长江口滨海湿地水鸟对底栖微藻群落的营养级联效应

doi:10.17521/cjpe.2024.0170

摘要/Abstract

摘要： 底栖微藻是滨海湿地的初级生产者之一, 为滨海湿地食物网提供了能量和物质基础, 在滨海湿地生态系统维持中发挥着重要作用。以往研究多聚焦于环境因子、维管植物和植食动物对底栖微藻的影响, 忽略了捕食动物对底栖微藻的营养级联效应。该研究以长江口滨海盐沼湿地为研究系统, 通过开展野外控制实验, 并在一年间对底栖微藻群落的生物量和种类组成分别进行月度和季度测定, 解析了水鸟对底栖微藻的营养级联效应。结果发现: (1)去除水鸟显著降低了底栖微藻的生物量。去除水鸟后, 虽然水鸟直接摄食作用的缺乏有利于底栖微藻, 但摄食微藻的蟹类的增多更强烈地抑制了底栖微藻。(2)去除蟹类(模拟水鸟高强度捕食)也显著降低了底栖微藻的生物量。去除蟹类后, 摄食藻类的螺类大幅增多。(3)去除水鸟和去除蟹类均显著降低了优势微藻类群硅藻的多度, 提高了底栖微藻群落的多样性。该研究表明滨海湿地水鸟可通过直接或间接作用对底栖微藻群落产生强烈的下行调控效应, 丰富了对滨海湿地微藻群落调控机制的理论认识。

关键词: 滨海湿地, 营养级联, 动物消费者, 底栖微藻, 群落多样性

Abstract:

Aims Benthic microalgae are one of the primary producers in coastal wetlands, providing basic energy and material to the food web of coastal wetlands and playing an important role in maintaining the stability of coastal wetland ecosystems. Previous studies have focused on the effects of environmental factors, vascular plants and herbivores on benthic microalgae, neglecting the trophic cascade effects of predators.
Methods We investigated the trophic cascade effects of waterbirds on benthic microalgae in a manipulative field experiment in a coastal wetland in the Chang Jiang (Yangtze) estuary, where we measured the biomass of benthic microalgae monthly and their species composition quarterly for a year.
Important findings Results showed that: (1) benthic microalgal biomass was significantly decreased in waterbird exclusion treatments. In waterbird exclusion treatments, although the lack of direct consumption by waterbirds facilitated benthic microalgae, increases in the abundance of crabs feeding on microalgae suppressed benthic microalgae more strongly. (2) Crab exclusion treatments (simulating intense predation by waterbirds) also significantly reduced benthic microalgal biomass. In crab exclusion treatments, the abundance of snail feeding on microalgae increased substantially. (3) Waterbird and crab exclusion treatments both significantly reduced the abundance of the dominant microalgal taxa, diatoms, and increased the diversity of benthic microalgal communities. This study demonstrates that waterbirds in coastal wetlands can exert strong top-down effects on benthic microalgal communities through multiple direct or indirect processes, and enriches our understanding of the mechanisms controlling microalgal communities in coastal wetlands.

Key words: coastal wetlands, trophic cascade, animal consumers, benthic microalgae, community diversity

刘盈麟, 李春明, 王昊, 武长路, 贺强. 长江口滨海湿地水鸟对底栖微藻群落的营养级联效应. 植物生态学报, 2025, 49(3): 367-378. DOI: 10.17521/cjpe.2024.0170

LIU Ying-Lin, LI Chun-Ming, WANG Hao, WU Chang-Lu, HE Qiang. Trophic cascades of waterbirds on benthic microalgal communities in coastal wetlands in the Yangtze estuary. Chinese Journal of Plant Ecology, 2025, 49(3): 367-378. DOI: 10.17521/cjpe.2024.0170

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2024.0170

https://www.plant-ecology.com/CN/Y2025/V49/I3/367

图/表 7

图1 不同实验处理中底栖微藻的生物量(以叶绿素a含量表征) (平均值±标准误)。同一月份中, 不同小写字母表示不同处理间具有统计学差异(p < 0.05)。季节通过不同背景颜色间隔。

Fig. 1 Biomass (given as chlorophyll a content) of benthic microalgae in different experimental treatments (mean ± SE). Within a month, different lowercase letters indicate statistical differences between different treatments (p < 0.05). Seasons are separated by shadings of different colors.

表1 不同实验处理中水鸟足迹、蟹类、螺类的多度(平均值±标准误)

Table 1 Abundances of waterbird tracks, crab burrows, and snails in different experimental treatments (mean ± SE)

响应变量 Response variable	种植+水鸟去除 Planting + waterbird exclusion	种植+蟹类去除 Planting + crab exclusion	种植 Planting	空白对照 Control	p (Tr)	p (Ti)	p (Tr × Ti)
水鸟足迹 Waterbird tracks	3.50 ± 2.17^b	0.17 ± 0.33^c	170.17 ± 45.24^a	165.63 ± 49.42^a	<0.000 1	<0.000 1	<0.000 1
蟹洞 Crab burrows	26.80 ± 2.98^a	0.38 ± 0.32^c	13.54 ± 1.77^b	13.25 ± 1.53^b	<0.000 1	0.000 3	0.220 0
拟沼螺 Assiminea sp.	4.92 ± 1.49^b	30.25 ± 6.89^a	2.79 ± 0.82^b	3.50 ± 1.40^b	<0.000 1	0.008 5	0.001 6
拟蟹守螺 Cerithidea sp.	3.42 ± 1.21^b	17.54 ± 5.81^a	2.00 ± 0.58^b	2.38 ± 0.83^b	<0.000 1	<0.000 1	0.015 6

图2 底栖微藻生物量(叶绿素a含量表征)与不同动物消费者多度的关系。A, 水鸟足迹(子图为不包含种植+水鸟去除和种植+蟹类去除处理的分析结果)。B, 蟹类(子图为不包含种植+蟹类去除处理的分析结果)。C, 拟沼螺。D, 拟蟹守螺。p为线性混合效应模型的显著性, R2为模型对因变量的解释率, 灰色区域为95%置信区间。

Fig. 2 Relationships between the biomass of benthic microalgae (given as chlorophyll a content) and the abundances of different animal consumers. A, Waterbird tracks (the inset shows the results without planting + waterbird exclusion and planting + crab exclusion treatments). B, Crabs (the inset shows the results without planting + crab exclusion treatments). C, Assiminea sp. D, Cerithidea sp. p indicates the statistical significance of a linear mixed-effects model, and R2 is the proportion of variation in the dependent variable explained by the model, the gray areas are 95% confidence intervals.

图3 水鸟调控底栖微藻生物量的结构方程模型分析。A, 假设模型。B, 统计模型。路径对应的数字为路径系数; *, p < 0.05; **, p < 0.01; ***, p < 0.001; R2为路径的拟合度。

Fig. 3 Structural equation modeling of the effects of waterbirds on the biomass of benthic microalgae. A, Hypothetical model. B, Statistical model. The numbers corresponding to paths are path coefficients; *, p < 0.05; **, p < 0.01; ***, p < 0.001; R2 is the fit of the path.

图4 底栖微藻平均相对多度在不同实验处理间的差异(平均值±标准误)。A, 门分类水平。B, 属分类水平(仅展示多度占比大于1%的门或属; <1%的归为其他)。对于同一个门或属, 不同小写字母表示不同处理间具有显著差异(p < 0.05)。

Fig. 4 Differences in the mean relative abundance (%) of benthic microalgae among different experimental treatments (mean ± SE). A, Phylum level. B, Genus level (only for phyla and genera with an abundance percentage greater than 1%; those < 1% are shown as others). Within a phylum or genus, different lowercase letters indicate significant differences between treatments (p < 0.05).

图5 不同实验处理中底栖藻类群落的非度量多维尺度分析(NMDS) (属分类水平)。椭圆代表95%置信限, stress为低维空间中样本间的相对距离与原始数据中相对距离之间的差异; 通常认为, 当stress < 0.2时, 模型拟合效果可接受。

Fig. 5 Non-metric multidimensional scaling (NMDS) analysis for the genus-level composition of benthic microalgal communities in different experimental treatments. Ellipses indicate 95% confidence limit. Stress indicates the difference between the relative distances of samples in the lower-dimensional space and those in the original high-dimensional data; when stress is <0.2, it is generally considered that the model fit is acceptable.

图6 不同季节不同实验处理中底栖微藻群落的多样性指数(平均值±标准误)。同一季节中, 不同小写字母表示不同实验处理间具有显著差异(p < 0.05)。

Fig. 6 Diversity indices of benthic microalgae communities in different experimental treatments in different seasons (mean ± SE). Within a season, different lowercase letters indicate significant differences between treatments (p < 0.05).

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