灵长类动物对植物种子的传播作用
陈远1, 王征2, 向左甫1,*
1 .中南林业科技大学生命科学与技术学院, 长沙 410004
2 .南京林业大学生物与环境学院, 南京 210037
* 通讯作者 Author for correspondence. E-mail: xiangzf@csuft.edu.cn
摘要

种子传播对植物种群空间分布和群落生物多样性维系有着深远的影响。森林灵长类动物可有效地传播植物种子, 其对果实的选择不仅受其自身形态、生理和行为特征的影响, 也与果实的形态特征和同域分布的其他动物类群的取食竞争密切相关。灵长类动物传播种子的模式可分为消化道传播、携带传播和颊囊传播, 其中消化道传播距离远、种子萌发或幼苗建成率高, 是最为有效的传播模式。灵长类动物对种子的传播作用还能促进退化生境的恢复。建议今后研究中应考虑灵长类动物的多途径种子传播和多种因素对种子扩散与萌发的综合影响, 同时要更加客观地评估灵长类动物缺失对森林植被更新的影响。

关键词: 灵长类动物; 食果过程; 种子传播; 植被更新; 生物多样性保护
Seed dispersal by primates
Yuan Chen1, Zheng Wang2, Zuofu Xiang1,*
1 College of Life Science and Technology, Central South University of Forestry and Technology, Changsha 410004
2 College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037
Abstract

Seed dispersal facilitates the recruitment of plants, which has profound influences upon the spatial distribution of forest plants and the maintenance of biodiversity. Recently, the role of primates in the process of seed dispersal has been increasingly studied. Primates play an important and special role in plant recruitment and vegetation regeneration in the form of feeding on fruits and dispersing seeds. The selection of different fruits is not only closely related to the quality of fruits and the feeding competition of sympatric animals, but also varies greatly with morphological, physiological, and behavioral features of different primates. According to the processes of fruit treatment, the patterns of seed dispersal by primates can be classified as endozoochory, epizoochory, and synzoochory. These patterns have different effects on the distance of seed dispersal, seed germination, and the establishment of seedlings. The most effective pattern is endozoochory, characterized by long-distance dispersal and high rates of seed germination and seedling establishment. Seed dispersal by many primate species helps to restore degraded habitats. Studies on the ecological processes of seed dispersal by primates and determined factors would be conducive to determine the role of primates in the forest ecological system, the contribution of primates to vegetation regeneration, and to provide theoretical evidence for forest ecosystem management and biodiversity conservation.

Key wordS: primates; frugivory; seed dispersal; vegetation regeneration; biodiversity conservation

在热带雨林中, 50%以上的植物果实被食果动物(以哺乳类和鸟类为主)取食(Howe & Smallwood, 1982; Levey et al, 2002), 并且60-94%的木本植物借助食果动物来实现种子的传播(Arroyo-Rodrí guez et al, 2015)。啮齿类、翼手类和灵长类是传播种子的主要的哺乳动物类群(鲁长虎, 2001), 关于前两类动物的种子传播作用研究历史较长, 而直到最近20年人们才认识到灵长类动物对植物种子传播的重要作用(Arroyo-Rodrí guez et al, 2015)。栖息于森林中的灵长类虽然食性广泛多样, 但有25-40%的种类取食植物果实, 排出或吐出大量具有萌发能力的种子(Lambert, 1999), 对森林植被的更新和生物多样性的维系起着至关重要的作用(Cain et al, 2000; Wang & Smith, 2002)。迄今为止, 很多学者以狐猴科(Dew & Wright, 1998)、卷尾猴科(Wehncke & Dominguez, 2007)、僧面猴科(Barnett et al, 2012)、蜘蛛猴科(Bicca-Marques, 2003)、狨科(Cardoso et al, 2011)、猴科(Albert et al, 2013)、长臂猿科(范朋飞等, 2008)和猩猩科(Petre et al, 2015)等灵长类动物为研究对象, 对它们的食果过程、传播种子数量、传播距离和种子萌发率等方面进行了比较详细的研究。

灵长类动物传播种子的过程较为复杂, 涉及到它们的食性、种子传播模式、传播距离、对种子萌发和幼苗建成的影响等多个层面(Schupp et al, 2010)。作为森林中典型的大型食果动物, 了解灵长类动物种子传播的生态过程, 不仅有助于探讨森林生态系统中动植物间的相互关系及其生态意义, 还可进一步明确灵长类动物对森林植被更新的贡献。

1 影响灵长类动物取食和传播果实的因素

灵长类动物的食性范围广泛, 不同种类取食的植物种类和数量也存在较大差异。而它们多样的取食行为和活动模式形成了较复杂的果实处理过程。一般来说, 影响灵长类取食和传播果实或者种子的因素主要有以下3点:

(1) 灵长类动物的个体特征, 如形态特征(口腔和肠道特点)、生理特征(食物消化时间)和行为习惯等因素, 均影响它们取食和传播植物的果实和种子。许多灵长类动物有着较长的消化道, 食物滞留时间(gut retention time)较长(Maisels, 1993), 往往能取食大量的种子(Rudran, 1978), 但其口腔大小、牙齿形态以及肠道形态结构都会影响它们吞咽的种子大小与种类。如, 南美洲的白面僧面猴(Pithecia pithecia)和红背僧面猴属(Chiropotes)动物因具有高度特化的牙齿, 能够取食具有硬质外壳的大型果实(Norconk et al, 2011)。动物的取食行为, 如取食果肉后是将种子吞下还是丢弃, 也会影响果实(种子)的传播(Lambert, 1998)。例如, 在厄瓜多尔亚松国家公园, 白额蜘蛛猴(Ateles belzebuth)至少取食152种植物的果实, 它们将绝大多数种子(98%)整体吞下, 其中毁坏的种子仅占极少数(Link & Fiore, 2006); 在中国云南的无量山, 黑长臂猿(Nomascus concolor)取食31种植物果实, 并为27种肉质果植物传播种子(范朋飞等, 2008)。

(2) 植物果实的丰富度或分布模式、果实和种子的硬度、大小、颜色和形态以及所具有的营养成分均能影响灵长类动物对果实的选择(Leighton, 1993; Russo & Chapman, 2011; 阮海河等, 2013)。栖息地果实数量多且成熟期持续时间长, 灵长类动物就会多次在该树采食, 对植物种子的搬运频次和数量也会增多(Agetsuma & Noma, 1995; Garber & Paciulli, 1997)。Sengupta和Radhakrishna (2015)发现, 猕猴(Macaca mulatta)更喜欢取食具有壳状外皮、多汁而柔软的果肉, 以及具有中大型种子和坚硬种皮的大型果实; 阮海河等(2013)也发现, 在越南的广平风芽-格邦国家自然公园, 河静黑叶猴(Trachypithecus francoisi hatinhensis)对处理难度较小的浆果和核果有着明显的偏好, 并且更多地选择黄色、红色和绿色的果实。

(3) 灵长类动物的觅食对策也受到同域生活的其他动物类群的竞争影响。如, McConkey等(2002)在印度尼西亚的加里曼丹岛发现, 灰长臂猿(Hylobates muelleri)和黑掌长臂猿(H. agilis)的果实选择受到了其他灵长类动物(猩猩和猕猴)的竞争影响。一般而言, 植物果实被森林中所有食果动物共同取食, 食性广泛的动物相对于食性较窄的动物更容易获取果实和传播种子(Sengupta & Radhakrishna, 2015)。

2 灵长类动物的种子传播作用
2.1 种子传播模式

灵长类动物对种子的传播模式可分为3种: 消化道传播(endozoochory)、携带传播(epizoochory)和颊囊传播(synzoochory) (Kaplin & Moermond, 1998; Albert et al, 2013)。

(1) 消化道传播模式, 即吞咽后排出种子。这是灵长类动物最主要的传播模式(Russo & Chapman, 2011)。如, 在非洲刚果的萨隆加国家公园, 倭黑猩猩(Pan paniscus)所传播的植物种子中, 93%以上是经消化道传播(Beaune et al, 2013); 在南美洲新热带区, 消化道传播亦是最为常见的灵长类动物的种子传播模式(Estrada & Coates-Estrada, 1984; Chapman, 1989; Andresen, 1999), 该模式无论从种子传播的距离或是对种子的萌发都起着积极作用(Lambert, 2002; Russo & Chapman, 2011)。

(2) 携带传播模式, 即取食果肉后丢弃种子。这种模式在灵长类动物种子传播中不太常见。一般的途径是灵长类动物取食果肉后直接丢弃或吐出种子, 有些甚至是将未吃完的果实整个丢弃。Koné 等(2008)研究发现, 非洲西部国家公园的几种猴科灵长类动物能将果实带离母树一段距离, 它们常在打开果实时丢弃种子或把肉质的浆果取食后吐出种子。

(3) 颊囊传播模式, 即颊囊处理后吐出种子。仅见于具有颊囊的猕猴属(Macaca)和长尾猴属(Cercopithecus)灵长类动物(Albert et al, 2013; Linden et al, 2015)。它们在取食时先将果实塞满颊囊并暂时储存, 在母树以外的地点处理完果实后吐出种子, 进而起到传播种子的作用(Corlett & Lucas, 1990), 部分吞下的种子则可认为是经消化道传播。猕猴属动物通过使用颊囊, 能传播体积较大且数量多的种子, 而它们较大的活动范围则促进了种子的长距离传播(Albert et al, 2014)。

2.2 种子传播距离

与其他动物类群相比, 灵长类动物活动于森林的各个林层(Albert et al, 2013), 因此使得传播的种子在空间分布上更为广泛。不同的传播模式对种子传播的距离差异很大: 携带传播模式传播的距离通常仅有几米, 造成种子大量聚集在母树周围, 资源竞争等因素使种子死亡率大幅度上升(Janzen, 1970; Connell, 1971)。消化道传播模式却能将种子带到离母树数百米甚至数千米的适宜生境而提高了种子的存活率(Russo & Chapman, 2011)。颊囊传播模式中, 猕猴属动物虽然有特殊颊囊进行种子传播, 但其粪便内的种子平均传播距离(116.5 m)远长于口腔吐出种子的距离(19.2 m), 并且猕猴属动物吐出的种子有39%是在取食树种的树冠下发现的, 而粪便中传播的种子通常都远离母树树冠(Sengupta et al, 2014)。

种子的传播距离还受其他一些因素影响。如, 在消化道传播模式中, 灵长类动物的日间移动模式和消化道滞留时间均会影响种子的传播距离。许多灵长类动物多年栖息在同一地点(如休息场所和夜宿地) (Chapman, 1989; Julliot, 1997), 导致这些地点的种子排放率很高而未进行有效传播(Russo & Chapman, 2011)。一些体型较大的灵长类动物通常每天能进行长距离移动(Carbone et al, 2005), 种子传播距离也因其较长的消化道滞留时间而潜在增长(Petre et al, 2015)。如, 在巴西片断化森林中体型较大的吼猴属(Alouatta)动物具有较长的日间活动距离, 能将种子传播至距离母树497 m远的地方(Bicca-Marques, 2003); 少数大型猿类对种子的传播距离有时甚至超过1, 000 m (Tsuji et al, 2010; Beaune et al, 2013)。此外, 摄取种子的时间也会影响种子的传播距离, 例如, 安第斯绒毛猴(Lagotherix lagothricha)对上午取食种子的传播距离更远(Stevenson et al, 2014)。

种子的传播距离对其后期萌发及扩散有着重要的影响, 长距离传播有助于提高植物更新的可能性, 对于植物种群的扩张、小种群的维系、定殖和基因流动有着重要意义(Schupp et al, 2010)。一般而言, 距离母树5 m远的种子存活率明显高于母树树冠下的种子(Chapman & Chapman, 1995), 但只有被传播至距离母树超过100 m远的地方, 才认为是最为有效的种子传播方式(Cain et al, 2000; Schupp et al, 2010)。因此, 尽管灵长类动物对植物种子的传播距离因传播模式各异, 但仅消化道传播属于长距离传播, 才是维系植物动态、促进种群扩张和基因流动的关键的传播模式。

2.3 传播对种子萌发和幼苗建成的影响

灵长类动物取食果实不仅能将种子带到适宜萌发的微环境, 减少种子萌发时植物种间的竞争和被捕食者捕食的危险(Andresen, 1999), 更重要的是在传播过程中, 种子经过动物的处理而改变了其萌发特性和幼苗的建成能力(Arroyo-Rodrí guez et al, 2015)。已有研究表明灵长类动物的传播作用促进了植物种子的萌发, 对幼苗的生长有着积极作用(Stevenson et al, 2002; Righini et al, 2004; Beaune et al, 2013)。

消化道传播可以提高种子的萌发率, 缩短种子萌发所需的时间(Traveset, 1998), 主要原因是: (1)动物消化道对内果皮和种皮进行的化学或机械性摩擦产生了“ 破皮” 作用, 促进了种子的萌发(Traveset & Verdú , 2002); (2)种子外的果肉能抑制种子的萌发或促进病原体的生长(Traveset et al, 2007), 灵长类动物将它们移除起到了“ 解除抑制” 的作用; (3)灵长类动物粪便中所含的营养物质具有施肥效应(Robertson et al, 2006)。如, 在委内瑞拉古里水库的陆桥岛屿上, 红吼猴(Alouatta seniculus)粪便的密集堆积能够丰富土壤中氮、磷等营养物质, 促进幼苗的建成(Feeley, 2004)。此外, Arroyo-Rodrí guez等(2015)发现, 吼猴属灵长类的消化道对植物种子生存和萌发的另一个积极作用是控制了果实或种子中昆虫幼虫的发生。

但也有研究发现, 灵长类动物通过对果实(种子)的取食给种子的萌发带来了负作用(Estrada & Coates-Estrada, 1984; Poulsen et al, 2001; Stevenson et al, 2002)。主要原因是灵长类动物在取食过程中容易将种子的种皮一并嚼碎(Hemingway, 1996), 一些小型的种子经消化道处理后很难存活下来(Dew & Wright, 1998; Mourthé et al, 2008)。另外, 体型较大的灵长类动物粪堆中聚集着较多的种子(Chapman, 1989; Gonzá lez-Zamora et al, 2014), 这可能引起病原体感染或增加被取食(如啮齿类等)的概率(Howe & Smallwood, 1982), 使种子的存活率降低。

3 灵长类动物与森林植物的关系

灵长类动物通过取食植物果实, 将种子带离母树, 直至种子萌发和幼苗建成, 形成完整而有效的传播途径。在长期的进化过程中, 灵长类动物和食源植物间已经形成了广泛的互利或互惠关系, 它们之间的协同进化是一种动态平衡状态(Lord et al, 2002; Fleming & Kress, 2011)。研究表明, 食果动物对种子的传播在热带生态系统中是一种普遍存在的现象, 果食性猴科灵长类的食物至少包含80%的果实, 促进了75%的种子萌发(Fuzessy et al, 2016)。在木本植物中, 有50-90%的物种被食果性脊椎动物取食, 并且大部分树种的果实出现了明显利于动物传播的形态特征(Howe & Smallwood, 1982; Janson, 1983; Tabarelli & Peres, 2002)。

灵长类动物对种子的传播不仅对于森林植物的空间分布和植物多样性维系有着重要的影响, 而且在种子传播网络中所扮演的角色往往是关键性的。如, 在刚果萨隆加国家公园, 尽管在无动物传播和风力散播的作用下有种子排放, 但许多植物物种因缺少倭黑猩猩而无法在果实掉落区域实现自我更新并充分地进行种群扩张(Beaune, 2015); 同样, 在新热带区森林中蜘蛛猴科灵长类的丰度和植物幼苗的多样性表现出正相关关系(Stevenson, 2011)。

灵长类动物对森林植被的恢复起到积极作用(Russo & Chapman, 2011), 例如, 大多数非灵长类食果动物不能使用隔离或者空旷的栖息地(Albert et al, 2013), 而猕猴属动物却能够穿越各种类型的森林, 这种游走式的活动格局为退化生境的修复提供了帮助; 吼猴属动物有助于森林的次级演替, 能促进退化栖息地的恢复(Arroyo-Rodrí guez et al, 2015)。

4 灵长类动物传播种子的生态学意义

灵长类动物是热带和亚热带地区食果脊椎动物的重要组成部分, 对植物果实的取食和种子传播产生了巨大的影响(Garber & Lambert, 1998)。许多研究表明, 灵长类动物之所以成为重要的植物种子传播者, 主要是因为植物种子经动物消化道排出后仍保持着良好的萌发能力(Stevenson et al, 2002; Righini et al, 2004; Sengupta et al, 2014)。很显然, 食果性的灵长类动物通过对植物果实和种子的取食, 对种子传播产生了积极影响(Fuzessy et al, 2016), 灵长类动物对种子的传播不但影响了植物从种子到幼苗期的存活状态(Janzen, 1970; McCanny, 1985), 最终还影响植物在群落中的空间分布格局(Nathan & Muller-Landau, 2000; Wang & Smith, 2002)。更为重要的是, 灵长类动物的种子传播对于许多热带树种的定殖起着关键作用, 这对维持植物种群的多样性有着重要意义(Howe & Smallwood, 1982; Julliot, 1997; Link & Fiore, 2006)。

灵长类动物在森林生态系统中扮演着独特的生态角色。与其他传播动物类群相比, 灵长类动物体型多样、活动范围大且具有复杂的取食行为等特点(Stevenson et al, 2002; Martins, 2006; Bravo, 2009), 这些特点为种子提供的传播途径较为独特, 并且这些传播方式(如种子传播距离等)通常是植物生长环境中其他动物传播者无法替代的(Tutin et al, 1991; Otani, 2010; Bueno et al, 2013)。一般来说, 成熟的大型植物果实无法由食果鸟类、果蝠类和某些食果性树栖哺乳动物(如蜜熊Potos flavus)打开或吞下后带离母树进行传播(Hallwachs, 1986; Link & Fiore, 2006)。虽然掉落至地面的某些大型果实或种子可经贮藏性啮齿动物的分散贮食(scatter-hoarding)而传播, 但这对于种子传播的作用甚微, 只有通过灵长类动物的取食才能大幅度地改变此类种子扩散的模式(Tutin et al, 1991; Jansen et al, 2002; Otani, 2010)。如, 在哥伦比亚奎瓦国家公园, 几种果实具有外皮包被的植物种子, 仅通过安第斯绒毛猴进行传播(Stevenson et al, 2014); 较小型的传播者, 如鸟类、啮齿类和果蝠类虽能传播一些植物种子, 但因果实处理过程、种子传播数量和种子排放生境的差异等而不能产生与倭黑猩猩相似的传播效果(Beaune, 2015)。

5 研究展望

我国关于灵长类动物与植物种子传播的关系研究起步较晚, 尚有大量的工作需要开展。目前, 灵长类动物种子传播过程的研究多在于独立探究单方面的传播途径, 但种子传播的过程是多途径同时进行的, 甚至传播后期种子萌发也受多种因素影响。为进一步理解灵长类动物在森林生态系统中的地位, 以及加强生物多样性保护、森林生态系统管理, 仍需要深入开展如下相关研究:

(1) 综合考虑灵长类动物的多途径种子传播。由于灵长类动物特殊的取食行为, 传播种子时往往是几种模式同时进行, 还可能具有一定的互补性。若将多种传播模式结合起来分析, 并加以模型化, 能更充分地理解灵长类动物在森林生态系统中所扮演的角色。

(2) 充分考虑多种因素对种子扩散与萌发的影响。在灵长类动物传播种子后, 地面的种子还会受到森林中其他动物(如鸟类、啮齿类)的二次传播, 也可能受到蜣螂(Onthophagus spp.)等昆虫的捕食, 这些因素也会影响种子传播的有效性, 未来应该加强这方面的研究。

(3) 客观评估灵长类动物缺失对森林植被更新的影响。近年来, 生境破坏等因素使灵长类动物种群数量减少, 这无疑将改变动植物系统的稳定性, 进而给植物的更新带来消极影响(Stevenson, 2011)。在开展灵长类动物种子传播研究的同时, 更应该客观评估灵长类对森林植被更新的影响。

致谢: 陈浩春、张波、郭程、卢浪、魏博彦等在论文初稿形成过程中给予了有益的帮助; 两位审稿专家对论文的初稿提出了宝贵意见和建议, 在此一并致谢。

作者声明没有竞争性利益冲突.

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