数计算夜栖鸟类多样性及夜栖植物多样性。为防止数量较多的优势种对研究结果影响过大而导致忽视数量较少的鸟类对夜栖植物的利用, 采用稀有度加权丰富度(rarity-weighted richness, RWR)确定关键夜栖植物。其计算过程分为两步: (1)通过鸟类利用夜栖植物种数的倒数计算得到各种鸟类的稀有度(如灰喜鹊 Cyanopica cyanus)利用29种植物夜栖, 稀有度为1/29), 仅利用1种植物夜栖的鸟类稀有度最高, 利用夜栖植物种类最多的鸟类稀有度最低; (2)夜栖植物的稀有度加权丰富度为所有利用其夜栖的鸟类的稀有度之和(Williams et al, 1996; Albuquerque et al, 2019)。计算公式如下:
其中, Ti为鸟类i夜栖时利用植物种类的数量, n为利用该植物夜栖的鸟类数量。
使用χ2检验分析夜栖鸟类对调查轨迹两侧20 m内本土植物和外来植物的利用是否存在显著差异。使用Kolmogorov-Smirnov正态分布检验胸径、树高、冠幅及鸟类的栖枝高度是否为正态分布。当P值大于0.05时为正态分布, 采用单因素方差分析(one-way ANOVA)进行差异性分析。反之则为非正态分布, 采用Kruskal-Wallis检验进行差异性分析。使用Spearman相关分析检验胸径、树高、冠幅之间的相关性。使用偏相关分析检验栖枝高度与胸径、树高、冠幅之间的相关性。使用R软件lme4程序包的glmer函数(Bates et al, 2015), 分别采用具有二项分布及Gamma分布的广义线性混合模型分析不同季节夜栖鸟类对植物来源及胸径、树高、冠幅、栖枝高度的利用差异。分别将植物来源及胸径、树高、冠幅、栖枝高度作为响应变量, 季节作为固定变量, 鸟类物种作为随机变量进行分析。使用emmeans程序包的emmeans函数进行事后分析(Lenth, 2022)。本文所有统计分析均在R 4.4.1中完成(R Core Team, 2021)。
2 结果
2.1 夜栖鸟类与夜栖植物
共记录夜栖鸟类3目12科23种1,865只次, 夜栖植物22科34属45种(图2)。夜栖鸟类中优势种为灰喜鹊、麻雀(Passer montanus)、喜鹊(Pica pica)和珠颈斑鸠(Streptopelia chinensis), 其总数量占全部夜栖鸟类的84.72%; 其他19种鸟类为非优势种, 共占15.28%。利用夜栖植物种类最多的鸟类为灰喜鹊(29种), 之后依次为麻雀(27种)、喜鹊(26种)、珠颈斑鸠(23种)、乌鸫(Turdus mandarinus, 12种)、白头鹎(Pycnonotus sinensis, 8种)、黑尾蜡嘴雀(Eophona migratoria, 4种)等(图3)。利用夜栖植物多样性(Shannon-Wiener指数)最高的鸟类为灰喜鹊(2.504), 之后依次为麻雀(2.341)、珠颈斑鸠(2.282)、喜鹊(2.175)、乌鸫(1.619)、白头鹎(1.251)、山斑鸠(Streptopelia orientalis, 1.099)等。
图2
图2
夜栖鸟类与夜栖植物的关系。左侧鸟类名后的数字表示记录到此夜栖鸟类的个体数量, 右侧植物名前的数字表示夜栖于该种植物的鸟类个体数量。线条的宽度表示鸟类数量, 鸟类个体数量越多, 线条越宽。
Fig. 2
The relationship between night-roosting birds and plants. The number after the name of the bird on the left indicates the number of individuals recorded to this night-roosting bird. The number before the name of the plant on the right indicates the number of individual birds nocturnally inhabiting the plant. The width of the line indicates the number of birds, and the wider the line, the greater the number of birds.
图3
图3
夜栖鸟类利用植物种数。1: 灰喜鹊; 2: 麻雀; 3: 喜鹊; 4: 珠颈斑鸠; 5: 乌鸫; 6: 白头鹎; 7: 黑尾蜡嘴雀; 8: 山斑鸠; 9: 燕雀; 10: 北灰鹟; 11: 赤颈鸫; 12: 红喉姬鹟; 13: 红尾斑鸫; 14: 红胸姬鹟; 15: 虎斑地鸫; 16: 灰背鸫; 17: 灰椋鸟; 18: 家燕; 19: 煤山雀; 20: 乌鹟; 21: 沼泽山雀; 22: 棕头鸦雀; 23: 纵纹腹小鸮。
Fig. 3
Number of plant species used by night-roosting birds. 1, Cyanopica cyanus; 2, Passer montanus; 3, Pica pica; 4, Streptopelia chinensis; 5, Turdus mandarinus; 6, Pycnonotus sinensis; 7, Eophona migratoria; 8, Streptopelia orientalis; 9, Fringilla montifringilla; 10, Muscicapa dauurica; 11, Turdus ruficollis; 12, Ficedula albicilla; 13, Turdus naumanni; 14, Ficedula parva; 15, Zoothera aurea; 16, Turdus hortulorum; 17, Spodiopsar cineraceus; 18, Hirundo rustica; 19, Periparus ater; 20, Muscicapa sibirica; 21, Poecile palustris; 22, Sinosuthora webbiana; 23, Athene noctua.
夜栖植物中, 本土植物14种(占全部夜栖植物种类的31.11%), 外来植物31种(占68.89%) (图2)。在调查轨迹两侧20 m内的植物中, 本土植物数量占45.08%, 外来植物数量占54.92%。夜栖在本土植物上的鸟类数量占20.38%, 夜栖在外来植物上的鸟类数量占79.62%, 夜栖鸟类对本土植物和外来植物的利用存在显著差异(χ2 = 520.73, df = 1, P < 0.01)。非优势种(97.54%)对外来植物的利用显著多于优势种 (76.39%) (χ2 = 66.545, df = 1, P < 0.01)。夜栖鸟类利用最多的植物为圆柏(Juniperus chinensis, 22.47%), 之后依次为美国红梣(Fraxinus pennsylvanica, 17.75%)、早园竹(Phyllostachys propinqua, 8.42%)、一球悬铃木(Platanus occidentalis, 8.04%)、旱柳(Salix matsudana, 5.74%)、槐(Styphnolobium japonicum, 5.58%)、栾(Koelreuteria paniculata, 3.54%)等(图2)。吸引夜栖鸟类物种最多的植物为圆柏(13种), 之后依次为美国红梣(10种)、一球悬铃木(7种)、油松(Pinus tabuliformis, 7种)、刺槐(Robinia pseudoacacia, 6种)、早园竹(6种)、栾(6种)、榆树(Ulmus pumila, 6种)等(图2)。吸引夜栖鸟类物种多样性(Shannon-Wiener指数)最高的植物为圆柏(1.662), 之后依次为油松(1.649)、榆树(1.519)、一球悬铃木(1.484)、美国红梣(1.412)、刺槐(1.373)、杜仲(Eucommia ulmoides, 1.332)等。夜栖鸟类稀有度加权丰富度最高的植物为圆柏(5.445), 之后依次为美国红梣(2.945)、早园竹(2.745)、油松(2.237)、榆树(1.403)、栾(1.278)、槐(1.241)等。
胸径、树高、冠幅之间显著相关(P < 0.01)。偏相关分析显示, 栖枝高度与胸径无显著相关性(r = -0.025, df = 1,704, P = 0.307), 与树高(r = 0.442, df = 1,704, P < 0.01)和冠幅(r = 0.058, df = 1,704, P < 0.05)均呈显著正相关。本土植物的胸径、树高、冠幅以及夜栖鸟类的栖枝高度均显著大于外来植物(表1)。
表1 本土和外来夜栖植物的比较(Kruskal-Wallis检验) (平均值 ± 标准误)
Table 1
| 本土植物 Native plants | 外来植物 Alien plants | χ2 | P | |
|---|---|---|---|---|
| 胸径 Diameter at breast height (cm) | 39.28 ± 0.78 | 33.80 ± 0.52 | 71.115 | < 0.01 |
| 树高 Tree height (m) | 14.65 ± 0.15 | 12.84 ± 0.11 | 147.18 | < 0.01 |
| 冠幅 Canopy (m) | 10.44 ± 0.16 | 8.03 ± 0.11 | 167.71 | < 0.01 |
| 栖枝高度 Perch height (m) | 10.41 ± 0.15 | 8.46 ± 0.08 | 147.18 | < 0.01 |
2.2 鸟类对夜栖植物利用的季节差异
春季共记录夜栖植物28种, 其中本土植物7种, 外来植物21种。夏季共记录夜栖植物33种, 其中本土植物12种, 外来植物21种。秋季共记录夜栖植物24种, 其中本土植物8种, 外来植物16种。冬季共记录夜栖植物19种, 其中本土植物5种, 外来植物14种。鸟类在各个季节对不同来源植物的利用存在显著差异(Z = 3.331, P < 0.01), 冬季对外来植物的利用显著多于其他季节(P < 0.01) (图4)。夜栖植物的胸径(t = 7.612, P < 0.01)、树高(t = 5.116, P < 0.01)、冠幅(t = 5.219, P < 0.01)和夜栖鸟类的栖枝高度(t = 3.887, P < 0.01)均存在显著的季节差异。其中, 夜栖植物的胸径、树高和冠幅均表现为夏季最大(P < 0.01)且冬季最小(P < 0.01), 鸟类的栖枝高度表现为冬季显著低于其他季节(P < 0.05) (图5)。
图4
图4
各季节夜栖鸟类对本土和外来植物的利用比例
Fig. 4
Proportion of native and alien plants used by night-roosting birds in each season
图5
图5
各季节夜栖植物的胸径(A)、树高(B)、冠幅(C)和栖枝高度(D)
Fig. 5
Diameter at breast height (A), tree height (B), canopy (C) and perch height (D) of night roosting plants in different season
3 讨论及建议
园林植物不仅为城市居民提供了休闲娱乐的场所, 也为城市鸟类提供了重要的栖息环境(Davis & Glick, 1978)。城市园林中采用的外来植物会在一定程度上改变当地鸟类的群落结构(Shupova, 2021), 一些生态幅较广的鸟类可以很好地在城市中生存, 并形成较大的种群数量(Glazier, 1986)。研究中记录到的麻雀、灰喜鹊和喜鹊是夜栖鸟类优势种, 也是北京城市中数量最多的鸟类(张淑萍等, 2006; 郑冰晶和董丽, 2019), 夜栖时利用的植物种类最多, 利用的植物多样性也最高, 这说明了它们对城市园林环境具有较好的适应能力(张淑萍等, 2006; 鲍明霞等, 2019; 潘扬等, 2019)。我们的研究表明, 北京城市鸟类夜栖时除了利用槐、榆树、旱柳、栾等本土植物, 也利用大量外来植物, 如圆柏、美国红梣、一球悬铃木、早园竹、油松等(图2)。虽然一些研究表明, 大量外来植物的引入可能会影响整个生态系统的健康(彭少麟和向言词, 1999; Catling, 2005), 但在受人类行为严重干预的城市环境中, 原生植被已经被严重破坏, 园林建设中的外来植物形态多样, 且有一些常绿树种, 为夜栖鸟类提供了更加丰富的夜栖环境, 城市鸟类利用外来植物夜栖也是对城市化环境的适应。
夜栖状态下的鸟类会减少对外界刺激的回应(Webb, 1974), 对捕食者的反应速度也相应降低, 夜栖地的安全性成为影响鸟类对夜栖植物利用的重要因素(Amo et al, 2011)。夜栖在较高的栖枝上可以增大鸟类与地面行人及其他捕食者的距离(Peh & Sodhi, 2002), 有利于保障夜栖时的安全。我们的研究表明, 鸟类栖枝高度随植物树高、冠幅的增大而增加, 本土植物的树高和冠幅均显著大于外来植物(表1), 可以为鸟类提供更高的栖枝。鸟类通常会利用盖度较高和隐蔽性较好的植物夜栖, 减少被捕食者发现的几率(潘扬等, 2019)。冬季落叶前本土植物均枝叶繁茂, 可以在较高的位置为鸟类提供隐蔽的夜栖环境。
昼行性鸟类夜间依靠白天储存的能量维持正常生命活动, 保温性成为影响鸟类利用夜栖植物的另一个重要因素(Walsberg, 1986; Bonnet-Lebrun et al, 2020)。夏季气温较高, 鸟类夜栖时因散热而损失的能量较少(Bonnet-Lebrun et al, 2020), 而在温度较低的冬季, 鸟类夜栖时需要消耗大量能量维持体温, 此时夜栖植物的保温性对减少鸟类热量散失至关重要(Walsberg, 1986; Bonnet-Lebrun et al, 2020), 鸟类在冬季会偏向于利用郁闭度较高、保温性较好的植物夜栖(Buttemer, 1985; Thompson & Fritzell, 1988; Thiel et al, 2007)。圆柏、早园竹、油松及侧柏在北京城市鸟类冬季利用的植物中占较大比例, 且为外来植物(图2), 相对于其他落叶植物枝叶更加茂密, 能够有效地阻挡空气流动, 减缓散热速度, 为鸟类提供了更好的保温条件(Francis, 1976; Butte- mer, 1985; Walsberg, 1986)。
在进行以提高城市鸟类多样性为目的的园林建设时, 夏季夜栖植物可以选择保留或种植具有较大树高和冠幅的乔木, 冬季夜栖植物可以选择具有较大郁闭度的乔木或茂密灌丛, 为鸟类提供保温性能较好的夜栖环境。鸟类主要利用的植物中, 圆柏和油松吸引鸟类的数量、种类、物种多样性和稀有度加权丰富度均较高。虽然圆柏和油松在平原地区的城市环境中为人工种植的外来植物(Wang et al, 2012), 但在中国的中部和北部山区有自然分布(贺士元, 1992)。它们引入城市的时间较长, 对环境没有明显的不利影响。在城市园林建设中适度种植这两种植物, 可以在冬季为鸟类提供可利用的夜栖环境。但在非城市环境中, 仍建议采用本土植物, 以恢复平原地区的鸟类群落结构。
致谢
感谢复旦大学马志军教授、北京大学华方圆教授、中山大学马亮副教授、中国科学院动物研究所宓春荣和姜中文、北京林业大学张康情对本文提出的改进建议。感谢张晨曦、包瑞颖、托蕾、崔馨水和徐宁在数据收集过程中提供的帮助。
附录 Supplementary Material
附录1 红外热成像仪中的夜栖鸟类图像
Appendix 1 Images of night-roosting birds in the infrared thermal imager
附录2 夜栖鸟类图片
Appendix 2 Images of night-roosting birds
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DOI:10.1360/biodiv.060013
[本文引用: 2]
本文以北京市为例研究了城市化水平不同的8个区域中麻雀(Passer montanus的数量分布现状以及影响麻雀分布的栖息地因子。结果表明, 越冬期和繁殖期的麻雀数量均与城市化程度呈显著的负相关关系; 城市化程度高的城市中心商业区、高层居民区和城市主干道中的麻雀数量均很少; 城市化程度较低的城乡结合区、公园、城市的平房区及古建筑区域中麻雀数量均较多; 高校校园和低层楼房居民区, 虽然城市化程度相对较高, 但由于植被较丰富, 麻雀数量也较多。平房面积、针叶树数量、阔叶树数量、空调数量、高层楼房的面积、硬化地面的面积、人流量及车流量是影响麻雀栖息地利用的重要因素。其中平房面积、针叶树、阔叶树、空调的数量增加, 可为麻雀提供栖息条件而有利于麻雀的利用; 硬化地面的面积、高层楼房的面积、人流量及车流量的增加, 由于减少了杂草等麻雀的食物来源并增加了干扰, 不利于麻雀的利用。结果表明, 虽然麻雀是一个适应人类生活环境的物种, 但在快速的城市化变迁中,它已表现出对高度城市化环境的不适应。在城市的规划与建设中, 应考虑到为以麻雀为代表的城市鸟类提供生存必要的植被和繁殖场所, 构建人鸟和谐共存的生态城市。
Study of bird preference to plant habitat and species in Beijing urban park
北京城市公园中鸟类对植物生境及种类的偏好研究
Urban ornithological research in China: A review
中国城市鸟类学研究进展
Sampling adequacy estimation for plant species composition by accumulation curves—A case study of urban vegetation in Beijing, China
DOI:10.1016/j.landurbplan.2009.12.008 URL [本文引用: 1]
Species composition and spatial structure of plants in urban parks of Beijing
By the method of stratified random sampling, the species composition and spatial structure of the plants in 53 parks in Beijing urban area were investigated, aimed to provide basic information for the protection of plant diversity in the parks and the management of the parks. A total of 492 plant species belong to 96 families and 283 genera were recorded. Based on the data of 21 investigation items about the trees, shrubs, and grasses in the study area and related statistical analyses, the plant structural patterns commonly seen in the green space of the parks of Beijing urban area were introduced. Among the plants in the parks, native species occupied 5386% of the total. The chorological composition of the genera embraced broad kinds of geographical elements in China, and the predominance of dominant plants was remarkable. In most green patches of the parks, herbaceous species were more abundant and had higher coverage, shrubs had relatively low coverage and were less beneath tree canopy, and trees and shrubs had lower species richness and density. The canopy breadth and the diameter of breast height of trees as well as the breadth of shrubs and the heights of trees and shrubs were basically at the second grade, but the canopy structure of the trees were better, with good conditions of sunlight and growth. The crown missing of the shrubs was relatively low. It was suggested from correlation analyses and document survey of Beijing parks construction history that park landscape design, alien species introduction, and cultivation management were the main factors affecting the species composition and spatial structure of the plants in Beijing urban parks.
北京城区公园的植物种类构成及空间结构
