家畜排泄物对牧草种子传播和萌发的作用

张静，陈先江，侯扶江

(草地农业生态系统国家重点实验室，农业部草牧业创新重点实验室，兰州大学草地农业科技学院，甘肃 兰州 730020)

家畜排泄物对牧草种子传播和萌发的作用

张静，陈先江，侯扶江

(草地农业生态系统国家重点实验室，农业部草牧业创新重点实验室，兰州大学草地农业科技学院，甘肃 兰州 730020)

放牧调控牧草的生殖格局，包括牧草有性繁殖和无性繁殖分配、种子生产、传播和萌发等，其中家畜的排泄物是重要的作用途径之一。放牧家畜的排泄物促进种子生产、远距离扩散和种子萌发，同时也会损伤种子、抑制萌发等。本文从种子生产、传播及萌发等方面阐述放牧家畜排泄物对牧草种子的作用，认为其是牧草自然更新有效途径之一。放牧家畜排泄物能够增加种子产量、采食几率、散布距离及改变萌发自身与生境条件,从而提高种子传播数量和质量，以促进牧草的有效自然更新。通过了解家畜排泄物在牧草种子传播和萌发中的作用并再此基础上探讨牧草自然更新的机制，以期为草地更新和退化草地恢复提供理论参考。

放牧；草地；有性繁殖；消化道；种子扩散；土壤

牧草的更新方式通常有无性和有性繁殖两种，Nathan和Muller将有性繁殖的时空模型归纳为植株、种子生产、短暂土壤种子库(transient soil seed bank)、持久种子库(persistent soil seed bank or permanent soil seed bank)和幼苗5个时期，种子生产、散布形式及种子域的形式(包含距离、方向的分布和贮藏种子的群集等)是核心[1]。家畜排泄物占据放牧地30%～40%的面积[2-3]，是家畜向草地返还物质的主要途径[4-5]，而且对牧草种子的扩散和萌发、实生苗生长等有直接和间接作用[6]，排泄物在草地牧草自然更新方面的重要性就不言而喻了。

根据目前国内外的研究，放牧家畜排泄物对牧草更新的作用主要包括排泄物分解利用、种子的消化道传播和萌发等几方面。在分解利用上，小尺度内排泄物能改变土壤养分[7]，继而可能影响种子形成[8]；而以粪排泄物为载体的传播方式的研究[9]成为学者们关注热点。在北美[10-11]、欧洲[12-13]、亚洲[14-15]等地区，探究了不同家畜对不同牧草种子传播和萌发的作用，主要涉及了放牧家畜有牛[16-17]、羊[18-19]、鹿[20-21]等。为此，本文重点围绕排泄物在牧草种子生产、传播及萌发过程等方面的作用进行论述，以阐明放牧家畜对天然草地牧草更新的机制，为合理利用草地及改善草地生态环境提供参考。

1 家畜排泄物对牧草种子生产的作用

放牧家畜排泄物中的营养成分转化为溶解态后经过淋溶渗漏[22]和微生物分解等方式进入土壤，改善土壤pH，提高土壤C、N、P等元素的含量和土壤肥力(表1)，从而促进植物的生长，同时改变草地养分再分配[29]，对草地生态系统的养分平衡起到一定的调节作用。N、P、K等元素都能促进牧草生殖构件的形成或增加种子的产量：N元素能增加无芒雀麦(Bromusinermis)[30]和羊草(Leymuschinensis)的生殖枝、小花数[31]、籽实和结实率[32]及燕麦(Avenasativa)的穗长及繁殖生物量[33]；P元素则具有促进牧草生长、生殖器官形成和果实发育的作用[34]及增加禾本科种子产量[35]；而K元素同样也能增加羊草籽实和结实率[32]。排泄物作为有机肥能够提高禾草生殖分配[36]及增加豆科类植物种子的产量和质量[37]。经过施加腐熟羊粪，可以有效增加青海草地早熟禾(Poapratensiscv. Qinghai)的种子产量[38]。总之，排泄物的分解是一个漫长的过程，对牧草种子生产的影响也因此在短期内不显著，但是经过处理腐熟的排泄物能有效地增加种子的产量。因此，在放牧草地上如何简单、高效的利用放牧家畜排泄物这一方面需要更加深入的研究。

表1 粪斑下土壤养分差异Table 1 Effect of dung on soil nutrient content

2 家畜排泄物对牧草种子传播的作用

2.1种子的传播与保存

家畜消化道传播(endozoochory)是家畜采食牧草种子后，种子在消化道内随家畜运动、并通过粪便排泄，远离植物母体的过程[12]。家畜消化道处理促进牧草种子萌发，粪便施肥可提高其出苗率和幼苗建植[39]。牧草种子通过家畜消化道的传播，改变放牧草地植物种子的密度，加快退化草地的生态恢复[16]。家畜消化道传播的有效性取决于种子摄入、消化道对种子的作用、种子传播距离等。

种子摄入是消化道传播的基础。排泄物主要在牧草的气味、营养成分方面影响家畜对种子的摄入而间接作用消化道传播。其作用过程包括：1)粪排泄物因其气味常导致家畜不喜欢采食粪斑处的牧草[4]而减少种子的摄入[40]；2)随着排泄物养分进入土壤，提高其附近牧草营养品质、种子产量而促进家畜采食[41-42]，增加种子摄入几率。虽然粪排泄物能短暂减少家畜对牧草种子的摄入量，但从长远来看，家畜排泄物是有助于动物对牧草种子的摄入而间接贡献于消化道传播。

家畜消化道传播的关键点是消化道对种子的作用，主要包含家畜咀嚼、胃及肠道的作用。种子的自身特性如：大小、形状、寿命和种皮特性等都是消化道传播的影响因子。在种子大小的研究上多数学者认为小种子要比大种子更容易出现在粪排泄物里并更具有活力[43-44]。对这一结论，学者们给出了两种解释机制：较主流的解释是小种子在动物消化道过程中受到的迫害小。小种子因其个体较小，容易逃避动物咀嚼迫害[45]且通过消化道的速度快[46]而减少损害。通过对200种不同植物种子的对比发现，植物种子的个体越小表示在消化过程中停留的时间就越短，从而增加了种子的存活率，使之能成功通过消化道传播[47]。另一种解释认为每一个植物在其种子大小和种子数量上都是有着协调式的产出，因此种子较小的相应产生的种子数量就较多了，这就增大了小种子出现在粪便中的几率[48]。然而，也有学者提出了不同的观点，认为大种子对于小种子而言却有着其自身的优势[49]。大种子由于其面积、质量比较小，使得大种子具有不错的抵抗消化道迫害的能力而增加消化道传播的成功率。而种子的其它特性如：种子形状的作用是影响种子通过消化道的速率，而种皮特性和种子寿命则是影响种子通过消化道后的活力(表2)。可见，相对而言种子若小、圆、且拥有较坚硬种皮则更能成功的经家畜消化道来传播。

放牧家畜消化道传播为种子的远距离传播提供了一个有效的途径[55]，它满足了远距离传播的两个前提条件：1)粪中包含有足够数量的种子。却因种子、家畜种类和放牧方式的差异而各异。在美国大草原，放牧野牛粪中的平均种子密度为每克干粪2～9粒[56]，结缕草(Zoysiajaponica)草地放牧的黄牛粪中含有的种子数量平均为每克干粪101.7粒[15]；荷兰钙质草原，每克干绵羊粪中只含有(0.8±0.14)粒种子[57]，而结缕草草地放牧中山羊粪中含有每克干粪29.13粒[15]。2)家畜能携带种子产生较大的位移。有研究表明，放牧绵羊或山羊可以携带着采食进入体内的种子行走24～36 h[58]，在时间段之内它们的行走最大距离3～17 km[59]。

家畜排泄物通过改变种子生存环境而使种子得到良好的保存。一方面粪便的覆盖可以使在下层的种子逃避鼠、鸟等捕食者的捕食，从而增加种子的存活率；另一方面粪便的包裹为种子提供一种良好的庇护场所，改善种子的保存环境而使得种子得以保存。同时家畜的粪便是一些粪食型、捕食型无脊椎动物的取食和繁殖场所，在这些无脊椎动物的捕食过程中，粪便被移动到土壤表层下，其中的种子也随之被带入土壤下层并得到很好的保存。蜣螂作为一种典型的食粪无脊椎动物，在此过程中扮演着重要的角色[60-61]。家畜排泄物作为家畜消化道传播种子的载体虽因动物和植物之间的物种差异而各异，但对于牧草来说却是一种有效的扩散形式。它能在一定程度上有效地扩大种子传播范围，增加种子传播的有效性。

表2 家畜影响种子的因素Table 2 Seed factors and influence on livestock biology

2.2土壤种子库

土壤种子库(soil seed bank)是存在于土壤上层凋落物和土壤中全部存活种子的总和。放牧能有效地改变草地土壤种子库的密度和物种组成(表3)。土壤种子库通常可以简单的分为短暂土壤种子库和持久土壤种子库。持久土壤种子库指种子在土壤中休眠期至少为一年，虽然粪在草地上保留的时间不是很长，但是其中包含的种子与持久土壤种子库中的种子有相同的活力[67]。因此有学者认为，粪中的种子对持久土壤种子库影响更明显，是植物通过种子入侵草地的重要途径[68]；同时，也促进退化草地的恢复[69-70]。北欧石灰岩地区的草地，随着牛粪的分解，粪斑下土壤的短暂种子库所占比例减少，而其持久土壤种子库占比增加[71]。不仅如此，粪排泄物还能增加了粪斑下土壤种子库的物种丰富度和某些种子的密度。在Biaowiea森林中野牛粪斑下的表层土壤种子库中的荨麻(Urticadioica)、灯芯草(Juncuseffuses)以及苔草(Carexremota)等种子密度显著增加，粟草(Miliumeffusum)、水蓼(Polygonumhydropiper)、玄参(Scrophularianodosa)等喜湿植物的种子可能从野牛粪中转移到土壤里，增加了土壤种子库的物种丰富度[72]。然目前国内外在排泄物对土壤种子库的影响方面研究较少，只是在一些动物和部分地区有研究，难以成为普适结论。

表3 放牧对土壤种子库的影响Table 3 Effect of grazing on soil seed bank

3 家畜排泄物对草地种子萌发的作用

种子的萌发受其自身及环境条件的综合影响(图1)，而家畜排泄物对种子萌发的作用因素也较多，从作用效果上可归为两类：促进或抑制萌发。排泄物能促进种子萌发的作用途径包括：1)家畜采食、消化后促进萌发。一般，种子发芽率与家畜个体大小之间呈正相关关系[73-74]。日本结缕草种子经黄牛采食后发芽率显著提高，山羊采食后发芽率的提高不显著[15]。然而，南非Thornveld草地，山羊和邦斯玛拉牛采食代儿茶(Dichrostachyscinerea)和阿拉伯金合欢(Acacianilotica)后显著促进两者种子萌发，且羊粪的萌发率高于牛粪[39]。2)直接改变种子萌发环境而促进萌发。家畜粪可以改善种子萌发所需的水分条件，破碎和水分渗透后的羊粪能促进种子发芽[57]并影响实生苗生长[75]，且在西欧，践踏后的羊粪萌发物种数是未经过践踏的2～3.6倍[76]。3)间接改变种子萌发环境而促进萌发。排泄物主要是改变了土壤中能影响种子萌发的pH和N、P等元素的含量。pH能通过改变种子内在的代谢而显著影响种子的萌发，对于碱蓬(Suaedasalsa)种子而言，较高的pH能提高其种子的萌发率[77]；N、P元素的增加可以促进碱蓬[78]、老芒麦(Elymussibiricus)和诺丹冰草(Agropyrondesertorumcv. Norda)种子的萌发[79]。

图1 影响种子萌发的因素Fig. 1 Factors affecting seed germination

排泄物主要是通过改变萌发环境条件而抑制种子萌发。如，新鲜牛粪覆盖厚度的增加会阻碍干旱土壤中细叶百脉根(Loutstenuis)种子的萌发[80]；粪便的形状也抑制种子萌发：羊粪为球形且有硬壳，阻碍粪中种子萌发，羊粪粒干燥迅速也不利于种子萌发和实生苗生长。而且粪中的有害物质[66]和N浓度过高、pH不适宜等化学指标也可能抑制种子的萌发[81]。对于羊草种子来说，其种子的发芽率随着pH的增加而降低[82]。

4 讨论与展望

4.1作用机制

以种子为繁殖体的更新方式是牧草自然更新的重要方式。种子传播影响着植物种群续存及物种多样性维系[83]；种子萌发特性影响着牧草繁殖的成功率及群落的建成与演替。放牧家畜排泄物能够通过改良土壤而促进植物有性生长、提高种子存活率等；能直接或间接地影响种子的传播及萌发，为牧草以种子为繁殖体的更新方式提供有利的条件(图2)。对放牧家畜排泄物在牧草种子传播和萌发作用的研究可以从种子质量和数量两方面加深其对牧草更新的了解[84]。种子传播数量是家畜采食牧草的频次和其每次所传播种子数量的乘积[85]。受排泄物影响，牧草营养增加、种子产量提高，家畜采食频次和采食数量增加，从而提高传播数量。种子传播质量取决于家畜消化、传播距离和种子适宜生境萌发[86]，排泄物对其影响来自以下两种机制：种子经过家畜消化道作用并随家畜运动而产生位移，导致种子存活概率和传播距离改变；经过消化道作用改变种子萌发自身条件和受排泄物影响而改变种子萌发生境条件。这几种机制直观地体现了排泄物与牧草更新关系，通过了解排泄物对种子传播和萌发作用的机制有助于理解草地植物群落更新及其演替规律。

图2 排泄物对种子传播与萌发的作用Fig. 2 Effect of feces in seed dispersal and germination

注：①增加排泄物分布；②经过在家畜消化道内随家畜运动并通过粪排泄物，达到传播的目的；③排泄物的包裹和覆盖能改变萌发环境，促进或抑制萌发；④排泄物含有丰富的养分，能促进牧草的生长与发育；⑤随着排泄物的分解，养分进入土壤，改变土壤理化性质；⑥养分充足的土壤条件，能促进牧草的生长；⑦牧草的生殖发育，影响种子的形成及质量；⑧土壤pH、营养元素能作用于种子，影响萌发率；⑨通过消化道及其它方式传播种子的过程中，种子受到外部条件作用而影响种子的萌发率。

Note: ①Increase excreta distribution; ②Through excreta excretion by livestock in the digestive tract with the livestock movement, to achieve the purpose of dispersal; ③With the excreta wrapped or coverage, it can change seed germination environment to promote or inhibit germination; ④Excreta is rich in nutrients, which can promote the growth and development of forage; ⑤With the decomposition of excreta, the nutrients into the soil and changing the physical and chemical properties of soil; ⑥The nutrient-rich soil conditions can promote the growth of forage;⑦The reproductive development of forage can affecting seed formation and quality; ⑧The soil pH and nutrient elements can act on the seeds to affecting the germination rate; ⑨In the process of dispersal seeds in the digestive tract and other ways, the seeds are affected by external conditions and affected the seed germination rate.

4.2研究展望

虽然目前现有的研究成果在排泄物对牧草种子传播和萌发方面奠定了基础，今后可以在以下几个方面加强研究：1)加强排泄物对土壤种子库的研究，关于这方面的研究较少，不能形成一种普适的结论；这也许能够在保存和恢复植物物种与群落多样性提供帮助。2)家畜排泄物对种子的传播仍是国内外研究的热点，但大多还停留在对种子传播作用的认知上，在研究尺度、作用机理和有效利用方面需加强。3)加大排泄物在种子传播中的有效性研究，有助于了解种子更新在区域性植被恢复中所产生的作用。4)以往研究都关注于改良栽培草地的牧草或对牧草生长的影响，加强尿排泄物在种子萌发方面的研究，有助于为以种子为繁殖体的更新过程提供一种新途径。

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Effectsoflivestockexcretaonherbageseeddispersalandgermination

Zhang Jing, Chen Xian-jiang, Hou Fu-jiang

(State Key Laboratory of Grassland Agro-Ecosystems, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture, China, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, Gansu, China)

Grazing regulation of forage impacts forage consumption, growth, reproduction, seed production, dispersal, and germination. Dispersal of seeds through livestock excrement was one of the important means of seeds transport. While excreta from livestock can promote long-distance dispersal and seed germination, it can also damage the seeds, and affect germination. Therefore, we studied the effects of excreta on plant reproduction, propagation and germination of herbage seed. Our results show that livestock excreta served as a natural and effective means of herbage seed dispersal and regeneration. Livestock excreta increased seed production in herbage, improved likelihood of feeding, increased dispersal distance and also expanded the forage habitat. Through improved understanding of the role of excreta in herbage seed dispersal and germination it is possible to explore new approaches that may provide a theoretical framework to minimize grassland degradation and propose solutions for restoration of grasslands.

grazing; grassland; sexual reproduction; alimentary canal; seed dispersal; soil

Hou Fu-jiang E-mail:cyhoufj@lzu.edu.cn

10.11829/j.issn.1001-0629.2016-0475

张静，陈先江，侯扶江.家畜排泄物对牧草种子传播和萌发的作用.草业科学,2017,34(10)：2070-2079.

Zhang J,Chen X J,Hou F J.Effects of livestock excreta on herbage seed dispersal and germination.Pratacultural Science，2017,34(10)：2070-2079.

S812.8;Q945.34

A

1001-0629(2017)10-2070-10

2016-09-13

2017-02-20

国家自然科学基金(31672472);教育部“创新团队发展计划”(IRT-17R50)

张静(1989-)，男，四川成都人，在读硕士生，主要从事牧场管理研究。E-mail:zhangjing2014@lzu.edu.cn

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

(责任编辑 张瑾)