草地生物土壤结皮

马 洁，陈先江，侯扶江

(草地农业生态系统国家重点实验室 兰州大学草地农业科技学院，甘肃 兰州 730020)



草地生物土壤结皮

马 洁，陈先江，侯扶江

(草地农业生态系统国家重点实验室 兰州大学草地农业科技学院，甘肃 兰州 730020)

摘要：生物土壤结皮是由隐花植物与土壤中的细菌、真菌以及土壤颗粒结合形成的复杂生物覆盖体,它们广泛分布于世界上各草地类组中，在改善生态环境和防治草地退化方面起到了积极的作用。多年来，国内外学者就相关问题开展了大量的研究，但总体来说，主要研究仍集中在对其功能和作用的认知方面，而对全球变化背景下生物土壤结皮的演变以及它们维护生态系统稳定性机理方面的研究还十分欠缺。本文综述了国内外该领域的现有研究成果，讨论了目前研究的不足以及未来的研究方向，以期促进生物土壤结皮相关研究，加深对草地生态系统土壤演替过程的认识。

关键词：土壤结皮；组成多样性；分布；生态功能；研究展望

草地是面积最大的陆地生态系统，具有改良土壤、调节气候、净化环境、维持物种多样性等的作用[1]。随着人类活动加强，草原不合理利用，加之全球气候变化，草地面积减少、生产力下降，制约了农牧业生产和人民生活的提升。草地退化及其生态恢复已经成为世界性问题[2],从生物土壤结皮(biological soil crusts)的角度，揭示草地退化和恢复机制是其中的重要方面[3-4]。

草地生物土壤结皮是由生活于草地土壤表面的非维管束植物(蓝藻、绿藻、硅藻、地衣和苔藓)和微生物(土壤细菌、真菌等)，与土壤颗粒通过团聚和胶结作用在土壤表层形成的复合生物体[5]。它能固定大气中的氮、碳，增加土壤有机质，改良土壤[6]，在荒漠草地中的盖度甚至超过生物总盖度的40%[7]。生物土壤结皮往往出现在高等植物分布受限的环境或者植物之间的空地上，生物种类不易辨别，所以长期受到忽视。20世纪90年代以后，人们发现生物土壤结皮在防止草地退化等方面有重要作用，其研究逐渐引起人们的重视，对它的保护已被列入草地生态系统管理尤其是荒漠草地管理的优先等级[8]。此后，国内外学者对生物土壤结皮的时空格局、生物组成、形态结构、生态功能和管理等开展了全面研究[9]。

1草地生物土壤结皮的组成及演替

生物土壤结皮群落主要由自养生物体和异养生物体组成。前者主要包括藻类(algae)、地衣(lichen)和苔藓(moss)等，其光合作用是结皮群落生产力的主要来源；后者主要包括细菌(bacteria)、微小真菌(microfungi)等，在结皮中起分解和代谢作用[10]。它们利用菌丝体、假根以及分泌物胶结微小的土壤颗粒和大气降尘，团聚成厚度为3～10 mm的毯状结构覆盖在地表，成为草地生态系统的“系统工程师”[11]。根据生物土壤结皮群落中优势生物组分，可以划分为藻类结皮、地衣结皮和苔藓结皮[12]，各类型结皮的形态、功能各异，组成成分具有多样性。

藻类结皮是生物土壤结皮演替的最初阶段。它以物理结皮和微生物结皮为基础，随着时间的推移，微环境条件改善，沙粒间隙被大气降尘所填充，细菌分泌的胞外多糖黏结形成表面细致平滑的无机层，藻类出现并迅速繁殖[13-14]。生物土壤结皮中蓝藻(Cyanobacteria)的种类和数量比例较高[15]。藻类对土壤类型的适应性因种而异，不同区域的群落组成差异性较大。譬如黄土高原3个侵蚀区藻类的种类组成及优势种均有差异[16]。藻类虽不易被肉眼观察到，但有藻类的土壤表面一般会有相对应的色斑，蓝细菌占优势的结皮往往呈现蓝绿色或黑色，而绿藻会在土壤湿润时呈绿色[17]。藻类能够显著提高土壤的酶活性和土壤肥力，促进藻类结皮发育成地衣或苔藓结皮[18-19]。

地衣是藻类和菌类的共生体，它具有菌丝和假根等，能够黏结土壤，穿透沙土表层并紧密连接叶状体，形成稳定的结皮形态，进而抵御风水侵蚀，促进有机物累积[20]。草地生态系统中地衣的盖度与地表环境的稳定性相关，可以指示环境的变化[21]。美国西部、哥伦比亚等地广泛存在着地衣结皮[22]。腾格里沙漠、沙坡头地区也鉴定出分属于5目13科16属的地衣植物22种[23]。地衣结皮的颜色呈现黑、褐、白、绿色，表面呈凹凸不平的壳状，可以通过形态特征与藻类结皮相区别[24]。

苔藓结皮是生物土壤结皮发育和演替的最高阶段，能显著加快矿物质风化的速度，积累营养元素供植物生长[25]。古尔班通古特沙漠的垄间低地生存着以刺叶墙藓(Tortuladesertorum)和真藓为优势种的苔藓植物[26]，沙坡头有真藓为优势种的2科7属共16种苔藓植物[27]。苔藓结皮的多度和盖度与土壤粘粒含量呈正比，土表粗糙度的增加有利于种子萌发及植物的侵入、定居[28-30]。生长后期，苔藓结皮呈现较深的颜色，有效吸收光照，下层土壤在寒冷的天气下保持较高的温度，以保证土壤微生物的生长活动[31](表1)。

一般情况下，生物土壤结皮的演替始于大型丝状蓝细菌等藻类定殖；随着地表固定和土壤基质的改善，地衣和苔藓开始生长，结皮自身的蓄水、抗机械干扰以及固沙能力依次增强(图1)。这个过程中，组成植物种从低等到高等，种群丰富度和群落多样性从小到大[42]。但是当环境条件适宜时，结皮的演替也可能不经过其中一个阶段而直接发育到更高级的阶段。在生物结皮成为典型特征的地域，密集频繁的放牧、旅游和火烧等造成生物土壤结皮减少，甚至向上一个阶段退化[43]。

2影响草地结皮分布的因素

生物土壤结皮能够适应多种气候条件和土壤生境，对外界胁迫具有一定抗性，在世界各类草地生态系统中多有分布[44]。生物土壤结皮的组成、发育以及盖度、多度等存在地域间甚至地域内的差异。

在全球或区域尺度上，生物土壤结皮的分布主要受气候影响。结皮的酶活性、新陈代谢速率、生理活动与温度和降水密切相关[45]。降水较多，则适宜形成以苔藓为优势种的生物土壤结皮[46]。温度变化会改变地面的蒸散特征，不利于对温度敏感的结皮生物的生长。温度升高会影响结皮在夜间捕获凝结水的能力，从而缩短其生物活性[47]。

在景观尺度上，土壤的质地和化学特性影响着生物结皮群落组成，土壤颗粒是主导因素。土壤质地较细能提高藻类、地衣、苔藓的盖度和物种丰富度[48]。碱性土壤适宜蓝藻类结皮的发育，绿藻则偏好酸性土壤；土壤碳酸钙含量高促进地衣定植[49]。蓝藻的丰富度与钠、镉、锂、铜、钼、锶含量呈负相关，与铅和锌含量呈正相关[50]。

在生态系统尺度上，生物结皮的分布对地貌部位有强选择性。在古尔班通古特沙漠，藻结皮主要分布于沙垄坡部, 从沙坡至丘间低地，逐渐演替为连片分布地衣结皮和斑块状的与地衣镶嵌而生的苔藓结皮，同时生物结皮的盖度、厚度、抗压性从垄间至垄顶逐渐减小[51]。

表1　各类草地生物土壤结皮群落组成多样性Table 1　Community composition diversity of biological soil crusts in several types of grassland

在群落尺度上，同一生境中的高等植物与生物结皮的形成有密切联系。一般盖度高的植被遮蔽光照和降水，结皮生物体无法与其竞争资源；植被稀疏的荒漠，高等植物的生长受水分限制而呈斑块状[52]，斑块之间的裸地为生物土壤结皮提供了空间、水分和光照，这也是生物土壤结皮主要集中于干旱、半干旱地区的原因之一。

人类活动是影响生物土壤结皮分布的重要因素。放牧、旅游和火烧等高强度的活动会导致结皮减少甚至消失。放牧家畜的践踏集中作用于土壤表面的结皮层，对微生物的数量分布及其碳氮代谢产生明显作用[53]。火烧是常用的生态系统管理手段，生物土壤结皮对轻度火烧具有一定的适应性，且轻度火烧可消除地表的凋落物，减少高等植物的生物量，有利于结皮的再形成和重新分布；但中高强度的火烧显著降低结皮盖度，增加地表侵蚀的风险[54-55]。

生物土壤结皮广泛分布于各类型的荒漠生态系统，以及高山冻原和较湿润地区植被演替的早期阶段[56]，它的出现和发展特征可以用作评价草地生态环境健康状况的指标[57](表2)。总之，气候、海拔、土壤、维管植物群落、家畜和野生动物、人类管理以及草地生态系统的健康状况等共同影响着生物土壤结皮的分布。

3草地生物土壤结皮的生态功能

3.1生物土壤结皮对土壤养分的影响

高等植物是土壤有机质的重要来源，但植物株丛间隙的裸地上有机质匮乏。生物土壤结皮在地表繁殖，蓝藻、地衣、绿藻和苔类通过光合作用固定碳，提高植物间隙的土壤肥力。生物土壤结皮主要影响0～5 cm土壤有机质，可为浅根系植物种子的萌发和生长提供有机肥，促进植物的繁衍与更新[62]。冻原高山草地和冷荒漠草地中以苔藓、地衣为主的结皮能固定大量的泥炭，成为陆地生态系统的重要碳汇[63]。湿度和土壤呼吸等因素限制结皮，固定有机碳，生物结皮减少土壤CO2排放的作用与结皮厚度正相关[64]。

图1　生物土壤结皮的演替Fig.1　The succession of biological soil crust

注：①降尘填充沙粒间隙，丝状藻类定殖；②地表固定，外界干扰少；③基质稳定，水分充足；④人工接种；充足的光照、水分，微地形条件适宜；土壤表面及基质稳定；⑤火烧，高强度的放牧，高密度的旅游，频繁的交通；⑥长期机械干扰、家畜和人类活动；⑦土壤结构遭到破坏；生态环境持续性恶化，水土流失严重，草地退化加剧。

Note： ①The gap among sands full with dustfull, and algae are colonization. ②The process needs stable soil surface and less disturbance. ③Moss needs good soil matrixs and suitable moisture condition. ④Artificial inoculation;enough illumination and moisture and suitable microtopography condition; stable soil surface and matrixs. ⑤Burn,high grazing intensity, excessive tourism, and traffic disturbance frequently. ⑥Long-term mechanical disturbance and activities of livestocks and human. ⑦The soil structure were destroyed; entironment getting worse, soil erosion severly and degenerate seriously.

表2　生物土壤结皮与草地生态系统健康状况Table 2　The relationship between biological soil crusts and grassland ecosystem healthy condition

荒漠中的氮主要来自于大气沉降和生物固氮，其中土壤结皮中的蓝细菌可以固定大气中的氮，提供荒漠植物和土壤生物重要营养源[65]。北极地区，与苔藓结皮共生的藻青菌所固定的氮占冻原高山草地氮年固定总量的80%[45]。美国犹他州胶衣属地衣的氮输入量为13 kg·(hm2·a)-1，相当于无结皮土壤表层氮输入量[1.4 kg·(hm2·a)-1]的10倍[66]。苔藓结皮下土壤氮素转化速率及其对温度的敏感性均高于无结皮土壤，从而提高土壤的供氮能力，促进氮素转化与循环，加快草地土壤的修复[67]。

结皮形成过程中，藻类首先在植物根部出现，然后具有固氮功能的地衣开始定殖，改善了土壤的结构和持水力，为苔藓植物的生长创造了条件[68]。苔藓和地衣植物富集又促进表土的腐殖质累积，增加钾、钙、镁、磷等元素，从而提高草地生产力。

图2　生物土壤结皮的主要生态功能Fig.2　The main ecological function of biological soil crusts

注：①促进植物生长，捕获种子；②降低风速，为结皮发育提供稳定的阴蔽环境；③稳定地表，累积营养，参与水循环；④结皮生长的载体,影响其演替过程；⑤增加土壤温度、湿度,加快微生物活动；⑥结皮形成和生长的参与者；⑦为节肢动物提供食物，为昆虫提供适宜的生境；⑧适度放牧促进结皮发育。

Note： ①Promote plants growth and capture their seeds. ②Reduce wind speed, and provide stable environment for crusts. ③Fix soil surface, accumulate nutriention and attend the water cycle. ④Carrier of crusts growth. and effect it’s evolution process. ⑤Elevated soil moisture and temperature to quicken it’s activities. ⑥Participant of crusts formation. and development. ⑦Provide foods for arthropods, and suitable habitat for insects. ⑧Moderate grazing would beneficial to crusts’ growth.

3.2生物土壤结皮与微生物

微生物既是土壤结皮形成的参与者，反过来又受到结皮发育程度的影响[69]。通过调节土壤的温度和湿度，生物土壤结皮显著地增加了细菌、放线菌和真菌等的分布，它的发育也为微生物的生长繁殖创造了良好的条件，研究表明，生物土壤结皮类型与土壤微生物生物量密切相关[70-71],其微生物活性随着结皮发育而持续增加[72]；苔藓结皮下土壤微生物量碳氮显著高于其它类型结皮[73]。

3.3生物土壤结皮与植物的相互作用

由于研究区域、植物种类、结皮组成、所受干扰程度和土壤基本情况的复杂性，生物结皮和种子植物之间的关系尚无定论。一些研究认为，生物结皮累积了大量植物生长所必需的元素，促进了植物吸收营养和生长，而植被能降低风速、形成阴敝而稳定的环境，从而加快结皮的发育[74]；但也有研究表明，苔藓植物迅速吸收养分，与维管植物竞争资源，植被与苔藓结皮的盖度呈负相关[75]；此外有观点认为两者占据着不同的生态位，没有明显的互惠或竞争关系[76]。

除了与植株的直接关系，生物结皮的粗糙度也直接影响到土壤对种子的捕获能力[77]。荒漠土壤种子库在苔藓结皮上的储量显著高于表面光滑藻类结皮[78]，而种子的萌发与结皮层的含水量存在正相关关系[79]。

3.4生物土壤结皮在水文过程中的作用

草地生物结皮参与的水文过程主要包括降水入渗、凝结水捕获以及蒸发。起伏型结皮可以增加入渗和土壤的含水量，而光滑型结皮容易造成地表径流[80]，去除生物结皮明显提高水分的入渗率[81]。生物土壤结皮可以对水分再分配，增加土壤条件的多样性[82]。

凝结水是荒漠生态系统持续而稳定的水源，生物土壤结皮捕获凝结水能够促进有效水分的浅层化和生物量积累，促进结皮固氮、光合作用和生长，结皮叶绿素含量与其凝结水捕获能力正相关[83]。藻类结皮对土壤水分蒸发的影响与土壤含水量相关；土壤含水量较高时，藻类结皮下土壤的蒸发明显高于无结皮土壤；土壤变干时，结皮有效减小蒸发量，将水分保持在土壤中[84]。

3.5其它

生物土壤结皮对于草地生态系统环境的稳定有重要作用。生物土壤结皮显著降低风和水等对土壤的侵蚀，结皮稳定地表的能力随着其发育而增强[85-86]。颜色较深的苔藓和地衣结皮显著降低地表反射率，吸收更多能量，提高土壤温度，加速微生物活动和种子萌发[87]。生物土壤结皮可以维护草地生态系统的土壤食物网，其发育过程中累积的养分和生物量直接被食草动物、原生动物(变形虫、纤毛虫和鞭毛虫等)、线虫以及节肢动物(螨等)等利用，调控土壤养分分配和分解[88]。

4展望

作为草地生态系统的结构和功能组分，生物土壤结皮能够改良土壤，提高生态系统抵御风水侵蚀的能力，为维管植物的定居和繁育提供基础条件。20世纪后期以来，国内开展了多种草地生态系统生物结皮的研究，揭示了结皮在生态系统的作用和独特的生物多样性，对于认识景观的功能、结构和反馈机制具有重要作用。以往的研究重点集中在结皮功能和作用的认知上，对全球变化背景下生物土壤结皮的演变，及其对生态系统管理的长期反馈等研究较少，而这些知识是判别草地退化发生和发展及其机理的基础。人类活动对生物土壤结皮的破坏短期内难以通过自然恢复，适度利用阈值和人工辅助修复土壤结皮的技术对于退化草地治理具有实践意义。生物土壤结皮在区域草地生态系统能量和物质平衡中有重要作用，利用遥感监测，建立生物土壤结皮的生态系统管理体系，预测结皮在区域尺度上的时空变化，也亟待研究。

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(责任编辑王芳)

DOI:10.11829/j.issn.1001-0629.2015-0414

*收稿日期：2015-07-23接受日期：2015-10-09

基金项目：国家自然科学基金(31172249)；长江学者和创新团队发展计划(IRT13019)；国家科技支撑计划课题(2011BAD17B02-03，2012BAD13B05)

通信作者：侯扶江(1971-)，男，河南扶沟人，教授，博导，博士，主要从事草地-家畜互作研究。 E-mail:cyhoufj@lzu.edu.cn

中图分类号：S812.2

文献标识码：A

文章编号：1001-0629(2016)7-1243-10*

Corresponding author:Hou Fu-jiangE-mail:cyhoufj@lzu.edu.cn

A review on biological soil crusts of grassland

Ma Jie, Chen Xian-jiang, Hou Fu-jiang

(Key Laboratory of Grassland Farming Systems, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China)

Abstract:Biological soil crusts are a complex covering integrities developing by combining cryptigams with bacteria,fungi and soil particles, and are widely distributed in each grassland type in the world, and play an active role in improving the ecological environment and prevention of grassland degradation. In recently years, many studies throughout the world have been conducted in this field, and these studies focus on the cognition of its function and effect. However, how biological soil crusts develop under global change and how they maintain the stability of the ecosystem are still not well documented. This paper reviewed the research achievements in this filed, and discussed the current shortage and future directions of the research, and these would encourage the biological soil crusts to further advance and helpful understand the soil evolution in grassland ecosystem.

Key words：biological soil crusts; composition diversity; distribution; ecological functions; prospect

马洁，陈先江，侯扶江.草地生物土壤结皮.草业科学,2016,33(7)：1243-1252.

Ma J,Chen X J,Hou F J.A review on biological soil crusts of grassland.Pratacultural Science，2016,33(7)：1243-1252.

前植物生产层

第一作者：马洁(1992-)，女，甘肃定西人，在读硕士生，主要从事生物土壤结皮研究。E-mail:majie14@lzu.edu.cn