旅游干扰对松山油松林土壤微生物多样性及群落结构的影响

doi:10.17521/cjpe.2022.0072

摘要/Abstract

摘要：

掌握旅游干扰对土壤微生物多样性及群落结构的影响, 有助于旅游区环境资源的恢复和管理。该研究在北京松山国家级自然保护区油松(Pinus tabuliformis)林内设置了不同旅游干扰强度(高干扰、低干扰和无干扰)的样地, 调查样地内微生境状况, 测量土壤理化性质, 利用第二代高通量测序技术测定土壤微生物多样性和群落结构, 以评价不同旅游干扰强度对油松林土壤微生物的影响机制。结果显示: 1)高强度干扰显著降低了土壤真菌α多样性, 低强度干扰显著降低了土壤真菌系统发育多样性。干扰强度越大, 土壤真菌多样性越低, 而土壤细菌多样性越高。2)在土壤真菌群落方面, 3类样地的土壤优势真菌门均为担子菌门(Basidiomycota)和子囊菌门(Ascomycota); 高强度干扰显著降低了子囊菌门相对多度, 对担子菌门相对多度无显著影响, 而低强度干扰均对担子菌门和子囊菌门无显著影响。LEfSe分析表明无干扰区的差异类群为真菌Pseudogymnoascus属和3个真菌物种(Oidiodendron griseum、Acrodontium hydnicola、Metacordyceps chlamydosporia); 低干扰区内未能检测到差异类群; 高干扰区差异类群为真菌Clavariaceae科。3)在土壤细菌群落方面, 3类样地的土壤优势细菌门均为变形菌门(Proteobacteria)、放线菌门(Actinobacteria)和酸杆菌门(Acidobacteria); 高强度干扰和低强度干扰对它们的多度无显著影响。LEfSe分析表明无干扰区的差异类群占总差异类群的82.05%, 指示性最强的为细菌Gaiellales和Solirubrobacterales目; 低干扰区未发现差异类群; 高干扰区的差异类群占总差异类群的17.95%, 主要表现为病原指示菌和与人类活动相关的菌群, 指示性最强的为细菌Flavobacteriia纲和疣微菌门(Verrucomicrobia)下一属。4)偏最小二乘法路径模型(PLS-PM)发现干扰强度显著影响微生境指标和土壤真菌多样性; 冗余分析显示, 土壤状况和微生境指标分别解释了不同干扰强度下真菌和细菌群落结构变化的71.35%和74.47%, 乔木胸径、草本盖度和凋落物盖度是不同干扰强度下真菌和细菌群落差异的主要因子。由上可见, 旅游干扰显著降低了油松林土壤微生物α多样性, 并显著影响了其群落结构, 影响效果的不同与干扰强度和微生物种类有关, 并且受到土壤理化性质和微生境状况调控。因此未来应注意旅游区内微生境和土壤状况的修复。

关键词: 旅游干扰, 微生境, 土壤理化性质, 微生物多样性, 群落结构, 松山国家级自然保护区

Abstract:

Aims Understanding the effect of tourism disturbances on soil microbial diversity and community structure is necessary for the restoration and management of environmental resources in tourist areas. Therefore, we conducted a field survey in Beijing Songshan National Nature Reserve, to reveal the effect of different tourism disturbance intensity on soil microorganisms in a Pinus tabuliformis forest.

Methods Three intensity groups, high disturbance (HD), low disturbance (LD) and no disturbance (ND), were conducted in the P. tabuliformis forest. We investigated microhabitat conditions and measured soil physicochemical properties. Next generation sequencing technique was used to determine the diversity and community structure of soil microorganisms. Then, we evaluated the impact of tourism disturbance intensity on soil microorganisms.

Important findings 1) HD significantly reduced soil fungal alpha diversity, and LD significantly reduced soil fungal phylogenetic diversity. Soil fungal diversity showed a decreasing trend, and soil bacterial diversity showed an increasing trend with increasing disturbance intensity. 2) For soil fungal community structure, the dominant phylum of three intensity groups were Basidiomycota and Ascomycota. HD disturbance significantly affected the relative abundance of Ascomycota, but had no effect on Basidiomycota, LD had no effect on both of them. LEfSe analysis showed that indicators of ND were Pseudogymnoascus and three species (Oidiodendron griseum, Acrodontium hydnicola, Metacordyceps chlamydosporia); indicator of HD was Clavariaceae; there was no indicator in LD. 3) For bacterial community structure, the dominant phylum of three intensity groups were Proteobacteria, Actinobacteria and Acidobacteria, but HD and LD had no effect on them. LEfSe showed that indicators of ND accounted for 82.05% of total indicators, and the most indicative ones were Gaiellales and Solirubrobacterales; indicators of HD accounted for 17.95% of total indicators, they mainly manifested as pathogenic indicator bacteria and bacterial groups related to human activities, the most indicative ones were Flavobacteriia and one genus of Verrucomicrobia; there was no indicator in LD. 4) Partial Least Squares Path Modeling (PLS-PM) found disturbance intensity significantly impacted microhabitat and alpha diversity of soil fungi. Redundancy analysis showed that soil and microhabitat condition explained 71.35% and 74.47% of variations in community structure of fungi and bacteria under different intensity group, respectively. Tree diameter at breast height, herb cover and litter cover were the main factors that altered fungal and bacterial community structure. In conclusion, tourism disturbance significantly reduced alpha diversity and impacted community structure of soil microbiota in the P. tabuliformis forest, and the degree of influence associated with disturbance intensity and the kind of microorganisms. Moreover, the impact was also controlled by microhabitat and soil physical and chemical properties. Therefore, future attentions should be paid to the restoration of microhabitats and soil conditions in tourism areas.

Key words: tourism disturbance, microhabitat, soil physicochemical property, microbial diversity, community structure, Songshan National Nature Reserve

冯可, 刘冬梅, 张琦, 安菁, 何双辉. 旅游干扰对松山油松林土壤微生物多样性及群落结构的影响. 植物生态学报, 2023, 47(4): 584-596. DOI: 10.17521/cjpe.2022.0072

FENG Ke, LIU Dong-Mei, ZHANG Qi, AN Jing, HE Shuang-Hui. Effect of tourism disturbance on soil microbial diversity and community structure in a Pinus tabuliformis forest. Chinese Journal of Plant Ecology, 2023, 47(4): 584-596. DOI: 10.17521/cjpe.2022.0072

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2022.0072

https://www.plant-ecology.com/CN/Y2023/V47/I4/584

图/表 12

图1 不同旅游干扰强度样地示意图。 A, 高强度旅游干扰样地。B, 低强度旅游干扰样地。C, 无旅游干扰样地。 △代表供游客使用、休闲和娱乐等建设的基础设施。

Fig. 1 Schematic diagram of plots with different tourism disturbance intensity. A, Plot with high tourism disturbance intensity. B, Plot with low tourism disturbance intensity. C, Plot with no tourism disturbance intensity. △ represents infrastructure for tourist use, leisure and entertainment, etc.

表1 北京松山自然保护区样地信息描述(平均值±标准差)

Table 1 Information for sampling plots in Songshan National Nature Reserve, Beijing (mean ± SD)

类型 Type	海拔 Altitude (m)	坡度 Slope (^o)	树种组成 Tree composition
无干扰 No disturbance	1 099 ± 126	31.25 ± 6.40	油松、北京丁香 Pinus tabuliformis, Syringa reticulata subsp. pekinensis
低干扰区 Low disturbance	1 008 ± 100	27.25 ± 3.27	油松、漆树 Pinus tabuliformis, Toxicodendron verniciflum
高干扰区 High disturbance	985 ± 88	25.25 ± 10.96	油松、山杨、北京丁香、核桃楸 Pinus tabuliformis, Populus davidiana, Syringa reticulata subsp. pekinensis, Juglans mandshurica

表2 北京松山自然保护区样地内微生境变量

Table 2 Description of microhabitat variables in sampling plots of Beijing Songshan Nature Reserve

变量 Variable	描述 Description
郁闭度 Canopy	20 m × 20 m样地中植被总盖度, 目测精度5% Total vegetation coverage in 20 m × 20 m plot, visually measured accuracy 5%
乔木密度 Tree density	20 m × 20 m样地中乔木总数 Total number of arbors in 20 m × 20 m plot
灌木密度 Shrub density	20 m × 20 m样地中灌木总数 Total number of shrubs in 20 m × 20 m plot
乔木盖度 Tree cover	20 m × 20 m样地中乔木覆盖程度, 目测精度5% Coverage of arbors in 20 m × 20 m plot, visually measured accuracy 5%
草本盖度 Herb cover	20 m × 20 m样地中草本覆盖程度, 目测精度5% Coverage of herbs in 20 m × 20 m plot, visually measured accuracy 5%
灌木盖度 Shrub cover	20 m × 20 m样地中灌木覆盖程度, 目测精度5% Coverage of shrubs in 20 m × 20 m plot, visually measured accuracy 5%
凋落物盖度 Litter cover	20 m × 20 m样地中各取样点凋落物覆盖程度, 目测精度5% Coverage of litters at each sampling site in 20 m × 20 m plot, visually measured accuracy 5%
乔木胸径 Tree diameter at breast height (DBH)	距20 m × 20 m样地中心点最近的8株乔木平均胸径 Average DBH of eight trees closest to the centre point of 20 m × 20 m plot
灌木胸径 Shrub DBH	距20 m × 20 m样地中心点最近的8株灌木平均胸径 Average DBH of eight shrubs closest to the centre point of 20 m × 20 m plot

表3 不同干扰强度下的松山油松林土壤真菌和细菌物种组成

Table 3 Soil bacterial and fungal species compositions in Songshan Pinus tabuliformis forest under different disturbance intensity groups

类别 Category	组 Group	门 Phylum	纲 Class	目 Order	科 Family	属 Genus	种 Species
真菌 Fungi	高干扰区 HD	11	57	135	336	626	963
	低干扰区 LD	12	60	153	384	586	873
	无干扰区 ND	14	54	136	343	683	1 053
细菌 Bacteria	高干扰区 HD	45	131	183	222	347	418
	低干扰区 LD	44	135	177	207	318	386
	无干扰区 ND	46	129	171	206	312	374

表4 松山油松林U检验组间土壤细菌和真菌α多样性差异

Table 4 Differences in soil bacterial and fungal alpha diversities between groups by U test in Songshan Pinus tabuliformis forest

类别 Category	指数 Index	无干扰-高干扰 ND-HD	低干扰-无干扰 LD-ND	低干扰-高干扰 LD-HD
真菌 Fungi	Faith系统发育多样性指数 Faith phylogenetic diversity index	39.06 (0.00^*)	-29.73 (0.00^*)	9.33 (0.59)
	香农-维纳多样性指数 Shannon-Wiener diversity index	1.66 (0.00^*)	1.12 (0.39)	2.78 (0.00^*)
	直观绝对序列变体 Observed ASV	177.70 (0.00^*)	570.45 (0.83)	748.15 (0.01^*)
	Pielou均匀度指数 Pielou evenness index	0.16 (0.00^*)	0.07 (0.27)	0.22 (0.00^*)
细菌 Bacteria	Faith系统发育多样性指数 Faith phylogenetic diversity index	-10.29 (0.08)	-0.63 (0.75)	-10.92 (0.20)
	香农-维纳多样性指数 Shannon-Wiener diversity index	0.03 (0.75)	-1.87 (0.00^*)	-1.84 (0.00^*)
	直观数量统计 Observed ASV	-0.60 (0.87)	-759.25 (0.00^*)	-759.85 (0.00^*)
	Pielou均匀度指数 Pielou evenness index	0.00 (0.59)	-0.13 (0.13)	-0.125 (0.07)

图2 北京松山自然保护区不同干扰强度下土壤微生物群落主坐标分析(PCoA)。 A, 土壤真菌。B, 土壤细菌。点越近, 圈越小, 微生物组成越相似。置信区间水平为0.85。LD, 低干扰区; HD, 高干扰区; ND, 无干扰区。

Fig. 2 Principal co-ordinates analysis (PCoA) of soil microbial communities in different disturbance intensity groups in Beijing Songshan Nature Reserve. A, Soil fungi. B, Soil bacteria. Closer distances between dots and smaller circles represent higher similarity in microbial composition. The confidence interval level is 0.85. LD, low disturbance group; HD, high disturbance group; ND, no disturbance group.

图3 北京松山自然保护区不同干扰强度下土壤微生物群落组成(门水平)。 A, 土壤真菌。B, 土壤细菌。LD, 低干扰区; HD, 高干扰区; ND, 无干扰区。图中整体分为上下两部分, 上半部分从左到右依次为低干扰区、高干扰区、无干扰区, 下半部分为各菌群; 上下连接的弦越粗代表菌群的占比越大。刻度数字表示菌群数量。

Fig. 3 Soil microbial community structure in different disturbance intensity groups (phylum level) in Beijing Songshan Nature Reserve. A, Soil fungi. B, Soil bacteria. LD, low disturbance group; HD, high disturbance group; ND, no disturbance group. The whole picture is divided into upper and lower part. The upper part from left to right represents low disturbance group, high disturbance group and no disturbance group, respectively, while the lower part represents different microbial taxa; the thicker the chord, the greater proportion of the corresponding microbial taxa. Scale number represent the number of microorganisms.

图4 北京松山自然保护区不同干扰强度下土壤真菌群落LEfSe分析。 HD, 高干扰区; ND, 无干扰区。线性判别分析(LDA) > 0说明是ND的差异类群, LDA < 0说明是HD的差异类群; 根据LDA结果构建的进化树(门到种水平)。其中绿色节点代表该水平的真菌在ND组含量较高, 红色节点代表该水平的真菌在HD组含量较高, 草绿色节点代表真菌在组间无显著差异。

Fig. 4 LEfSe analysis of fungal communities in different disturbance intensity groups in Beijing Songshan Nature Reserve. HD, high disturbance group; ND, no disturbance group. Linear discriminant analysis (LDA) > 0 indicates biomarkers of ND, LDA < 0 indicates biomarkers of HD; the evolutionary tree (phylum to species level) is constructed according to the LDA results. Among them, the green nodes represent ND hold more abundant fungi than other groups at this level, the red nodes represent HD hold more abundant fungi than other groups at this level, and the green nodes represent that there is no significant difference between groups.

图5 北京松山自然保护区不同干扰强度下土壤细菌群落LEfSe分析。 HD, 高干扰区; ND, 无干扰区。线性判别分析(LDA) > 0说明是ND的差异类群, LDA < 0说明是HD的差异类群; 根据LDA结果构建的进化树(门到种水平)。其中绿色节点代表该水平的细菌在ND组含量较高, 红色节点代表该水平的细菌在HD组含量较高, 草绿色节点代表细菌在组间无显著差异。

Fig. 5 LEfSe analysis of bacterial communities in different disturbance intensity groups in Beijing Songshan Nature Reserve. HD, high disturbance group; ND, no disturbance group. Linear discriminant analysis (LDA) > 0 indicates biomarkers of ND, LDA < 0 indicates biomarkers of HD; the evolutionary tree (phylum to species level) is constructed according to the LDA results. Among them, the green nodes represent ND hold more abundant bacteria than other groups at this level, the red nodes represent HD hold more abundant bacteria than other groups at this level, and the green nodes represent that there is no significant difference between groups.

表5 单因素方差分析、U检验和多重比较检验松山油松林组间土壤理化性质和微生境差异

Table 5 Differences in microhabitats and soil edaphic factors between groups by one-way ANOVA, U test and multiple comparisons in Songshan Pinus tabuliformis forest

变量 Variable	无干扰-高干扰 ND-HD	无干扰-低干扰 ND-LD	高干扰-低干扰 HD-LD
土壤含水量 Soil water content	0.04 (0.02^*)	0.01 (0.30)	-0.02 (0.30)
土壤全氮含量 Soil total nitrogen content	0.02 (0.43)	0.00 (0.83)	-0.02 (0.77)
土壤 pH Soil pH	-0.21 (0.12)	-0.10 (0.69)	0.11 (0.20)
土壤速效钾含量 Soil available potassium content	0.08 (0.00^*)	0.03 (0.34)	-0.05 (0.08)
土壤有机碳含量 Soil organic carbon content	0.71 (0.06)	0.54 (0.19)	-0.17 (0.78)
土壤有效磷含量 Soil available phosphorus content	0.30 (0.26)	-0.11 (0.46)	-0.41 (0.13)
郁闭度 Canopy	8.75 (0.07)	7.50 (0.13)	-1.25 (0.93)
乔木密度 Tree density	0.06 (0.09)	0.05 (0.18)	-0.01 (0.88)
灌木密度 Shrub density	1.76 (0.00^*)	0.70 (0.05^*)	-1.06 (0.00^*)
乔木盖度 Tree cover	15.00 (0.07)	11.25 (0.19)	-3.75 (0.80)
草本盖度 Herb cover	26.25 (0.00^*)	13.75 (0.05^*)	-12.50 (0.05^*)
灌木盖度 Shrub cover	10.00 (0.07)	6.25 (0.09)	-3.75 (0.61)
凋落物盖度 Litter cover	27.50 (0.00^*)	8.75 (0.30)	-18.75 (0.05^*)
乔木胸径 Tree DBH	28.87 (0.00^*)	11.59 (0.11)	-17.28 (0.05^*)
灌木胸径 Shrub DBH	0.46 (0.12)	0.16 (0.72)	-0.30 (0.36)

图6 最小路径模型预测不同干扰强度对松山油松林土壤微生物α多样性的影响。 A, 土壤真菌。B, 土壤细菌。黑色实线代表观察变量的载荷值, 红色箭头实线代表显著负相关, 红(黑)箭头虚线代表无显著相关性。

Fig. 6 PLS-PM predicted the impact of disturbance intensity on soil microbial alpha diversity in Songshan Pinus tabuliformis forest. A, Soil fungi. B, Soil bacteria. The solid black lines represent the loading values of observed variable, the solid red arrow lines represent a significant negative correlation, and the dashed red (black) arrow lines represent no significant correlation.

图7 不同干扰强度下松山油松林土壤微生物群落组成(门水平)与环境因子的冗余分析(RDA)。 A, 土壤真菌。B, 土壤细菌。LD, 低干扰区; HD, 高干扰区; ND, 无干扰区。AK, 速效钾含量; HC, 草本盖度; LC, 凋落物盖度; Tree_DBH, 乔木胸径; SWC, 土壤含水量。黑色箭头实线越长, 影响越大。

Fig. 7 Redundancy analysis (RDA) between soil microbial communities (phylum level) and environmental factor in different disturbance intensity groups in Songshan Pinus tabuliformis forest. A, Soil fungi. B, Soil bacteria. LD, low disturbance group; HD, high disturbance group; ND, no disturbance group. AK, available potassium content; HC, herb cover; LC, litter cover; Tree_DBH, tree diameter at breast height; SWC, soil water content. The longer the solid black arrow line, the greater the influence.

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