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林窗作为森林小尺度干扰,是土壤养分循环的重要驱动力[1]。林窗面积作为重要的林窗特征,对森林土壤养分循环与微生物群落有显著影响[2],同时林窗内微环境异质性也是影响森林土壤生态环境与系统功能的主要因素[3-4]。Muscolo等[5]研究表明,较中林窗(855 m2)和大林窗(1520 m2),小林窗(380 m2)土壤腐殖质含量和微生物生物量最高,有利于保持良好的土壤生态功能。而随后研究表明林窗面积(27 ~ 590 m2)与土壤微生物生物量呈负相关,大林窗(590 m2)内土壤养分循环效率低[2]。中林窗(200 m2)可有效提高土壤微生物量,促进了土壤碳氮循环[3]。小林窗(40 ~ 50 m2)有利于土壤微生物群落结构发展[6],可见不同林窗面积内土壤养分循环和微生物群落特征存在差异。土壤微生物作为土壤中最活跃和最易变化的组分[7],是土壤养分转化、循环的主要驱动力[8],在森林生态系统具有重要作用[9],因此明确林窗面积对土壤养分循环与土壤微生物群落的影响尤为必要。
在森林林窗群落中,季节变化通过改变林窗内光照、温度和水分等环境条件,进而影响土壤理化性质、物质的分解与矿化过程[10],导致林窗微环境异质性,进而影响土壤微生物群落的组成与多样性[10-11]。林窗季节动态变化改变了光照分配格局[11]。林窗生长季(夏季)土壤养分循环效率与有机质含量较高,土壤微生物生物量碳含量为夏高春低,微生物生物量氮含量为夏高冬低,森林土壤微生物生物量随季节动态变化存在差异[12-13]。可见季节变化改变了林窗土壤物质循环和转化,驱动着土壤微生物群落的动态变化。然而,在不同季节下林窗面积对土壤微生物群落的影响机制尚不明确,限制了土壤微生物对林窗响应过程的理解。
格氏栲(Castanopsis kawakamii)是分布于我国中亚热带地区南缘的第三季孑遗植物[14],仅零星分布于南亚热带和中亚热带南缘区域,包括福建、江西、广东、广西、台湾等地。而在福建三明格氏栲自然保护区有700 hm2以格氏栲为群落优势种的天然林[15],引起了广泛关注[15-17]。由于种群已过熟,加之激烈的种间竞争和人为干扰,林窗数量增多[14]。林窗干扰改善了格氏栲群落物种多样性,促进了土壤微生物群落结构改变,对土壤生态环境和系统功能有重要影响[18-19]。目前有关格氏栲天然林不同季节下林窗面积对土壤微生物群落的影响尚未见报道。明确格氏栲林土壤养分和微生物群落对林窗面积的季节动态响应机制,揭示不同季节林窗内土壤微生物功能多样性影响因子,有助于揭示土壤微生物对林窗响应过程。为此,以格氏栲天然林为研究对象,研究林窗大小和季节内土壤理化性质和微生物代谢功能,明确林窗面积和季节对土壤养分有效性与微生物群落功能多样性的影响,揭示生长季与非生长季土壤微生物群落功能多样性的主要影响因子。研究旨在揭示格氏栲天然林土壤微生物动态变化的影响机制,为格氏栲天然林保护提供科学依据。
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格氏栲自然保护区位于福建省三明市郊西南部(26°07′ ~ 26°10′N、117°24′ ~ 117°27′E),面积近700 hm2,为低山、谷地、丘陵地带,属武夷山东延支脉,海拔180 ~ 604 m。亚热带季风型气候,年平均温度为19.4 ℃,无霜期300 d。年降雨量1 500 mm,3—8月降雨量占全年75%,年平均相对湿度79%。年平均风速1.6 m/s。土壤主要类型为暗红壤。植被包括亚热带常绿阔叶林、落叶阔叶林、针阔混交林、灌丛等。乔木层主要树种有格氏栲、米槠(Castanopsis carlesii)和马尾松(Pinus massoniana)等[14-15]。
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以三明格氏栲自然保护区为研究区,在研究区内随机选取不同大小的林窗,在每个林窗中心点距离地面1 m处,使用数码相机(NIKON D7200, NIKON, Tokyo, Japan)搭配鱼眼镜头(AF DX Fisheye Nikkor ED 10.5 mm F2.8G, NIKON, Tokyo, Japan)拍摄林冠半球形照片。根据半球面影像法[20]确定林窗面积,选取小(SG)、中(MG)、大(LG)林窗各3个[21],另外,在邻近林窗样地,郁闭度约0.80的林分中,设置3个面积10 m × 10 m非林窗样地作为对照(NG),平均冠层高度为15 m,乔木层平均胸径为30 cm,平均树龄为120 ~ 150年生。样地概况见表1。
表 1 林窗研究样地概况
Table 1. General situation of the research plots of the forest gaps
林窗 Forest gap GS/m2 SHC/% LG 206.17 ± 4.53 0.85 MG 73.15 ± 1.93 0.67 SG 33.49 ± 2.48 0.50 NG 100 ± 0 0.77 注:LG为大林窗;MG为中林窗;SG为小林窗;NG为对照;GS为林窗面积;SHC为灌草覆盖度。数据为均值 ± 标准差,n = 3,下同。Notes: LG, large gap; MG, medium gap; SG, small gap; NG, control; GS, forest gap size; SHC, shrub and herb coverage. The data are mean ± standard deviation, n = 3. The same below. -
根据福建省森林生态系统生长季(4—11月)与非生长季(12—次年3月)设定[22],分别于2019年1月(非生长季)与8月(生长季),在福建省三明格氏栲自然保护区进行采样。依次在设立的每个林窗与对照样地中,于东、南、西、北4个方向与样地中心点设置5个土壤取样点,利用五点取样法,避开树干和林窗边缘,去除森林凋落物,采集0 ~ 10 cm土层土样进行混合[6]。样品采集后装入塑料袋并置于保鲜箱中,立即运回实验室,过2 mm筛后置冰箱中− 20 ℃保存。所有收集土壤样品均单独处理。
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土壤环境因子选取可直接影响微生物群落的常用理化指标[23]。土壤理化性质测定包括:土壤含水量(SWC)采用烘干法;土壤pH值采用电位法;使用温度记录器(DS1922L-F50 iButton,MAXIM,USA)测定土壤温度,每4 h监测1次;有机碳测定使用元素分析仪(VARIO MAX,ELEMENTAR,GER);碱解氮含量测定使用碱解扩散法;速效磷含量测定采用碳酸氢钠浸提−钼锑抗比色法;速效钾含量测定采用火焰光度法[24]。
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土壤微生物群落代谢功能采用Biolog微平板法测定[25]。称取5 g鲜土于高压灭菌的三角瓶中,加入100 mL含有0.85%的NaCl无菌水,封口,120 r/min震荡30 min,冰浴静置2 min,取上清液5 mL于灭菌过的100 mL三角瓶中,加入45 mL无菌水,重复稀释3 次,制得1∶1 000的提取液,立即用于ELSIA反应。将Biolog微平板预热到25 ℃,用移液枪吸取150 mL提取液于各个孔中,28 ℃恒温培养192 h,每24 h用酶标仪读取590 nm的吸光度值。
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土壤微生物群落对碳源利用的整体能力用平均颜色变化率(average well color development,AWCD)测定。具体计算公式[25]:
$$ {\rm{AWCD}} = \mathop \sum \left( {{C_i} - R} \right)/31 $$ 式中:
$ {C}_{i} $ 为每孔的吸光度;R为对照孔的吸光值。培养144 h后微孔吸光值趋于稳定,因此对培养144 h的数据进行Simpson优势度指数、Shannon-Wiener多样性指数和Pielou指数分析,分别用以评估微生物群落常见种优势度、物种丰富度和物种均匀度[25-26]。
采用SPSS 22.0中双因素方差分析和Duncan法进行方差分析和多重比较(α = 0.05),分析不同季节与不同林窗面积间土壤理化性质、微生物群落功能多样性指数差异性。采用广义线性模型(GLM)中基于正态分布的Gaussian模型探讨影响微生物功能多样性的环境因子,依据AIC准则采用逐步回归法优化模型。GLM分析使用R 3.6.1的broom、glm2包实现[27],相关图标制作在Excel 2010中完成。
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林窗土壤特性的双因素分析结果表明(表2),林窗内不同生长季节间土壤温度、pH值、速效钾和速效磷含量存在极显著差异(P < 0.001)。由表3可知,林窗生长季土壤温度、速效钾含量显著高于非生长季,pH值和速效磷含量显著低于非生长季。林窗面积显著影响土壤pH值、速效钾和速效磷含量(P < 0.01)。林窗生长季土壤pH值(3.21 ~ 3.4)整体小于非生长季(3.37 ~ 3.54),大林窗中土壤pH值均显著高于其他林窗(P < 0.05)。生长季大林窗中速效钾含量最高。土壤速效磷含量受林窗面积与生长季节交互作用的显著影响(P < 0.01),生长季速效磷含量显著低于非生长季,随林窗面积增大速效磷含量显著减少,表明林窗面积增大限制了土壤速效磷的积累。
表 2 林窗土壤特性的双因素方差分析
Table 2. Two-way ANOVA analysis of soil characteristics in different growing seasons and gap size
环境因子 Environmental factor 因子 Factor 自由度 df F P ST 季节 Season 1 2 707.332 < 0.001*** 林窗面积 Forest gap size 3 0.978 0.428 季节 × 林窗面积 Season × forest gap size 3 0.325 0.807 SWC 季节 Season 1 2.246 0.153 林窗面积 Forest gap size 3 0.298 0.826 季节 × 林窗面积 Season × forest gap size 3 0.077 0.972 pH 季节 Season 1 45.334 < 0.001*** 林窗面积 Forest gap size 3 5.256 0.010** 季节 × 林窗面积 Season × forest gap size 3 2.132 0.136 HN 季节 Season 1 3.219 0.092 林窗面积 Forest gap size 3 1.256 0.323 季节 × 林窗面积 Season × forest gap size 3 0.586 0.633 AK 季节 Season 1 84.533 < 0.001*** 林窗面积 Forest gap size 3 9.146 0.001** 季节 × 林窗面积 Season × forest gap size 3 0.733 0.548 AP 季节 Season 1 28.392 < 0.001*** 林窗面积 Forest gap size 3 18.916 < 0.001*** 季节 × 林窗面积 Season × forest gap size 3 7.052 0.003** SOC 季节 Season 1 1.439 0.248 林窗面积 Forest gap size 3 2.032 0.150 季节 × 林窗面积 Season × forest gap size 3 1.521 0.247 注:ST为土壤温度;SWC为土壤含水量;HN为碱解氮;AK为速效钾;AP为速效磷;SOC为有机碳,下同。*代表差异显著(P < 0.05);**代表差异极显著(P < 0.01);***代表差异极显著(P < 0.001),下同。Notes: ST, soil temperature; SWC, soil water content; HN, alkali-hydrolyzable nitrogen; AK, available potassium; AP, available phosphorus; SOC, soil organic carbon. * represents significant difference (P < 0.05); ** represents extremely significant difference (P < 0.01); *** represents extremely significant difference (P < 0.001). The same below. 表 3 不同面积林窗生长季与非生长季土壤特性
Table 3. Soil characteristics of forest gaps with different size in growing season and non-growing season
季节 Season 林窗
Forest gapST/℃ pH HN/(mg∙kg− 1) AK/(mg∙kg− 1) AP/(mg∙kg− 1) 生长季 Growing season LG 25.9 ± 0.65a 3.4 ± 0.08b 212.05 ± 34.94ab 120.89 ± 20.25a 5.89 ± 2.72d MG 25.7 ± 0.37a 3.25 ± 0.01cd 215.32 ± 7.09ab 86.51 ± 6.13ab 10.61 ± 0.30c SG 25.64 ± 0.14a 3.24 ± 0.08cd 182.57 ± 20.6b 93.56 ± 8.14b 12.57 ± 1.00abc NG 25.6 ± 0.59a 3.21 ± 0.03d 235.79 ± 12.76ab 94.85 ± 2.55b 12.64 ± 1.03abc 非生长季 Non-growing season LG 12.94 ± 0.36b 3.54 ± 0.09a 222.69 ± 55.27ab 75.46 ± 12.31cd 12.01 ± 0.01bc MG 12.63 ± 0.33b 3.37 ± 0.1bc 231.7 ± 49.14ab 56.01 ± 2.88e 12.08 ± 0.27bc SG 12.63 ± 0.07b 3.45 ± 0.1ab 234.15 ± 15.6ab 61.2 ± 6.91de 13.2 ± 0.64ab NG 12.02 ± 1.38b 3.53 ± 0.01a 248.07 ± 11.26a 59.89 ± 0.36de 14.33 ± 0.59a 注:同一列数据后不同字母表示差异显著(P < 0.05),下同。Notes: different letters in the same column indicate significant difference(P < 0.05). The same below. -
Biolog微平板微孔中碳源利用情况采用平均颜色变化率(AWCD)表示,可反映土壤微生物对碳源的利用能力与代谢活性[28]。表4中随培养时间变化,土壤微生物群落代谢的AWCD值变化极显著(P < 0.001),林窗内生长季节对土壤微生物碳源利用能力有极显著影响(P < 0.001)。在培养中后期,林窗内生长季微生物AWCD值显著高于非生长季(图1),说明生长季土壤微生物对碳源整体利用程度高,土壤微生物活性高。非生长季土壤微生物AWCD值规律为NG > SG > MG > LG,表明对照的土壤微生物对碳源利用程度最高,土壤微生物活性最高。
图 1 不同林窗内生长季与非生长季土壤微生物AWCD值
Figure 1. Soil microbial AWCD values of different forest gaps in growing season and non-growing season
表 4 林窗土壤平均颜色变化率值的双因素方差分析
Table 4. Two-way ANOVA on soil average well color development(AWCD)value of forest gaps
组间因子
Intergroup factordf F P 组内因子
Intragroup factor自由度
dfF P 季节 Season 1 250.338 < 0.001*** 时间 Time 8 989.012 < 0.001*** 林窗面积 Forest gap size 3 0.455 0.717 时间 × 季节 Time × season 8 224.237 < 0.001*** 季节 × 林窗面积
Season × forest gap size3 0.111 0.952 时间 × 林窗面积 Time × forest gap size 24 0.601 0.926 时间 × 季节 × 林窗面积
Time × season × forest gap size24 0.263 1.000 -
林窗生长季土壤微生物144 h对不同碳源的利用率均高于非生长季(图2),生长季土壤微生物对氨基酸类碳源利用程度最高,不同面积林窗内土壤对不同碳源的利用程度无显著差异(P > 0.05)。林窗非生长季土壤微生物对氨基酸类、羧酸类碳源利用程度最高,大林窗土壤微生物对氨基酸类、多聚物类和糖类碳源的利用程度均显著低于其他面积的林窗(P < 0.05),土壤微生物活性最低。
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生物多样性指数描述了生物的类型数、丰富和均匀程度。由表5可知,林窗内不同生长季节间土壤微生物功能多样性指数中Simpson指数、Shannon-Wiener指数和Pielou指数均具有显著差异(P < 0.01),林窗生长季Simpson指数显著低于非生长季,Shannon-Wiener指数和Pielou指数均显著高于非生长季,说明林窗生长季土壤微生物常见种优势度低,物种丰富度与均匀度高。生长季节、林窗面积和二者的交互作用均显著影响Shannon-Wiener指数和Pielou指数,表明生长季节与林窗面积共同作用于土壤微生物功能多样性。表5中生长季林窗面积对土壤微生物群落功能多样性指数无显著影响(P > 0.05)。非生长季小林窗Simpson指数显著高于中林窗、非林窗,表明土壤中微生物常见种优势度高;中林窗Shannon-Wiener指数、Pielou指数显著高于其他林窗和非林窗(P < 0.05),表明非生长季中林窗的形成提高了土壤微生物群落的物种丰富度和物种均一性,对土壤微生物群落起促进作用(表6)。
表 5 不同生长季节与林窗面积的微生物功能多样性双因素分析结果
Table 5. Results of two-way ANOVA of functional diversity of microorganisms in different growing seasons and forest gap size
多样性指数 Diversity index 因子 Factor df F P Simpson 指数
Simpson index季节 Season 1 8.773 0.009** 林窗面积 Forest gap size 3 1.684 0.210 季节 × 林窗面积 Season × forest gap size 3 1.557 0.239 Shannon-Wiener指数
Shannon-Wiener index季节 Season 1 350.491 < 0.001*** 林窗面积 Forest gap size 3 4.298 0.021* 季节 × 林窗面积 Season × forest gap size 3 4.403 0.019* Pielou 指数
Pielou index季节 Season 1 350.665 < 0.001*** 林窗面积 Forest gap size 3 4.281 0.021* 季节 × 林窗面积 Season × forest gap size 3 4.406 0.019* 表 6 不同面积林窗土壤微生物功能多样性
Table 6. Functional diversity of soil microorganisms of forest gaps in different size
季节
Season林窗
Forest gapSimpson指数
Simpson indexShannon-Wiener指数
Shannon-Wiener indexPielou指数
Pielou index生长季 Growing season LG 0.984 4 ± 0.000 2b 4.88 ± 0.02a 0.985 7 ± 0.004 3a MG 0.984 2 ± 0.000 3b 4.86 ± 0.01a 0.980 6 ± 0.002 2a SG 0.984 8 ± 0.000 3b 4.9 ± 0.01a 0.988 3 ± 0.001 4a NG 0.983 9 ± 0.001 1b 4.84 ± 0.05a 0.977 8 ± 0.010 9a 非生长季 Non-growing season LG 1.011 7 ± 0.006 7ab 4.49 ± 0.02c 0.906 5 ± 0.003 4c MG 0.996 7 ± 0.007b 4.63 ± 0.03b 0.935 3 ± 0.005 6b SG 1.031 0 ± 0.051 3a 4.54 ± 0.09c 0.917 1 ± 0.017 8c NG 0.987 0 ± 0.002b 4.48 ± 0.05c 0.904 0 ± 0.010 9c -
依据AIC准则采用逐步回归法优化模型(表7),通过GLM对土壤微生物功能多样性与环境因子之间关系进行分析(表8)。林窗生长季Simpson指数与土壤温度和速效钾含量呈显著正相关(P < 0.05,B > 0),其中土壤温度与其呈极显著正相关(P < 0.001,B > 0),表明土壤温度是生长季土壤微生物群落功能多样性的主要影响因子。林窗非生长季Simpson指数与土壤温度、含水量和碱解氮呈显著正相关(P < 0.05,B > 0),与速效钾和有机碳含量呈显著负相关(P < 0.05,B < 0),其中碱解氮与速效钾含量与其呈极显著相关(P < 0.001)。Shannon-Wiener指数和Pielou指数与土壤含水量和林窗面积含量呈极显著负相关(P < 0.01,B < 0),与土壤速效钾含量呈显著正相关(P < 0.05,B > 0),其中土壤含水量和林窗面积与其呈极显著相关(P < 0.01),表明土壤含水量和林窗面积是非生长季土壤微生物群落功能多样性的主要影响因子。
表 7 土壤微生物功能多样性与环境因子间逐步回归结果
Table 7. Results of stepwise regression between functional diversity of soil microorganisms and environmental factors
季节 Season 多样性指数 Diversity index 环境因子 Environmental factor AIC 生长季 Growing season Simpson指数 Simpson index ST + SWC + pH + HN + AK + AP + SOC + GA − 423.13 ST + SWC + pH + AK + AP + SOC + GA − 424.92 ST + pH + AK + AP + SOC + GA − 426.74 ST + pH + AK + AP + SOC − 428.27 Shannon-Wiener指数 Shannon-Wiener index ST + SWC + pH + HN + AK + AP + SOC + GA − 181.88 ST + SWC + pH + HN + AK + AP + SOC − 183.66 ST + SWC + pH + HN + AP + SOC − 185.52 ST + SWC + pH + HN + SOC − 187.35 ST + SWC + HN + SOC − 188.68 ST + HN + SOC − 189.73 ST + SOC − 191.15 Pielou指数 Pielou index ST + SWC + pH + HN + AK + AP + SOC + GA − 277.94 ST + SWC + pH + HN + AK + AP + SOC − 279.72 ST + SWC + pH + HN + AP + SOC − 281.57 ST + SWC + pH + HN + SOC − 283.41 ST + SWC + HN + SOC 284.73 ST + HN + SOC − 285.79 ST + SOC − 287.21 非生长季 Non-growing season Simpson指数 Simpson index ST + SWC + pH + HN + AK + AP + SOC + GA − 284.55 ST + SWC + pH + HN + AK + SOC + GA − 286.52 ST + SWC + pH + HN + AK + SOC − 288.46 ST + SWC + HN + AK + SOC − 289.41 Shannon-Wiener指数 Shannon-Wiener index ST + SWC + pH + HN + AK + AP + SOC + GA − 84.2 SWC + pH + HN + AK + AP + SOC + GA − 86.11 SWC + pH + HN + AK + AP + GA − 87.56 Pielou指数 Pielou index ST + SWC + pH + HN + AK + AP + SOC + GA − 180.22 SWC + pH + HN + AK + AP + SOC + GA − 182.13 SWC + pH + HN + AK + AP + GA − 183.58 注:AIC为赤池信息准则。下同。Notes: AIC,akaike information criterion.The same below. 表 8 土壤微生物功能多样性与环境因子间GLM分析
Table 8. GLM analysis of the relationship between functional diversity of soil microorganisms and environmental factors
季节
Season多样性指数
Diversity index环境因子
Environmental factorAIC β SE t P 生长季
Growing seasonSimpson指数
Simpson indexST − 428.27 1.25 × 10− 3 2.76 × 10− 4 4.525 0 0.000 9*** AK 3.12 × 10− 5 1.36 × 10− 5 2.298 0 0.038 6* Shannon-Wiener指数
Shannon-Wiener index— − 191.15 — — — — Pielou指数
Pielou index— − 287.21 — — — — 非生长季
Non-growing seasonSimpson指数
Simpson indexST − 289.41 3.47 × 10− 3 1.52 × 10− 3 2.289 0 0.031 2* SWC 2.46 × 10− 3 8.92 × 10− 4 2.754 0 0.011 0* HN 2.03 × 10− 4 3.96 × 10− 5 5.134 0 < 0.000 1*** AK − 7.74 × 10− 4 1.61 × 10− 4 − 4.808 0 < 0.000 1*** SOC − 1.44 × 10− 2 4.16 × 10− 3 − 3.471 0 0.002 0** Shannon-Wiener指数
Shannon-Wiener indexSWC − 87.56 − 0.089 1 0.025 9 − 3.455 0 0.002 2** AK 0.016 4 0.005 9 2.784 0 0.010 6* GA − 0.002 8 0.000 9 − 3.049 0 0.005 7** Pielou指数
Pielou indexSWC − 183.58 − 0.018 0 0.005 2 − 3.443 0 0.002 2** AK 0.003 3 0.001 2 2.784 0 0.010 6* GA − 0.000 6 0.000 2 − 3.050 0 0.005 7** -
林窗形成后环境异质性增加,影响土壤理化性质与凋落物分解[12]。林窗形成显著提高了土壤pH值,大林窗土壤pH值最高,林窗形成降低了土壤酸度,在于林窗形成减少了凋落物输入,凋落物分解产生的腐殖质酸减少,土壤酸性降低,与梁晶等[29]研究一致。对照土壤碱解氮和速效磷含量均高于林窗土壤,林窗促进了土壤微生物和植物根系对碱解氮、速效磷的吸收,提高了土壤养分利用率,有利于土壤养分循环。其次凋落物积累与分解是影响土壤养分储存与循环的重要因素[30],非林窗地表凋落物积累较多,凋落物分解增加了土壤养分含量,保证了格氏栲群落的生长繁育。
在森林生态系统中,林窗内土壤微环境呈季节动态变化[10]。林窗生长季速效钾含量显著高于非生长季,可能是因为生长季土壤温度高,降水增多,土壤干湿交替会引起黏土矿物的收缩与膨胀,影响速效钾的固定与释放[31]。生长季土壤速效磷含量显著低于非生长季,在于生长季植物根系与土壤微生物代谢旺盛,对速效磷需求量增加,与薛敬意等[32]研究一致。
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林窗内生长季土壤微生物AWCD值高于非生长季(图1),生长季微生物功能多样性指数中Shannon-Wiener指数、Pielou指数均高于非生长季(表6),表明生长季土壤微生物活性与功能多样性高,呈现多物种共存趋势。土壤温度的季节变化是影响土壤微生物代谢和养分有效性的重要因素[33],生长季土壤温度高于非生长季(表3),促进了土壤微生物代谢能力与功能多样性升高,更适于土壤微生物繁殖代谢。林窗非生长季土壤微生物的碳源代谢能力与林窗面积呈负相关,表明非生长季林窗抑制了土壤微生物活性升高,且随林窗面积增大,抑制作用更为强烈,土壤养分循环效率降低,与Schliemann等研究一致[2]。
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不同面积林窗内非生长季土壤微生物对多聚物类、糖类和氨基酸类碳源的利用差异显著(图2)。许振羽等[34]研究也发现了类似现象:土壤微生物对不同碳源利用能力不同,与植物根系分泌物等有关。植物根系代谢过程中会向土壤中分泌大量有机物,包含糖类、酚类和氨基酸类等有机化合物[35],也为土壤中微生物生长繁殖提供了养料,二者形成相互调节关系,促进了土壤有机质循环,增强了土壤系统的稳定性。
格氏栲林土壤微生物对氨基酸类碳源利用率最高,微生物可有效利用氨基酸类碳源,合成植物生长所需有机氮以促进植物生长[36]。王晶晶等[37]在常绿阔叶林研究结果显示,土壤微生物对羧酸类碳源利用率最高。吴则焰等[38]对中亚热带各海拔植被带研究结果显示,碳水化合物和羧酸类碳源是土壤微生物的主要碳源。与本研究结果不同,这可能是由于森林群落组成不同,森林群落结构决定了土壤中凋落物与根系分泌物的种类与质量,影响着土壤微生物代谢功能[39]。
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GLM分析表明林窗内不同生长季节间土壤微生物功能多样性影响因子不同。林窗生长季Simpson指数与土壤温度、速效钾含量呈正相关(表8),其中与土壤温度呈极显著正相关,与张红等[40]研究一致,表明林窗生长季土壤微生物群落起分异作用的环境因子是土壤温度。非生长季中土壤含水量、碱解氮和速效钾含量与微生物群落功能多样性有极显著影响。其中Simpson指数与碱解氮含量呈极显著正相关,表明土壤碱解氮是微生物代谢的重要元素,其含量升高有利于提高微生物常见种优势度[41]。非生长季土壤速效钾含量与Shannon-Wiener指数和Pielou指数正相关,同时非生长季土壤速效钾含量与微生物功能多样性均低于生长季,表明土壤中速效钾含量降低限制了土壤微生物功能多样性升高,存在供求矛盾,不利于格氏栲幼苗生长及群落发展[42]。林窗面积与非生长季Shannon-Wiener指数和Pielou指数呈显著负相关(表7),表明林窗形成后土壤理化环境改变,凋落物输入与植物根系分泌物减少导致供给微生物代谢的养料不足[43],抑制了土壤微生物的生长繁殖,且随林窗面积增大抑制作用更明显。
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生长季格氏栲林林窗内微生物碳源利用能力与群落功能多样性显著高于非生长季。林窗内不同生长季节土壤微生物群落的季节变化格局存在差异,主要影响因子不同,生长季土壤微生物群落主要影响因子为土壤温度;非生长季主要影响因子为土壤碱解氮、速效钾含量、土壤含水量和林窗面积。即生长季不同林窗面积下土壤微生物碳源利用能力与功能多样性保持较高水平,有利于土壤养分循环。非生长季非林窗土壤环境有利于微生物生长代谢,维持土壤生态系统功能,保证格氏栲群落幼苗生长及群落发展。
通过Biolog微平板技术探究了不同林窗面积内土壤微生物群落代谢功能和功能多样性的季节动态变化,明确了林窗面积对土壤微生物群落的动态影响机制,为格氏栲林可持续发展提供了一定的科学依据。Biolog技术是研究微生物结构和功能多样性的重要方法,能有效解析土壤微生物群落结构特征,但无法明确具体微生物群落组成和结构信息,未来可采用变性梯度凝胶电泳技术(DGGE)和高通量测序等技术,进一步探讨格氏栲林林窗内土壤微生物群落组成和结构。
Seasonal dynamics of functional diversity of soil microbial communities in Castanopsis kawakamii forest gaps
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摘要:
目的 林窗作为森林生态系统中的小尺度干扰,对森林土壤养分循环与微生物群落功能多样性维持起着重要作用。明确不同林窗大小土壤养分和微生物群落功能多样性及其季节动态响应机制,有助于改善格氏栲林土壤生态环境。 方法 以格氏栲天然林林窗为对象,采用Biolog微平板法,研究不同林窗大小土壤理化性质、碳源利用能力和代谢特征的季节动态变化规律。 结果 (1)林窗生长季土壤温度、速效钾含量显著高于非生长季,pH值、速效磷含量显著低于非生长季。林窗形成促进了土壤pH值升高与速效钾积累,加速了微生物对碱解氮与速效磷的吸收和利用。(2)林窗生长季土壤微生物平均颜色变化率在培养的中后期显著高于非生长季。林窗内土壤微生物在生长季中主要利用碳源为羧酸、多聚物和氨基酸类,在非生长季中主要利用碳源为氨基酸类和羧酸类。(3)林窗土壤微生物功能多样性指数中,生长季Shannon-Wiener和Pielou指数显著高于非生长季,Simpson指数显著低于非生长季。林窗面积对生长季土壤微生物群落功能多样性指数影响不明显。非生长季小林窗Simpson指数最高,中林窗Shannon-Wiener指数和Pielou指数最高。(4)广义线性模型表明,林窗生长季的土壤温度和土壤速效钾含量升高有利于土壤微生物常见种优势度升高;非生长季土壤碱解氮含量降低,速效钾含量升高有利于微生物功能多样性升高。 结论 生长季林窗内土壤微生物群落功能多样性保持较高水平,土壤养分循环效率高;非生长季非林窗土壤环境有利于土壤微生物生长代谢,维持土壤生态系统功能。林窗形成导致土壤温度与速效养分含量的异质性是影响土壤微生物群落代谢特征和功能多样性的主要因素。 -
关键词:
- 林窗 /
- 土壤微生物 /
- 功能多样性 /
- Biolog微平板法 /
- 格氏栲林
Abstract:Objective As a small-scale disturbance in the forest ecosystem, the forest gap plays an important role in nutrient cycling and functional diversity of microbial community in the soil of forest. Clarifying the seasonal dynamic response mechanism of soil nutrients and functional diversity of microbial community to the forest size will help to improve the soil ecological environment of Castanopsis kawakamii forests. Method The gaps of C. kawakamii natural forests were used as research objects, and the Biolog micro-plate method was used, combining the regularity of soil physical and chemical properties, carbon source utilization capacity and metabolic characteristics with different size of forest gaps during growing season and non-growing season. Result (1) The soil temperature (ST), available potassium (AK) content in the growing season of the gaps were significantly higher than those in the non-growing season, and pH value, available phosphorus (AP) content were significantly lower than those in the non-growing season. The formation of forest gaps promoted the increase of soil pH value and the accumulation of available potassium (AK), and accelerated the absorption and utilization of alkali-hydrolyzable nitrogen (HN) and available phosphorus (AP) by microorganisms. (2) The average well color development (AWCD) of soil microorganisms in the growing season of the forest gaps was significantly higher than that in the non-growing season in the middle and late cultivation periods. The soil microorganisms of the forest gaps mainly used carboxylic acid, polymer, and amino acid carbon sources in the growing season, and mainly used the carbon sources as amino acid and carboxylic acid carbon sources in the non-growing season. (3) In soil microbial functional diversity indexes of forest gaps, Shannon-Wiener and Pielou indices in the growing season of the forest gaps were significantly higher than those in the non-growing season, and the Simpson index was significantly lower than in the non-growing season. Gap size had no significant effect on the functional diversity index of microbial community during the growing season. The Simpson index of the soil microbial community in the non-growing small forest window was the highest. The Shannon-Wiener index and Pielou index of the medium gaps were the highest. (4) Generalized linear model (GLM) analysis showed that increasing soil temperature (ST) and soil available potassium (AK) in the growing season of the forest gaps were conducive to increasing the dominance of common soil microorganism species. The reduction of soil alkaline nitrogen (HN) content and the increase of available potassium (AK) content in non-growing seasons were conducive to the increase of microbial diversity and uniformity. Conclusion Functionaldiversity of soil microbial community of the forest gaps during the growing season is maintained at a high level, and the soil nutrient cycling efficiency is high. The soil environment of non-gaps during the non-growing season is conducive to the growth and metabolism of soil microorganisms and maintains the function of the soil ecosystem. Heterogeneity of soil temperature and available nutrient content caused by the formation of forest gaps is the main factor affecting the metabolic characteristics and functional diversity of soil microbial communities. -
图 1 不同林窗内生长季与非生长季土壤微生物AWCD值
LG1为生长季大林窗;MG1为生长季中林窗;SG1为生长季小林窗;NG1为生长季对照;LG2为非生长季大林窗;MG2为非生长季中林窗;SG2为非生长季小林窗;NG2为非生长季对照。同一列数据上不同字母表示差异显著(P < 0.05)。下同。LG1, large forest gap in growing season; MG1, medium forest gap in growing season; SG1, small forest gap in growing season; NG1, control in growing season; LG2, large forest gap in non-growing season; MG2, medium forest gap in non-growing season; SG2, small forest gap in non-growing season; NG2, control in non-growing season. Different letters above the same column data indicate significant differences (P < 0.05).The same below.
Figure 1. Soil microbial AWCD values of different forest gaps in growing season and non-growing season
表 1 林窗研究样地概况
Table 1. General situation of the research plots of the forest gaps
林窗 Forest gap GS/m2 SHC/% LG 206.17 ± 4.53 0.85 MG 73.15 ± 1.93 0.67 SG 33.49 ± 2.48 0.50 NG 100 ± 0 0.77 注:LG为大林窗;MG为中林窗;SG为小林窗;NG为对照;GS为林窗面积;SHC为灌草覆盖度。数据为均值 ± 标准差,n = 3,下同。Notes: LG, large gap; MG, medium gap; SG, small gap; NG, control; GS, forest gap size; SHC, shrub and herb coverage. The data are mean ± standard deviation, n = 3. The same below. 表 2 林窗土壤特性的双因素方差分析
Table 2. Two-way ANOVA analysis of soil characteristics in different growing seasons and gap size
环境因子 Environmental factor 因子 Factor 自由度 df F P ST 季节 Season 1 2 707.332 < 0.001*** 林窗面积 Forest gap size 3 0.978 0.428 季节 × 林窗面积 Season × forest gap size 3 0.325 0.807 SWC 季节 Season 1 2.246 0.153 林窗面积 Forest gap size 3 0.298 0.826 季节 × 林窗面积 Season × forest gap size 3 0.077 0.972 pH 季节 Season 1 45.334 < 0.001*** 林窗面积 Forest gap size 3 5.256 0.010** 季节 × 林窗面积 Season × forest gap size 3 2.132 0.136 HN 季节 Season 1 3.219 0.092 林窗面积 Forest gap size 3 1.256 0.323 季节 × 林窗面积 Season × forest gap size 3 0.586 0.633 AK 季节 Season 1 84.533 < 0.001*** 林窗面积 Forest gap size 3 9.146 0.001** 季节 × 林窗面积 Season × forest gap size 3 0.733 0.548 AP 季节 Season 1 28.392 < 0.001*** 林窗面积 Forest gap size 3 18.916 < 0.001*** 季节 × 林窗面积 Season × forest gap size 3 7.052 0.003** SOC 季节 Season 1 1.439 0.248 林窗面积 Forest gap size 3 2.032 0.150 季节 × 林窗面积 Season × forest gap size 3 1.521 0.247 注:ST为土壤温度;SWC为土壤含水量;HN为碱解氮;AK为速效钾;AP为速效磷;SOC为有机碳,下同。*代表差异显著(P < 0.05);**代表差异极显著(P < 0.01);***代表差异极显著(P < 0.001),下同。Notes: ST, soil temperature; SWC, soil water content; HN, alkali-hydrolyzable nitrogen; AK, available potassium; AP, available phosphorus; SOC, soil organic carbon. * represents significant difference (P < 0.05); ** represents extremely significant difference (P < 0.01); *** represents extremely significant difference (P < 0.001). The same below. 表 3 不同面积林窗生长季与非生长季土壤特性
Table 3. Soil characteristics of forest gaps with different size in growing season and non-growing season
季节 Season 林窗
Forest gapST/℃ pH HN/(mg∙kg− 1) AK/(mg∙kg− 1) AP/(mg∙kg− 1) 生长季 Growing season LG 25.9 ± 0.65a 3.4 ± 0.08b 212.05 ± 34.94ab 120.89 ± 20.25a 5.89 ± 2.72d MG 25.7 ± 0.37a 3.25 ± 0.01cd 215.32 ± 7.09ab 86.51 ± 6.13ab 10.61 ± 0.30c SG 25.64 ± 0.14a 3.24 ± 0.08cd 182.57 ± 20.6b 93.56 ± 8.14b 12.57 ± 1.00abc NG 25.6 ± 0.59a 3.21 ± 0.03d 235.79 ± 12.76ab 94.85 ± 2.55b 12.64 ± 1.03abc 非生长季 Non-growing season LG 12.94 ± 0.36b 3.54 ± 0.09a 222.69 ± 55.27ab 75.46 ± 12.31cd 12.01 ± 0.01bc MG 12.63 ± 0.33b 3.37 ± 0.1bc 231.7 ± 49.14ab 56.01 ± 2.88e 12.08 ± 0.27bc SG 12.63 ± 0.07b 3.45 ± 0.1ab 234.15 ± 15.6ab 61.2 ± 6.91de 13.2 ± 0.64ab NG 12.02 ± 1.38b 3.53 ± 0.01a 248.07 ± 11.26a 59.89 ± 0.36de 14.33 ± 0.59a 注:同一列数据后不同字母表示差异显著(P < 0.05),下同。Notes: different letters in the same column indicate significant difference(P < 0.05). The same below. 表 4 林窗土壤平均颜色变化率值的双因素方差分析
Table 4. Two-way ANOVA on soil average well color development(AWCD)value of forest gaps
组间因子
Intergroup factordf F P 组内因子
Intragroup factor自由度
dfF P 季节 Season 1 250.338 < 0.001*** 时间 Time 8 989.012 < 0.001*** 林窗面积 Forest gap size 3 0.455 0.717 时间 × 季节 Time × season 8 224.237 < 0.001*** 季节 × 林窗面积
Season × forest gap size3 0.111 0.952 时间 × 林窗面积 Time × forest gap size 24 0.601 0.926 时间 × 季节 × 林窗面积
Time × season × forest gap size24 0.263 1.000 表 5 不同生长季节与林窗面积的微生物功能多样性双因素分析结果
Table 5. Results of two-way ANOVA of functional diversity of microorganisms in different growing seasons and forest gap size
多样性指数 Diversity index 因子 Factor df F P Simpson 指数
Simpson index季节 Season 1 8.773 0.009** 林窗面积 Forest gap size 3 1.684 0.210 季节 × 林窗面积 Season × forest gap size 3 1.557 0.239 Shannon-Wiener指数
Shannon-Wiener index季节 Season 1 350.491 < 0.001*** 林窗面积 Forest gap size 3 4.298 0.021* 季节 × 林窗面积 Season × forest gap size 3 4.403 0.019* Pielou 指数
Pielou index季节 Season 1 350.665 < 0.001*** 林窗面积 Forest gap size 3 4.281 0.021* 季节 × 林窗面积 Season × forest gap size 3 4.406 0.019* 表 6 不同面积林窗土壤微生物功能多样性
Table 6. Functional diversity of soil microorganisms of forest gaps in different size
季节
Season林窗
Forest gapSimpson指数
Simpson indexShannon-Wiener指数
Shannon-Wiener indexPielou指数
Pielou index生长季 Growing season LG 0.984 4 ± 0.000 2b 4.88 ± 0.02a 0.985 7 ± 0.004 3a MG 0.984 2 ± 0.000 3b 4.86 ± 0.01a 0.980 6 ± 0.002 2a SG 0.984 8 ± 0.000 3b 4.9 ± 0.01a 0.988 3 ± 0.001 4a NG 0.983 9 ± 0.001 1b 4.84 ± 0.05a 0.977 8 ± 0.010 9a 非生长季 Non-growing season LG 1.011 7 ± 0.006 7ab 4.49 ± 0.02c 0.906 5 ± 0.003 4c MG 0.996 7 ± 0.007b 4.63 ± 0.03b 0.935 3 ± 0.005 6b SG 1.031 0 ± 0.051 3a 4.54 ± 0.09c 0.917 1 ± 0.017 8c NG 0.987 0 ± 0.002b 4.48 ± 0.05c 0.904 0 ± 0.010 9c 表 7 土壤微生物功能多样性与环境因子间逐步回归结果
Table 7. Results of stepwise regression between functional diversity of soil microorganisms and environmental factors
季节 Season 多样性指数 Diversity index 环境因子 Environmental factor AIC 生长季 Growing season Simpson指数 Simpson index ST + SWC + pH + HN + AK + AP + SOC + GA − 423.13 ST + SWC + pH + AK + AP + SOC + GA − 424.92 ST + pH + AK + AP + SOC + GA − 426.74 ST + pH + AK + AP + SOC − 428.27 Shannon-Wiener指数 Shannon-Wiener index ST + SWC + pH + HN + AK + AP + SOC + GA − 181.88 ST + SWC + pH + HN + AK + AP + SOC − 183.66 ST + SWC + pH + HN + AP + SOC − 185.52 ST + SWC + pH + HN + SOC − 187.35 ST + SWC + HN + SOC − 188.68 ST + HN + SOC − 189.73 ST + SOC − 191.15 Pielou指数 Pielou index ST + SWC + pH + HN + AK + AP + SOC + GA − 277.94 ST + SWC + pH + HN + AK + AP + SOC − 279.72 ST + SWC + pH + HN + AP + SOC − 281.57 ST + SWC + pH + HN + SOC − 283.41 ST + SWC + HN + SOC 284.73 ST + HN + SOC − 285.79 ST + SOC − 287.21 非生长季 Non-growing season Simpson指数 Simpson index ST + SWC + pH + HN + AK + AP + SOC + GA − 284.55 ST + SWC + pH + HN + AK + SOC + GA − 286.52 ST + SWC + pH + HN + AK + SOC − 288.46 ST + SWC + HN + AK + SOC − 289.41 Shannon-Wiener指数 Shannon-Wiener index ST + SWC + pH + HN + AK + AP + SOC + GA − 84.2 SWC + pH + HN + AK + AP + SOC + GA − 86.11 SWC + pH + HN + AK + AP + GA − 87.56 Pielou指数 Pielou index ST + SWC + pH + HN + AK + AP + SOC + GA − 180.22 SWC + pH + HN + AK + AP + SOC + GA − 182.13 SWC + pH + HN + AK + AP + GA − 183.58 注:AIC为赤池信息准则。下同。Notes: AIC,akaike information criterion.The same below. 表 8 土壤微生物功能多样性与环境因子间GLM分析
Table 8. GLM analysis of the relationship between functional diversity of soil microorganisms and environmental factors
季节
Season多样性指数
Diversity index环境因子
Environmental factorAIC β SE t P 生长季
Growing seasonSimpson指数
Simpson indexST − 428.27 1.25 × 10− 3 2.76 × 10− 4 4.525 0 0.000 9*** AK 3.12 × 10− 5 1.36 × 10− 5 2.298 0 0.038 6* Shannon-Wiener指数
Shannon-Wiener index— − 191.15 — — — — Pielou指数
Pielou index— − 287.21 — — — — 非生长季
Non-growing seasonSimpson指数
Simpson indexST − 289.41 3.47 × 10− 3 1.52 × 10− 3 2.289 0 0.031 2* SWC 2.46 × 10− 3 8.92 × 10− 4 2.754 0 0.011 0* HN 2.03 × 10− 4 3.96 × 10− 5 5.134 0 < 0.000 1*** AK − 7.74 × 10− 4 1.61 × 10− 4 − 4.808 0 < 0.000 1*** SOC − 1.44 × 10− 2 4.16 × 10− 3 − 3.471 0 0.002 0** Shannon-Wiener指数
Shannon-Wiener indexSWC − 87.56 − 0.089 1 0.025 9 − 3.455 0 0.002 2** AK 0.016 4 0.005 9 2.784 0 0.010 6* GA − 0.002 8 0.000 9 − 3.049 0 0.005 7** Pielou指数
Pielou indexSWC − 183.58 − 0.018 0 0.005 2 − 3.443 0 0.002 2** AK 0.003 3 0.001 2 2.784 0 0.010 6* GA − 0.000 6 0.000 2 − 3.050 0 0.005 7** -
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