植物生态学报  2016 , 40 (10): 991-1002 https://doi.org/10.17521/cjpe.2015.0465

Orginal Article

内蒙古羊草草原不同退化阶段土壤养分与植物功能性状的关系

李丹1, 康萨如拉1**, 赵梦颖1, 张庆12, 任海娟1, 任婧1, 周俊梅1, 王珍1, 吴仁吉1, 牛建明12**

1内蒙古大学生命科学学院, 呼和浩特 010021
2内蒙古大学中美生态、能源与可持续性科学研究中心, 呼和浩特 010021

Relationships between soil nutrients and plant functional traits in different degradation stages of Leymus chinensis steppe in Nei Mongol, China

LI Dan1, KANG Saruul1*, ZHAO Meng-Ying1, ZHANG Qing12, REN Hai-Juan1, REN Jing1, ZHOU Jun-Mei1, WANG Zhen1, WU Ren-Ji1, NIU Jian-Ming12*

1College of Life Sciences, Inner Mongolia University, Hohhot 010021, China
2Sino-US Center for Conservation, Energy and Sustainability Sciences, Inner Mongolia University, Hohhot 010021, China

版权声明:  2016 植物生态学报编辑部 本文是遵循CCAL协议的开放存取期刊,引用请务必标明出处。

基金资助:  国家重点基础研究发展规划(973计划) (2012CB722201)、内蒙古自治区科技重大专项和国家自然科学基金(31460154)

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摘要

深入认识植物功能性状的生态学含义, 对于阐明不同自然与人为干扰环境下的群落构建途径, 进一步揭示生态系统服务维持机制具有重要的理论意义。该文以内蒙古锡林河流域羊草(Leymus chinensis)草原不同退化演替阶段的群落为研究对象, 分析了土壤养分与植物功能性状的变化特征及两者之间的关系。结果表明: (1)退化导致土壤养分含量逐渐减少, 全氮和全磷在未退化的羊草+杂类草群落与严重退化的羊草+冷蒿(Artemisia frigida)群落之间差异显著; (2)随着退化演替的进程, 群落最大高度和叶片碳氮比减小, 群落最大高度在未退化的羊草+杂类草群落与轻度退化的羊草+针茅(Stipa sp.)群落之间差异显著, 碳氮比在未退化的羊草+杂类草群落与严重退化的羊草+冷蒿群落之间差异显著; (3)不同退化演替阶段的群落, 其土壤养分对植物功能性状的影响有所差异。在羊草+针茅群落, 速效氮与群落最大高度、叶片木质素含量和叶片碳氮比均呈显著负相关关系。而在羊草+糙隐子草(Cleistogenes squarrosa)群落中, 上述3种植物功能性状则表现为均与全磷含量显著正相关; (4)群落植物功能性状之间的关系也因退化阶段不同而有所不同。在轻度退化的羊草+针茅群落中, 叶片木质素含量与其他4个功能性状显著正相关, 叶片碳氮比与群落最大高度、叶干物质含量、木质素含量呈显著正相关关系。在严重退化的羊草+冷蒿群落中, 所有性状均呈极显著正相关关系。表明植物通过功能性状的协调或组合, 以适应贫瘠的土壤环境。上述结果深化了对典型草原退化演替的认识, 对退化草地的恢复与保护具有一定的指导意义。

关键词: 植物功能性状 ; 土壤养分 ; 退化演替 ; 羊草草原 ; 锡林河流域

Abstract

Aims Understanding ecological implications of plant functional traits is helpful in exploring community assembly under different environments of nature and human disturbances, and then to reveal the maintenance mechanism of the ecosystem services. By analyzing vegetation and soil data derived from field observations in Leymus chinensis steppe of Xilin River Basin in Nei Mongol, we aimed to explore the responses of plant functional traits to changing soil nutrients at different degradation stages. Methods We observed 69 plots for both plant community structure and soil attributes using quadrat and soil-drilling methods. Five plant functional traits, namely the specific leaf area (SLA), leaf dry matter content (LDMC), leaf carbon to nitrogen ratio (C:N), leaf lignin content (LLC), and maximum height (MH), were measured for each plot. We also tested soil attributes, such as total nitrogen (TN), total phosphorus (TP), available nitrogen (AN), available phosphorus (AP), and organic carbon (OC). The sixty-nine communities were classified into four groups (undegraded L. chinensis + forbs, slightly degraded L. chinensis + Stipa sp., moderately degraded L. chinensis + Cleistogenes squarrosa, and heavily degraded L. chinensis + Artemisia frigida) using TWINSPAN software. The relationships between plant functional traits and soil nutrient variables were analyzed for the four community groups using the Pearson’s correlation test with SPSS 21.0 software. Important findings (1) The soil nutrients decreased with the grassland degradation process and there were significant differences in TN and TP between the undegraded L. chinensis + forbs and heavily degraded L. chinensis + A. frigida communities; (2) plant functional traits also showed strong differences between the degradation stages. MH and C:N decreased with degradation. A significant difference was observed in MH between the undegraded L. chinensis + forbs and slightly degraded L. chinensis + Stipa sp. communities. The difference in C:N was also significant between the undegraded L. chinensis + forbs and heavily degraded L. chinensis + A. frigida communities; (3) the effects of soil nutrients on plant functional traits changed with grassland degradation. AN was negatively correlated with MH, LLC, and C:N in the slightly degraded L. chinensis + Stipa sp. community. In the moderately degraded L. chinensis + C. squarrosa community, those three traits mentioned above showed significantly positive correlations with TP; (4) while analyzing the degraded grassland, different relationships between plant functional traits were found. In the slightly degraded L. chinensis + Stipa sp. community, LLC was positively correlated with all other traits. Moreover, positive correlations also occurred between C:N and MH, C:N and LDMC, and C:N and LLC. In the heavily degraded L. chinensis + A. frigida community, all traits demonstrated the most significantly positive correlations.

Keywords: plant functional traits ; soil nutrient ; degradation succession ; the Leymus chinensis steppe ; Xilin River Basin

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李丹, 康萨如拉, 赵梦颖, 张庆, 任海娟, 任婧, 周俊梅, 王珍, 吴仁吉, 牛建明. 内蒙古羊草草原不同退化阶段土壤养分与植物功能性状的关系. 植物生态学报, 2016, 40(10): 991-1002 https://doi.org/10.17521/cjpe.2015.0465

LI Dan, KANG Saruul, ZHAO Meng-Ying, ZHANG Qing, REN Hai-Juan, REN Jing, ZHOU Jun-Mei, WANG Zhen, WU Ren-Ji, NIU Jian-Ming. Relationships between soil nutrients and plant functional traits in different degradation stages of Leymus chinensis steppe in Nei Mongol, China. Chinese Journal of Plant Ecology, 2016, 40(10): 991-1002 https://doi.org/10.17521/cjpe.2015.0465

植物功能性状是植物长期对外界环境适应的产物, 并且与生态系统过程和功能关系密切(孟婷婷等, 2007; 习新强等, 2011)。群落中不同物种性状的分布是生境过滤与种间相似性限制共同作用的结果(Díaz et al., 1998; Bernard-Verdier et al., 2012), 相同物种在不同群落中的性状差异则表征了其环境可塑性(Violle et al., 2007; 习新强等, 2011)。可见, 植物功能性状是植物联系环境的纽带。近年来, 作为植被-环境关系研究的新证据, 植物功能性状已应用于古植被恢复(Gachet et al., 2003; 陈瑜和倪健, 2008)与古气候重建(Barboni et al., 2004)、生态恢复(孟婷婷等, 2007; 宋彦涛等, 2013)、群落构建(牛红玉等, 2011)等领域的研究中。

有关环境因子对植物功能性状的影响研究, 学者们多关注气候(温度、降水等)(Roderick et al., 2000; 宋立宁等, 2012)、地形地貌(海拔、坡度、坡向等)(李琪佳等, 2015)等自然环境因子, 以及放牧活动(王炜等, 2000; 李西良等, 2015)等人为干扰因子, 土壤因子与植物功能性状关系的研究相对不足, 且结论也不尽相同。土壤被认为是群落植物功能性状的主导者, 例如其对比叶面积等性状的变异解释了33%-60% (Becknell & Powers, 2014), 与叶面积等的变异也密切相关(Liu et al., 2012)。但是, 起决定作用的因素并没有一致性认识。就森林生态系统而言, 土壤含水量和全氮含量是影响亚热带常绿阔叶林植物功能性状变异的主要因素(丁佳等, 2011); 而在热带雨林老龄林中, 起关键作用的是土壤有机质含量和总磷含量(卜文圣等, 2013)。基于小尺度草地生态系统的控制实验发现, 土壤氮(N)、磷(P)含量与叶片N、P含量之间相互影响强烈(Fujita et al., 2013), 添加氮素显著提高了草本植物叶片N的含量, 虽然不同植物的响应程度各异(万宏伟等, 2008)。另一方面, 土壤养分能够引发多个独立功能性状的协调反应, 例如土壤肥力与比叶面积、叶片N、P含量正相关, 与叶片厚度、叶干物质含量负相关, 土壤C:N是主要的决定因子(Jager et al., 2015); 然而, 土壤养分的高低调控着其与植物功能性状的关系, 当土壤养分条件较差时, 土壤N含量与比叶面积显著负相关(García-Palacios et al., 2013)。可见, 土壤与植物功能性状的关系十分复杂, 性状以及性状之间的联系随着土壤与干扰的变化而变化, 说明植物通过不同的策略以适应不同的环境(Kühner & Kleyer, 2009), 性状组合的权衡可能是土壤养分作用于植物群落构建的重要机制之一, 进而影响着生态系统的功能与过程(Schellberg & Pontes, 2012)。因此, 有必要加强该领域的研究, 通过多方面的证据, 进一步探讨土壤对于植物功能性状的作用。

草地的退化不仅包括地上部分植被的衰退, 还会导致土壤养分的贫瘠与土壤质地的粗糙化(高英志等, 2004), 进而重塑了植被-环境关系。因此, 有必要从土壤养分与植物功能性状关系的视角, 进一步探讨放牧驱动下群落演替机制。本文以内蒙古锡林河流域羊草(Leymus chinensis)草原为研究对象, 通过分析不同退化演替阶段植物群落土壤养分与植物功能性状特征及其相关关系和动态, 探究典型草原生态系统中土壤养分对植物功能性状的作用, 阐明草地退化过程中植物功能性状对变化的土壤养分的响应, 其结果不仅有助于深化对典型草原退化演替的认识, 而且也能够为合理利用草地资源, 促进草地生态系统恢复与保护提供参考。

1 材料和方法

1.1 研究区概况

锡林河流域位于内蒙古自治区中部(43.43°- 44.65° N, 115.53°-117.20° E), 海拔1200-1250 m。该流域属于大陆性温带半干旱气候, 年平均气温-1.3-2.1 ℃, 年降水量350 mm。研究区域的土壤以栗钙土为主, 植被以典型草原占优势, 主要类型有羊草、大针茅(Stipa grandis)和克氏针茅(S. krylovii)草原等。羊草草原分布在地势低洼、地表平坦的阶地与平原, 以及丘坡下部与丘间, 由于长期的过度放牧, 该区域的羊草草原发生了明显的退化, 呈现出向针茅群落、糙隐子草(Cleistogenes squarrosa)群落和冷蒿(Artemisia frigida)群落的阶段性演替(刘钟龄等, 1998; 吴璇等, 2011)。

1.2 取样

2014年7月22日至8月8日在锡林河流域(43.43°- 44.65° N, 115.53°-117.20° E)进行野外调查与取样。依据地形地貌与植被特征, 共设置69个样地(图1), 获取植物群落基本数据, 采集植物和土壤样品。

植物群落调查采用样方法。每个样地在10 m × 10 m的范围内随机设置10个1 m × 1 m的样方, 分别记录每个样方中物种出现的频度。其中3个样方用于分种测产, 分别记录植物的营养枝高度、生殖枝高度, 且将植物齐地面剪下, 称取鲜质量并保存, 带回实验室后, 65 ℃烘干至恒质量, 称取干质量。

对频度大于20%的物种进行植物功能性状测定, 每个物种取6株未被采食的完整个体, 用米尺计测垂直株高, 记录每株植物叶片数; 分株装袋带回室内, 采用LI-3000C手持式激光叶面积仪(LI-COR, Lincoln, USA)测定叶面积, 随后将这些植物叶片烘干至质量恒定后, 称取叶干质量。采集频度大于20%物种的新鲜植株叶片, 带回实验室烘干至恒质量, 测定叶片木质素含量和碳氮比。

图1   样地分布图。

Fig. 1   The distribution map of observation sites.

使用直径6.8 cm的土钻获取土壤样品。在上述3个分种样方中各设有1钻, 共3钻, 钻取0-30 cm深度的土壤, 带回实验室。将3钻土样混合均匀, 过100目筛, 测定土壤全氮、全磷、速效氮、速效磷和有机碳。

1.3 植物与土壤指标的测定方法

1.3.1 植物功能性状

选取比叶面积(specific leaf area, SLA)、叶干物质含量(leaf dry matter content, LDMC)、最大高度(maximum height, MH)、叶片碳氮比(leaf carbon and nitrogen ratio, C:N)以及木质素含量(leaf lignin content, LLC)等5个代表性的植物功能性状。SLA=叶面积/叶干质量, 其值均为实测值, 它能够指示植物光合速率、相对生长速率和营养利用效率等情况(Wilson et al., 1999); LDMC=叶干质量/叶鲜质量, 其值为实测值, 它与资源利用、组织密度等生态功能紧密相关(Wilson et al., 1999); MH为植株底部到顶部的垂直距离的实测值, 体现了植物资源竞争能力以及繁殖策略(Westoby et al., 2002); 植物叶片C:N能够表示植物吸收营养所能同化碳的能力, 反映了植物的养分利用效率(Thompson et al., 1997; 杨惠敏和王冬梅, 2011); 植物叶片木质素含量代表了植物对放牧等逆境的应对策略(Griffiths & Gordon, 2003)。此外, 叶片碳、氮含量使用元素分析仪(VARIO EL III, Elementar Analysensysteme Gmbh, Hanau, Germany)测定; 叶片木质素含量采用紫外/可见光分光光度计(UV2300, 天美, 上海)测定, 并采用饲料中酸性洗涤木质素(GB/T20805- 2006)的方法进行检验。

采用Ackerly和Cornwell (2007)提出的方法, 获得每个样地的群落平均性状:

$$ \overline{P}_j =\frac{\sum_{i=1}^s a_{ij}\times t_{ij}}{\sum_{i=1}^s a_{ij}}$$

式中: 物种i在样地j中的权重系数是aij, t代表植物功能性状, S代表样地中出现的物种数,͞͞ Pj代表群落平均性状(Ackerly & Cornwell, 2007)。权重系数使用频度大于20%的物种在样地内的相对干质量与相对频度的平均值。

1.3.2 土壤

土壤养分指标包括土壤全氮(total nitrogen, TN)、速效氮(available nitrogen, AN)、全磷(total phosphorus, TP)、速效磷(available phosphorus, AP)和有机碳(organic carbon, OC), 其测试方法参考《土壤农化分析》第二版(南京农业大学, 1998)。土壤全氮含量测定采用凯氏定氮法; 速效氮(水解性氮)采用硼酸-氢氧化钠碱解土壤-扩散吸收法; 全磷采用硫酸-氢氧化钠熔融-钼锑抗比色法; 速效磷采用碳酸氢钠浸提-钼锑抗比色法; 有机碳采用重铬酸钾氧化外加热法(南京农业大学, 1998)。

1.4 统计分析

首先, 计算每个样地植物相对干质量并作为重要值, 获得物种-样地的重要值矩阵, 并利用TWINSPAN软件对69个样地进行群落分类; 其次, 采用单因素方差分析中Scheffe方法分别对4种群落植物功能性状与土壤养分含量进行差异显著性分析, 阐明群落演替过程中土壤养分和植物功能性状的变化特征; 最后, 利用Pearson相关性分析, 明晰植物功能性状与土壤养分含量之间和植物功能性状之间的关系, 探讨植物功能性状应对土壤养分变化的策略。采用IBM SPSS Statistics 21.0软件进行上述差异显著性与相关性分析。

2 结果

2.1 群落演替阶段划分

依据TWINSPAN群落分类结果(附录I)将69个样地划分为4个不同演替阶段类型: 未退化的羊草+杂类草群落、轻度退化的羊草+针茅群落、中度退化的羊草+糙隐子草群落和重度退化的羊草+冷蒿群落, 各类型包含的样地数量分别为22个、18个、21个和8个。

2.2 土壤养分变化特征

对土壤养分进行差异显著性分析的结果见图2。TN、TP随着退化演替逐渐减少, 并在羊草+杂类草群落与羊草+冷蒿群落之间呈现显著差异(p < 0.05); AN也随着退化演替逐渐减少, 并在羊草+杂类草群落与羊草+针茅群落之间呈现显著差异(p < 0.05); AP与OC则无显著差异。

2.3 植物功能性状变化特征

群落植物功能性状也随着退化演替发生了变化。如图3所示, MH随着退化演替整体呈现减小趋势, 并在羊草+杂类草群落与羊草+针茅群落之间差异显著(p < 0.05); C:N在演替前期逐渐增加, 但是在严重退化的羊草+冷蒿群落中达到最小值, 并与羊草+杂类草、羊草+糙隐子草群落之间呈现显著差异(p < 0.05)。SLA、LDMC和LLC差异不显著。

2.4 土壤养分含量与植物功能性状的关系

土壤养分含量特别是AN与TP对植物功能性状影响较为突出(表1)。在羊草+针茅群落中, 土壤AN与MH、LLC、C:N均呈显著的负相关关系。在羊草+糙隐子草群落中, 土壤TP与MH、LLC、C:N均表现出显著的正相关关系。另一方面, 植物功能性状在不同演替阶段, 受到不同土壤营养元素的调控。在羊草+杂类草群落中, C:N与AN、AP都显著负相关。在羊草+针茅群落中C:N只与AN极显著负相关。在羊草+糙隐子草群落中, C:N则与TP极显著正相关。而在羊草+冷蒿群落中, 植物功能性状与土壤养分无显著相关性。

表1   土壤养分含量与植物功能性状之间的关系

Table 1   Relationships between soil nutrient contents and plant functional traits

类型
Type
指标
Index
全氮
TN
速效氮
AN
全磷
TP
速效磷
AP
有机碳
OC
羊草+杂类草
Leymus chinensis + forbs
SLA-0.074-0.2080.128-0.2470.007
MH-0.1180.0980.0310.048-0.167
LDMC0.2250.2970.2080.0900.244
LLC-0.361-0.196-0.218-0.316-0.268
C:N-0.275-0.571**-0.043-0.534*-0.126
羊草+针茅
Leymus chinensis + Stipa sp.
SLA-0.051-0.3050.1060.1470.019
MH-0.398-0.515*-0.037-0.214-0.395
LDMC0.061-0.3490.2040.1420.054
LLC-0.384-0.667**-0.102-0.126-0.382
C:N-0.203-0.697**0.068-0.114-0.208
羊草+糙隐子草
Leymus chinensis + Cleistogenes squarrosa
SLA0.052-0.0780.034-0.1030.144
MH0.3710.2100.477*-0.0960.222
LDMC0.306-0.2570.3760.2930.049
LLC0.509*-0.0660.514*0.1810.286
C:N0.223-0.3620.562**0.262-0.029
羊草+冷蒿
Leymus chinensis + Artemisia frigida
SLA0.5190.1270.3090.2800.416
MH0.4320.1400.2360.2540.332
LDMC0.4040.3050.2020.1590.329
LLC0.3540.1440.1320.1430.250
C:N0.6080.3420.4410.2600.526

** , p < 0.01; *, p < 0.05. C:N, leaf carbon and nitrogen ratio; LDMC, leaf dry matter content; LLC, leaf lignin content; MH, maximum height; SLA, specific leaf area. AN, available nitrogen; AP, available phosphorus; OC, organic carbon; TN, total nitrogen; TP, total phosphorus.** , p < 0.01; *, p < 0.05。C:N, 叶片碳氮比; LDMC, 叶干物质含量; LLC, 叶片木质素含量; MH, 最大高度; SLA, 比叶面积。

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2.5 植物功能性状之间的关系

在不同的演替阶段, 植物功能性状之间表现出不同的关系(表2)。就羊草+杂类草群落而言, SLA与LDMC显著负相关, LLC与MH和C:N显著正相关; 在羊草+针茅群落中, 多数性状之间表现为显著的正相关关系, 如LDMC与MH, C:N与MH、LDMC和LLC, LLC与其他4个性状之间均呈现显著正相关; 在羊草+糙隐子草群落中, LLC与MH和LDMC显著正相关; 在羊草+冷蒿群落中, 所有性状之间都呈现极显著正相关关系。

图2   不同退化阶段土壤养分含量比较(平均值±标准误差)。I, 羊草+杂类草; II, 羊草+针茅; III, 羊草+糙隐子草; IV, 羊草+冷蒿。ns, 群落间差异不显著。每个子图中不同字母表示不同演替阶段之间差异显著(p < 0.05)。

Fig. 2   Comparison of soil nutrient among different degradation stages (mean ± SE). I, Leymus chinensis + forbs; II, Leymus chinensis + Stipa sp.; III, Leymus chinensis + Cleistogenes squarrosa; IV, Leymus chinensis + Artemisia frigida. ns refers to no significant difference at p > 0.05. Letters in each subgraph indicate significant differences between stages (p < 0.05). AN, available nitrogen; AP, available phosphorus; OC, organic carbon; TN, total nitrogen; TP, total phosphorus.

图3   不同退化阶段植物功能性状比较(平均值±标准误差)。I, 羊草+杂类草; II, 羊草+针茅; III, 羊草+糙隐子草; IV, 羊草+冷蒿。ns, 群落间差异不显著。每个子图中不同字母表示不同演替阶段之间差异显著(p < 0.05)。

Fig. 3   Comparison of plant functional traits among different degradation stages (mean ± SE). I, Leymus chinensis + forbs; II, Leymus chinensis + Stipa sp.; III, Leymus chinensis + Cleistogenes squarrosa; IV, Leymus chinensis + Artemisia frigida. ns refers to no significant difference at p > 0.05. Letters in each subgraph indicate significant differences between stages (p < 0.05). C:N, leaf carbon and nitrogen ratio; LDMC, leaf dry matter content; LLC, leaf lignin content; MH, maximum height; SLA, specific leaf area.

表2   植物功能性状之间的关系

Table 2   Relationships among plant functional traits

类型
Type
指标
Index
比叶面积
SLA
最大高度
MH
叶片干物质含量
LDMC
叶片木质素含量
LLC
叶片碳氮比
C:N
羊草+杂类草
Leymus chinensis + forbs
SLA10.015-0.435*-0.0500.268
MH1-0.0050.527*0.309
LDMC10.021-0.102
LLC10.575**
C:N1
羊草+针茅
Leymus chinensis + Stipa sp.
SLA10.4340.4250.603**0.406
MH10.518*0.681**0.565*
LDMC10.493*0.634**
LLC10.693**
C:N1
羊草+糙隐子草
Leymus chinensis +
Cleistogenes squarrosa
SLA1-0.128-0.0800.0880.184
MH10.3300.520*0.232
LDMC10.735**0.356
LLC10.388
C:N1
羊草+冷蒿
Leymus chinensis +
Artemisia frigida
SLA10.961**0.838**0.935**0.944**
MH10.854**0.919**0.892**
LDMC10.953**0.842**
LLC10.906**
C:N1

** , p < 0.01; *, p < 0.05. C:N, leaf carbon and nitrogen ratio; LDMC, leaf dry matter content; LLC, leaf lignin content; MH, maximum height; SLA, specific leaf area.** , p < 0.01; *, p < 0.05。C:N, 叶片碳氮比; LDMC, 叶干物质含量; LLC, 叶片木质素含量; MH, 最大高度; SLA, 比叶面积。

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3 讨论

3.1 草地退化改变了土壤养分含量与群落植物功能性状特征

研究表明, 草地退化导致土壤贫瘠(王明君等, 2010; 萨茹拉等, 2013)。本文针对锡林河流域羊草草原的研究也得到了一致的结果, 随着退化演替的加剧, 土壤全氮、速效氮和全磷含量呈现出减少的趋势, 并且全氮和全磷在演替过程的两端之间达到显著差异。大量研究认为, 放牧是导致研究区域草

地退化的最重要因素(李博, 1997; 姜晔等, 2010)。持续、高强度的放牧利用不仅使草地地上生物量降低, 群落结构发生变化, 推动逆行演替, 更重要的是减少了土壤氮、磷等养分含量, 进而影响生态系统养分循环, 削弱生态系统服务功能。

草地退化形成了新的土壤养分含量低的环境, 而植物可以通过调节外部形态结构及内部生理特征来适应这种环境, 并且将这种变化体现在植物功能性状特征上(冯秋红等, 2008; 龚时慧等, 2011)。我们发现, 群落水平的植物功能性状随着退化演替发生了改变, 最大高度和叶片碳氮比随着退化整体呈现降低趋势。最大高度的降低一方面可能与植物分配策略有关——在放牧胁迫下, 植物忽略其高度成本, 将物质投入到地下部分或单位干物质含量, 以达到生产力的最大化(Westoby et al., 2002); 另一方面, 植物通过个体小型化的途径, 躲避牲畜的采食(王炜等, 2000; 李建玮等, 2012)。而在人为干扰较少的群落中, 资源竞争促使植物转向高度投入, 以获得更多光能和增强繁殖能力(Ackerly & Cornwell, 2007; Bernard-Verdier et al., 2012)。植物叶片碳氮比可表示植物吸收营养所能同化碳的能力, 在一定程度上反映了植物的营养利用效率, 同时也指示了对土壤因子等环境变化的适应(Thompson et al., 1997)。在低的养分条件下, 植物的生长虽然缓慢, 但养分利用效率较高, 具有高的碳氮比(杨惠敏和王冬梅, 2011)。本文发现植物叶片碳氮比随着退化演替先逐渐增加, 符合上述观点, 但是在严重退化阶段又明显下降, 这可能与过度放牧有关。放牧提供了植物再生的机会, 氮含量则会不断增加(牛得草等, 2011), 而植物体内碳含量相对稳定, 因此植物碳氮比更多地受到氮含量的影响, 在严重退化的群落里碳氮比则达到最低(银晓瑞等, 2010; 牛得草等, 2011)。

3.2 草地退化改变了土壤养分与群落植物功能性状之间的关系

植物功能性状能够客观地反映植物对土壤等外部环境的响应与适应(McIntyre et al., 1999)。尤其对土壤氮、磷的变化具有显著的响应(杨浩和罗亚晨,2015)。在草地生态系统中, 植物的生长发育主要受氮素的限制(Bai et al., 2010; LeBauer & Treseder, 2008)。或者由于氮沉降的加剧, 草地生态系统可能由氮限制逐渐转向受氮、磷共同限制(Craine et al., 2008)。氮素添加使得比叶面积、叶片面积、植株高度和叶片氮含量均有所增加(潘庆民等, 2005; 万宏伟等, 2008; 白雪等, 2014), 磷添加对植物的地下性状影响更大(詹书侠等, 2016)。可见土壤氮、磷水平的高低, 能够引起群落植物功能性状的变化(白雪等, 2014; 毛伟等, 2014)。我们发现, 在样地水平或就某一具体的退化阶段而言, 土壤速效氮与植物叶片碳氮比之间显著负相关, 说明植物叶片碳氮比主要受到土壤氮素的限制, 随着土壤氮含量降低, 植物叶片氮含量也随之减小, 而植物叶片结构性碳的稳定性决定了植物叶片碳氮比随之增加(银晓瑞等, 2010; 牛得草等, 2011)。另一方面, 随着羊草草原的退化, 土壤氮素呈减少趋势(图2), 群落发生演替, 群落叶片碳氮比和高度也呈现减小趋势(图3)。即土壤氮素含量不同, 所形成的群落类型也不同, 因此群落的一些植物功能性状也发生了改变。由此推测, 土壤氮素可能是通过调控群落的物种组成与结构成为羊草草原退化演替群落构建的关键筛选要素。

土壤养分与群落植物功能性状之间的关系随着草地退化的加剧受到不同土壤营养元素的限制, 并且在退化演替的中期二者表现出密切的相关性。最大高度、叶片木质素含量和叶片碳氮比都是权衡资源分配及利用的代表性功能性状, 在羊草+针茅群落中, 三者与速效氮显著负相关; 在羊草+糙隐子草群落中, 三者则与全磷显著正相关, 进一步表明了植物功能性状对土壤养分依赖的敏感程度。植物功能性状是群落物种组成与结构的表征(Ackerly & Cornwell, 2007; Cornwell & Ackerly, 2009; Bernard- Verdier et al., 2012), 可见, 在羊草草原中度退化阶段, 土壤养分特别是氮和磷, 对于群落构建具有重要影响, 土壤元素对植物功能性状的调控更为强烈(Bernard-Verdier et al., 2012)。在重度退化的羊草+冷蒿群落阶段, 土壤养分与植物功能性状之间没有显著相关性, 可能是由于一方面草地退化是一个较为缓慢的过程, 随着退化的加剧, 土壤养分的筛选作用已经逐渐完成(Bernard-Verdier et al., 2012), 群落由适应能力强的物种占优势, 植物功能性状对土壤养分的变化不敏感; 另一方面, 土壤的其他特征如紧实度、机械组成等属性均发生了显著变化(李博, 1997; 张成霞和南志标, 2010), 共同作用于植物功能性状, 削弱了土壤养分对植物功能性状的影响, 例如羊草+冷蒿群落的土壤更趋于沙质化。

3.3 草地退化改变了群落植物功能性状之间的协调关系

植物功能性状对土壤条件变化的响应不仅仅反映在其本身的变化上, 也反映在功能性状之间的组合上(Kühner & Kleyer, 2009; 任海彦等, 2009; 杨冬梅等, 2012)。前人研究表明, 植物功能性状之间存在多种协同关系, 而且会发生改变。如在资源丰富的条件下, 较大的比叶面积与较高的光合速率相对应, 以适应多物种共存的竞争性环境(冯秋红等, 2008); 在资源贫乏的条件下, 较小的比叶面积和较大的叶片厚度和较低的叶片氮含量相对应, 以便高效地利用有限的资源(Bernard-Verdier et al., 2012)。我们发现, 在羊草+针茅群落中叶片木质素含量与其他所有性状显著正相关, 碳氮比与最大高度、叶干物质含量、叶片木质素含量均显著正相关, 说明在某种环境状况下这两种功能性状与其他性状之间是协同变化的(韦兰英和上官周平, 2008)。在羊草+冷蒿群落中, 植物功能性状之间均呈极显著正相关关系, 表明在草地严重退化的状态下, 植物通过多种功能性状的协同变化来调整对资源利用与分配的策略, 以应对极端的土壤条件(冯秋红等, 2008; 习新强等, 2011; 李西良等, 2015)。

综上所述, 草地退化不仅表现在植物群落结构的改变、生产力的衰退等方面, 由于受到土壤养分供给的限制, 群落植物功能性状特征也发生了深刻的变化。随着退化的不断加剧, 土壤养分逐渐减少, 植物功能性状发生了显著的变化, 土壤养分与植物功能性状之间的关系越来越密切, 表明土壤养分对植物功能性状具有重要的筛选作用。研究结果进一步揭示了土壤养分在羊草草原退化演替中的作用以及调控植物群落构建的机制, 有助于深入认识草地退化现象, 对于合理利用草地资源, 促进草地生态系统恢复与保护实践也具有重要参考价值。

图4   附录I TWINSPAN群落分类结果^顶端两行数字纵列代表样地编号, 从左至右如: 19、61、25至6样地; 每一行的左侧(前11个字符, 含空格)代表植物种编号, 其中Var是”变量”的缩写; 右侧0、1组合代表物种的分类;表格中央部分的数字与短线表示物种在样地中的重要性, 5代表最重要, 短线代表可以忽略; 表格底部的6行是样地分类结果, 0、1代表不同类群, 首先将样地划分为两类(倒数第6行), 接下来(倒数第5行)是对上述两个类群的再次划分(二分法), 形成4个类群, 以此类推。

Fig.4   Appendix I The result of TWINSPAN classification^ Site numbers are shown in vertical sequence (top-down) by the first two lines on the top of the table. The first three sites coded 19, 61, and 25, for example, are at the very beginning on the left, and the last one is site 6 on the right end. Code of plant species is shown on the very left (the first 11 chars, including blanks) for each line. Var is the abbreviation of “variable”. A group of 0 and 1 on the right demonstrates the classification of plant species; Numbers and dashes appeared in the central part of the table indicate the value of species in sites. The number 5 refers to the most important, and the sign of dash illustrates that the value of species in sites can be neglected; Results of site classification are summarized by the last 6 lines at the bottom of the table, 0 and 1 refer to differentiation. At first, all sites are categorized to 2 groups shown in the line 6 from the end. And then, these two groups are classified further into 4 groups (in the line 5 from the end) by means of dichotomy, and so forth.

致谢 感谢内蒙古农牧渔业生物实验研究中心的各位老师在样品室内分析工作中给予的帮助。

The authors have declared that no competing interests exist.

作者声明没有竞争性利益冲突.


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