生物多样性, 2021, 29(12): 1687-1699 doi: 10.17520/biods.2021141

综述

植物群落稀有种维持机制与土壤反馈的研究进展

戴冬,1,2, 邢华,1,2, 杨佳绒1,2, 刘雅静1,2, 蔡焕满3, 刘宇,,1,2,4,*

1.华东师范大学-阿尔伯塔大学生物多样性联合实验室, 华东师范大学生态与环境科学学院, 上海 200241

2.浙江天童森林生态系统国家野外科学观测研究站, 浙江宁波 315114

3.凤阳山-百山祖国家级自然保护区管理局百山祖管理处, 浙江丽水 323808

4.上海污染控制与生态安全研究院, 上海 200092

Advances in mechanisms of rare species maintenance and plant-soil feedback in plant communities

Dong Dai,1,2, Hua Xing,1,2, Jiarong Yang1,2, Yajing Liu1,2, Huanman Cai3, Yu Liu,,1,2,4,*

1 ECNU-UAlberta Joint Lab for Biodiversity Study, School of Ecology and Environmental Sciences, East China Normal University, Shanghai 200241

2 Tiantong National Station for Forest Ecosystem Research, Ningbo, Zhejiang 315114

3 Management of Baishanzu, Fengyangshan-Baishanzu National Nature Reserve, Lishui, Zhejiang 323808

4 Shanghai Institute of Pollution Control and Ecological Security, Shanghai 200092

通讯作者: *E-mail:yuliu@des.ecnu.edu.cn

编委: 米湘成

责任编辑: 黄祥忠

收稿日期: 2021-04-14   接受日期: 2021-07-20  

基金资助: 国家自然科学基金(31670531)
国家自然科学基金(32071645)

Corresponding authors: *E-mail:yuliu@des.ecnu.edu.cn

Received: 2021-04-14   Accepted: 2021-07-20  

摘要

自Janzen-Connell (J-C)假说提出后半个世纪以来, 生态学家在热带及亚热带森林对该假说开展的大量实证研究表明, 由专性天敌导致的J-C效应所引起的负密度制约是维持森林多样性和决定群落组成的重要驱动力, 该假说成功地解释了热带及亚热带森林的丰富多样性。土壤病原真菌所引起的植物-土壤负反馈是J-C效应最主要的表现形式。然而, 对于植物-土壤负反馈是否能够维持森林群落中的大量稀有种仍然存在许多争议。基于当代物种共存理论的“稀有种优势”假说认为, 只有在满足“可入侵准则” (即物种在稀有时具有种群增加的趋势)的前提下, 稀有种才能在群落中与其他物种长期共存。然而, 当前基于土壤反馈的实验结果与该理论预测相悖, 因此在稀有种的维持机制方面仍存在较大的分歧。本文通过介绍植物-土壤反馈理论, 整合了可能对稀有种维持有较大影响的因素, 包括共生菌根真菌、土壤养分以及植物细根性状等在影响土壤负反馈方面的相关研究, 并对这些因素如何影响群落中物种多度和稀有种在群落中的维持进行了探讨。最后, 我们也从其他角度探讨了一些对稀有种维持的研究。我们认为在未来对稀有种的研究中, 探讨使其长期存续的“优势”和制约其种群扩大的“限制”同等重要, 将当代物种共存理论与新技术、新方法相结合对于探究稀有种的维持机制具有重要的意义, 可为稀有种保护提供理论依据。

关键词: 同种负密度制约; 森林群落; 入侵准则; Janzen-Connell假说; 植物-土壤反馈; 稀有种; 物种多度

Abstract

Background & Aim: Since the Janzen-Connell (J-C) hypothesis was proposed half a century ago, a mounting number of studies have been conducted to test the hypothesis in tropical and subtropical forests. These studies have since greatly improved our understanding of how high biodiversity is maintained. In particular, the pathogenic fungi-induced J-C effect, a type of negative plant-soil feedback (PSF), has been well-recognized as a mechanism to maintain biodiversity and structure community composition, though the overall contribution of PSF to the persistence of a large number of rare species in nature remains controversial. As predicted by the modern species coexistence theory, the “invasion criterion” should be met for rare species to co-exist with other species such that one species will increase in abundance when rare. However, previous studies show results contrary to the prediction of such theory and have thus sparked debates on the mechanism underlying rare species maintenance.
Progresses: In this work, we review PSF and the potential factors associated with PSF, including mycorrhizal fungi, soil nutrient content, and fine root functional traits. We discuss their contributions in maintaining rare species and determining species abundance via PSF. In addition to PSF, some other perspectives about rare species maintenance are also covered in this review.
Prospects: We propose that the advantages in maintaining the long persistence of rare species and the limitations in restricting population expansion of rare species may be of equal importance for rare species. The combination of modern species coexistence theory and new techniques and methodologies provide promising future directions to fully understand rare species and to better conserve rare species in the future.

Keywords: conspecific negative density dependence; forest community; invasion criterion; Janzen-Connell hypothesis; plant-soil feedback; rare species; species abundance

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本文引用格式

戴冬, 邢华, 杨佳绒, 刘雅静, 蔡焕满, 刘宇 (2021) 植物群落稀有种维持机制与土壤反馈的研究进展. 生物多样性, 29, 1687-1699. doi:10.17520/biods.2021141.

Dong Dai, Hua Xing, Jiarong Yang, Yajing Liu, Huanman Cai, Yu Liu (2021) Advances in mechanisms of rare species maintenance and plant-soil feedback in plant communities. Biodiversity Science, 29, 1687-1699. doi:10.17520/biods.2021141.

热带和亚热带森林因具有较高的生物多样性而受到生态学家的关注, 研究其多样性的维持机制一直是生态学的核心问题之一。这些具有高多样性的森林最典型的特征就是存在大量的稀有树种。以2015年巴拿马Barro Colorado Island (BCI) 50 ha热带森林动态监测样地的复查数据为例, 尽管稀有树种的个体总数仅占样地内229,000株个体的0.76%, 但样地内300多个树种中稀有种多达40% (图1)。此处以Hubbell和Foster (1986)基于大样地的稀有种定义为依据来计算稀有种比例, 即每公顷平均物种多度 ≤ 1株(DBH ≥ 1 cm)的个体。但在不同条件下, 稀有种的定义也并不绝对, 如Rabinowitz (1981)就从不同角度指出了植物的7种稀有形式。在全球尺度上, Enquist等(2019)的研究甚至发现, 地球上约435,000种已知的植物中多达36.5%是极度稀有种。

图1

图1   Barro Colorado Island (BCI) 50 ha热带森林动态监测样地物种频度与物种多度的关系。曲线为趋势线。每个直方图宽度表示的多度跨度为50 (如第一个直方为多度1-50;由于图幅限制, 多度显示不完全); 数据来源: BCI样地2015年复查数据。

Fig. 1   The relationship between tree species frequency and species abundance in Barro Colorado Island (BCI) 50 ha tropical forest dynamics plot. The curve is the trend line. Width of each bar represents abundance span for 50 (e.g. the fist bar for the abundance from 1 to 50; the abundance is not complete due to the limitation of the picture size).


早在20世纪60年代初, 生态学家已开始思考稀有种与常见种的共存问题(Preston, 1962), 如自然界中为何存在如此多的稀有种? 它们又是如何在自然界中持久存在的? 尽管如此, 早期对植物多样性的研究仍更多地关注森林中的常见种, 而对稀有种的关注较少。近年来, 随着植物谱系多样性和功能多样性研究的发展, 稀有种在自然群落中的作用越来越受到关注(Mi et al, 2012, 2021; Jain et al, 2014; Leitão et al, 2016)。

引起物种稀有的原因多种多样, 既可能是由植物自身的因素引起, 如自身适合度较低(Leimu et al, 2006), 也可能是来自外部的因素所导致, 如生境破坏、气候变化等(He, 2009)。整体而言稀有种都具有种群小和分布区狭窄等特征(Chapman et al, 2018), 因此它们在面临环境变化时(如人类活动引起的生境破碎化、气候变暖等)有更高的灭绝风险(Pimm et al, 1988, 1995; Smith & Knapp, 2003; Jain et al, 2014), 更易走向灭绝漩涡(extinction vortex; Caughley, 1994)。群落中大量稀有种的存在显著提高了群落的α多样性, 同时对生态系统功能也有非常重要的作用(Le Bagousse-Pinguet et al, 2021)。因此, 保护稀有种是生物多样性保护的重要内容, 探讨稀有种的维持机制对于生物多样性保护和解释物种共存具有重要的意义。

近年来快速发展的植物-土壤反馈(plant-soil feedback, PSF)理论为解释稀有物种在群落中的共存与森林树种多度差异提供了一个突破点。Janzen和Connell于20世纪70年代初期各自独立提出了天敌引起的宿主密度/距离制约效应, 即Janzen-Connell (J-C)假说, 以解释热带森林的高度多样性(Janzen, 1970; Connell, 1971)。在过去的半个世纪J-C假说得到了极大的发展: 不仅在热带森林中得到广泛验证(Augspurger & Kelly, 1984; Bell et al, 2006; Li et al, 2009; Mangan et al, 2010b; Bagchi et al, 2014), 还在亚热带森林(Liu et al, 2012; Liang et al, 2015)、温带森林(Packer & Clay, 2000; Jia et al, 2020)以及草地生态系统(Petermann et al, 2008)得到了实证支持。随着对J-C假说研究的不断深入, 植食性昆虫和动物以及植物病原菌被发现是这一效应的主要驱动力。其中, 土壤病原真菌因具有较高的宿主专性、快速增殖的能力及对植物的种子和幼苗阶段较大的杀伤力而受到广泛关注, 并被大量研究证实是导致J-C效应的主要驱动因素(Packer & Clay, 2000; Bell et al, 2006; Liu et al, 2012; Bagchi et al, 2014; Jia et al, 2020)。因此, 研究土壤病原真菌所引起的土壤负反馈强度的差异有助于理解自然群落中植物多度差异的形成机制(Klironomos, 2002; Mangan et al, 2010b; Liu et al, 2015; Liang et al, 2016)。

本文围绕当前稀有种维持机制方面的各种观点, 结合当代物种共存理论来解释稀有种优势假说, 并介绍了当前植物-土壤反馈理论及其在稀有种维持方面的研究进展和存在的争议, 以期为更深入地探讨稀有种维持机制提供新的视角。

1 稀有种维持与稀有种优势假说

1.1 经典物种共存理论与稀有种维持

森林木本植物群落可以看成是常见种、中间种(多度介于常见种和稀有种之间的物种, intermediate species)和稀有种共存的群落。经典的物种共存理论强调生态位的分化, 例如不同物种在资源、时间以及空间等方面的分化(Grinnell, 1917)。长期以来, 生态位分化这一经典理论在研究群落生物多样性维持方面一直占据主导地位, 学界也普遍认可生态位分化对物种共存的重要性。根据传统的生态位理论, 有学者认为稀有种的稀有性是由于与其他竞争者的生态位有重叠, 而稀有种竞争能力较弱所导致(Dawson et al, 2012)。但如果稀有种竞争能力较弱, 并且处于多度的弱势地位, 那么应该更容易被竞争排除, 然而事实上稀有种仍然大量存在, 而且在一些研究中发现稀有种的竞争能力并不弱于常见种(Lloyd et al, 2002; Zhang & van Kleunen, 2019)。此外, 也有一些学者认为稀有种之所以稀有, 可能是因为生态位分化使其占据着特殊生态位(Brown, 1984; Gaston et al, 1997; Yenni et al, 2017)。这一观点虽然被一些研究所验证(Ai et al, 2013; Mi et al, 2021), 但由于量化群落中大量个体的生态位宽度和性状变异的工作量巨大, 仍缺乏更为直接与广泛的证据。因此, 传统生态位理论在解释稀有种的稀有机制方面存在一定的局限性, 而当代物种共存理论的提出则为解释这一机制提供了新的思路。

1.2 当代物种共存理论与稀有种优势假说

当代物种共存理论由Chesson于2000年提出, 该理论将物种间的差异划分为两种类型, 即生态位差异(niche difference)和平均适合度差异(fitness difference), 储诚进等(2017)对这一理论进行了详细的介绍。简而言之, 生态位差异与传统的物种共存理论相近, 强调时间、空间和资源等方面的分化, 而平均适合度差异则强调物种在资源利用、对抗天敌和生长繁殖等方面的差异, 也可以理解为竞争能力的差异。物种间的平均适合度差异越大越难以共存, 因为适合度高的物种总是倾向于将适合度低的物种竞争排除出群落。因此, 群落中的物种一方面可通过提高生态位差异来避免生态位重叠, 即稳定化机制(stabilizing mechanism)来实现共存, 另一方面也可以通过降低平均适合度差异, 减少将对方排除, 即均等化机制(equalizing mechanism)来实现共存(储诚进等, 2017)。当代物种共存理论为物种共存研究提供了一个具有综合性和普适性的理论框架。

根据当代物种共存理论, 当一个物种入侵一个由竞争者建立的稳定群落时, 要经历正的种群增长, 由此导致物种在稀有时的优势(MacArthur & Levins, 1967; Chesson, 2000), 即“稀有种优势”假说(Siepielski & McPeek, 2010)。该假说是稀有种维持机制的一个重要依据。早在1984年, Connell等在研究热带森林中的树种共存时就认为稀有种只有具有某种优势时才能防止局部灭绝并维持整个群落的高度多样性, 他们将该优势称作“群落补偿趋势” (community compensatory trend, Connell et al, 1984)。当一个物种稀有时, 其种群的平均适合度增加, 使得种群多度增长, 种群得以恢复; 当一个物种常见时, 其平均适合度降低, 从而阻止种群规模的进一步增加, 使得稀有种获益, 这一过程也是稳定化机制的体现(Chesson, 2000; 储诚进等, 2017)。这种物种在稀有时种群多度增加的趋势也被生态学家称作“可入侵准则(invasion criterion)”, 该准则同时也是衡量几个物种是否处于共存状态的重要标准: 如果群落中的所有种都满足当其数量稀有时种群可增长的条件, 才能说它们是处于共存的状态(MacArthur, 1972; Chesson, 2000; Adler et al, 2007)。Grainger等(2019)甚至认为这一准则是生态学研究中的“通用货币”。尽管得到广泛的理论支持, 但“稀有种优势”假说在自然环境下难以验证, 因此存在一定的争议。

2 土壤反馈与稀有种维持

2.1 从J-C假说到土壤反馈

在Janzen (1970)和Connell (1971)提出Janzen- Connell假说来解释热带森林中的同种负密度制约(conspecific negative density dependence, CNDD)现象之后, 大量的研究从各个角度对这一假说进行了论证。J-C假说认为, 母树的种子以母树为中心扩散, 离母树越远种子数量越少, 离母树越近幼苗遇到专性天敌的可能性越高, 幼苗的死亡率也越高, 这一机制维持了热带及亚热带森林中物种的多样性。通过实验发现, 许多生物都能够通过对植物的专性取食或寄生引起J-C效应, 如植食性昆虫(Forrister et al, 2019)、叶片病原菌(Bayandala et al, 2017)和土壤病原菌(Augspurger, 1984; Packer & Clay, 2000; Bell et al, 2006; Petermann et al, 2008)等。祝燕等(2009)在对负密度制约的综述中有过详细介绍。应当指出的是, 专性天敌所引起的J-C效应只是引起CNDD的一部分因素。除J-C效应之外, 相似资源的竞争以及化感作用等也可以引起CNDD。虽然目前普遍认为专性天敌是CNDD的最主要来源, 但二者并不能完全等同。近年来的大量研究发现, 土壤病原菌产生的土壤负反馈引起的J-C效应是维持森林树种多样性的最主要驱动因素(Packer & Clay, 2000; Mangan et al, 2010b; Liu et al, 2012; Jia et al, 2020)。具有较高宿主专性的土壤病原菌因对植物的种子萌发、幼苗定植和生长这些对种群结构非常重要但相对较为脆弱的阶段有较强的负面影响, 从而对同种植物产生较强的负反馈作用。

然而, 虽然许多实验验证了J-C假说, 并通过换土、施用杀菌剂等实验证明了土壤病原菌在其中扮演的重要角色, 但是仍然有许多实验并没有检测出土壤负反馈。Hyatt等(2003)通过一项综合了许多控制性实验的荟萃分析发现, 距离制约引起的J-C效应在自然界并不是一个普遍的现象。与此同时, 越来越多的研究发现除了土壤病原菌之外, 以丛枝菌根(arbuscular mycorrhizal, AM)真菌、外生菌根(ectomycorrhizal, EM)真菌为主的植物共生真菌由于可以通过增强植物的养分吸收、产生物理或化学防护等方式产生土壤正反馈, 从而削弱了土壤负反馈, 这很可能是导致在之前的许多实验中无法检测到负反馈或负反馈在不同研究中差异较大的原因。外生菌根真菌可以通过形成菌根套来阻碍病原菌侵染植物细根, 从而显著降低外生菌根植物受到的土壤负反馈作用(Marx, 1972); 而丛枝菌根真菌则可以通过诱导寄主产生一系列的免疫反应来提升宿主对病原菌的抗性(Jung et al, 2012; Cameron et al, 2013)。可见, 无论是外生菌根真菌还是丛枝菌根真菌, 在与细根形成共生后都能在不同程度上降低土壤病原真菌对植物细根的侵害。通过湿筛法分离丛枝菌根真菌孢子和病原真菌后进行的接种实验进一步发现, 丛枝菌根真菌和病原菌在母树下都存在距离依赖, 并且丛枝菌根真菌可以抵消土壤病原菌引起的J-C效应(Liang et al, 2015); 而对长期幼苗数据及土壤真菌群落进行测序分析发现, 不同物种的负反馈强度差异主要受菌根类型以及各类根际土壤真菌的积累速率的调控(Chen et al, 2019)。这些证据都表明菌根真菌影响了土壤病原菌引起的负反馈, 并可以在某种程度上影响群落结构。由于绝大部分植物都会与丛枝菌根或外生菌根等真菌形成共生(Smith & Read, 1997; Brundrett, 2009), 因此在考虑由土壤病原菌引起的负反馈时不能忽视菌根真菌产生的正反馈作用。土壤病原菌引起的负反馈与菌根真菌引起的正反馈之和被称作植物-土壤净反馈能力。植物-土壤净反馈通常作为直观反映土壤反馈强度的综合体现(Liu & He, 2019)。

2.2 土壤反馈与物种多度

土壤反馈理论对于解释热带森林多样性具有重要的作用, 因此可以结合稀有种由于其密度低可逃避专化性天敌的侵害(Vermeij & Grosberg, 2018), 同时依据“可入侵准则” (Siepielski & McPeek, 2010; Grainger et al, 2019)和天敌逃逸假说(Keane & Crawley, 2002), 并基于当代物种共存理论的入侵生态学框架(于文波和黎绍鹏, 2020), 尝试从土壤反馈理论促进物种共存的角度入手, 解析稀有种的存在及维持机制。

根据“稀有种优势”假说, 在群落中稳定存在的稀有种种群应具有较强的增长趋势, 而常见种的种群增长则受到更强的阻力。如果稀有种优势来自植物-土壤反馈, 那么稀有种理论上应该受到较弱的土壤净负反馈才有利于种群增长, 而常见种应当受到较强的土壤净负反馈, 其种群的进一步增长受到抑制。简而言之, 理论上土壤净负反馈强度应与物种的多度呈正相关。例如, 在一些草地生态系统和弃耕农田中对草本植物的研究发现了稀有种或低密度种受负反馈更低的现象(van de Voorde et al, 2012; Kos et al, 2013; Maron et al, 2016)。在森林生态系统中, Liu等(2015)在亚热带森林中通过幼苗实验对光叶红豆(Ormosia glaberrima)的高密度种群和低密度种群所受到的土壤负反馈进行对比, 发现光叶红豆幼苗在高密度种群的土壤中受到的土壤负反馈更强, 而在低密度种群的土壤中受到的土壤负反馈较弱。Schroeder等(2018)在墨西哥的热带森林中通过对根际土壤真菌进行高通量测序的方法对常见种和稀有种根际真菌群落进行了分析, 发现树种多度与根际共生真菌和病原菌的多样性均呈负相关, 但与共生真菌的负相关更强, 这一结果暗示稀有种在与土壤真菌群落的相互作用方面可能存在优势。

以上研究均发现低密度种群在植物-土壤反馈方面存在优势, 其幼苗受到更低的土壤负反馈, 从而相对于高密度种群有更强的种群增长潜力。总体而言, 由于木本植物的研究难度高于草本植物, 因此在森林生态系统中这一结论还有待进一步验证。

然而, 也有研究得出了与“稀有种优势假说”相反的结论。Klironomos (2002)对比本地稀有种和入侵种所受的负反馈差异后发现, 稀有种在同种土壤中的生物量因受到来自土壤病原菌的胁迫而下降, 而入侵种则在同种土壤中通过菌根真菌而受益; 植物积累病原菌的速度可以决定该物种在多大密度时才受到负反馈, 进而影响物种在群落中的多度。这一结果首先明确否定了“可入侵准则”, 即稀有种虽然与入侵种刚入侵时类似, 都具有较低的种群密度, 但是它们的植物-土壤反馈模式却截然不同: 稀有种并不具有类似入侵种的优势。此外, Klironomos (2002)认为稀有种之所以稀有是因为其更容易积累专性病原菌, 因而在较低密度时即可表现出土壤负反馈, 而常见种可以达到更大密度是因为其专性病原菌积累缓慢, 只有达到较高密度时才会表现出负反馈。

此后, Mangan等(2010b)在BCI和Gigante的热带森林中通过控制性实验发现, 母树的相对多度与土壤负反馈呈负相关, 即相对多度越高的树种其幼苗所受的土壤负反馈越小, 而这种负反馈差异是导致常见种之所以常见, 稀有种之所以稀有的主要原因。Klironomos (2002)和Mangan等(2010b)的观点一致, 都认为多度与负反馈强度呈负相关, 稀有种受到更强的负反馈。另外, Comita等(2010)和Johnson等(2012)也通过“从格局推断过程”的方式得出了稀有种受更强的同种负密度制约效应的结论。其中, Comita等(2010)使用层级贝叶斯法对BCI样地中的幼苗数据进行分析, 通过测试物种对邻近个体的敏感性与其在群落中的相对多度的关系, 发现稀有种比常见种受到更强的同种负密度制约; Johnson等(2012)则使用美国森林清查数据验证了物种局域多度与负密度制约的关系, 同样得出了稀有种受更强负反馈的结论。然而, 这种“从格局推断过程”的思路并不是为了探讨稀有种持续存在的原因, 而是用这一现象来解释分析结果, 因此其结论是否可靠值得商榷。

稀有种由于种群小, 已经在群落尺度上处于濒临灭绝的边缘, 如果受到更强的土壤负反馈则显然更难满足“物种在稀有时具有种群恢复的趋势”这一物种共存的基本条件(Chesson, 2000, 2008; Adler et al, 2007)。一些研究者也在相关研究中得出了稀有种受更强负反馈的类似结论(MacDougall et al, 2011; Yenni et al, 2012, 2017; Kempel et al, 2018)。如Yenni等(2012, 2017)通过理论模型研究发现, 稀有种受到的强自我限制能力促进了稀有种的长期存续, 强自我限制是稀有种存续的必要条件。

此外, 还有一些研究人员尝试从其他角度去寻找稀有种优势, 或者试图解释稀有种受更强负反馈的实验结果与稀有种在生态系统中有大量存在的矛盾。Bachelot和Kobe (2013)对热带森林中植物受到的天敌伤害类型进行研究发现, 天敌造成伤害类型的多样性随物种多度的增加而增加, 而天敌造成伤害类型的多样性越高, 植物的死亡风险越高, 这表明常见种会面临更多的天敌, 从而解释了稀有种在躲避天敌方面具有优势。Parker等(2015)从谱系的角度出发, 认为大多数病原体可以感染一种以上的物种, 导致病原体溢出到密切相关的其他物种上, 这可能导致土壤负反馈强度与宿主的多度不相关。结合系统发育模型, 他们认为稀有种在系统发育方面拥有优势。Schroeder等(2020)认为, 常见种可能受到较小的负反馈并不是因为其受到较低的同种土壤负反馈, 而是受到更高的异种土壤负反馈, 这从研究方法的角度对稀有种受到的负反馈强度与理论存在差异进行了解释。

尽管存在许多争议, 一些坚持稀有种劣势观点的学者仍在通过各种方式试图从其他研究角度来证实或解释这一观点。一些学者从基因的角度研究了稀有种稀有的原因(Marden et al, 2017; Stump et al, 2020)。Marden等(2017)通过检测热带地区6个物种的幼苗根部发现, 较小的种群总体上具有较低的R基因(resistance gene, 病原抗性基因)氨基酸多样性。他们认为稀有种较小的种群降低了R基因多样性和基于病原菌识别的免疫反应, 从而导致稀有种的种群有更强的病害传播能力和更强的易感性; 如果局域尺度的稀有种种群无法从更大的外部种群获得新的R基因等位基因来增强防御, 则本地稀有种将无法维持其多度并将走向灭绝。文章的结论否定了稀有种优势。这一结论也同时否定了稀有种与常见种在生态系统中处于长期共存状态这一基本假设。

综上, 大量相关研究已经证明土壤负反馈是产生负密度制约从而维持森林多样性的重要驱动因素, 但在物种多度与负反馈强度的关系上还存在相当大的争议。尽管如此, 土壤微生物与植物的相互作用仍被认为是解释森林生态系统的多样性机制以及稀有种在群落中存续的关键因素。

3 调控土壤负反馈的其他因素

3.1 植物与菌根真菌的共生关系

研究人员很早就意识到与植物共生的菌根真菌可以通过产生正反馈来抵消部分病原菌引起的负反馈(Marx, 1972; Newsham et al, 1995; Wehner et al, 2010), 但因为菌根真菌在土壤中广泛存在, 且绝大部分植物均会与菌根真菌形成共生, 但并不像植物-病原菌那样存在较强的种水平上的专性共生, 所以认为菌根真菌只是广泛地对整个植物群落施加正反馈, 而对菌根真菌是否可以影响群落结构并不了解。随着研究的深入, 不同丛枝菌根真菌物种或群落对宿主植物具有不同作用的现象被逐渐发现, 因此其对群落水平物种多样性的维持能力的影响也逐渐为生态学家所关注(van der Heijden et al, 1998; Bever, 1999)。研究人员发现不同植物物种对丛枝菌根真菌的依赖程度不同, 对接种不同丛枝菌根真菌的响应也不同(van der Heijden et al, 1998)。通过改变丛枝菌根真菌的群落组成, 可对植物生长产生由正到负的影响(Bever, 2002; Klironomos, 2003)。此外, 有的植物会改变自身土壤中的丛枝菌根真菌群落, 使之对其后代更有益, 而同时对异种植物不利(Bever, 2002; Mangan et al, 2010a)。而在稀有种的维持方面, Bachelot等(2017)在群落尺度上发现, 丛枝菌根真菌多样性会使稀有种受益, Schroeder等(2020)通过计算机模拟的研究也支持菌根真菌的宿主亲和力会影响群落结构。这些证据表明, 丛枝菌根真菌并不是简单地对所有植物施加相同的正反馈, 而是随着植物种类、多样性的差异而存在巨大差异。相同丛枝菌根真菌对不同宿主植物也会存在亲和力的差异。从而导致其具有影响群落结构的能力, 并可能对稀有种的维持产生潜在的影响。但受限于土壤丛枝菌根真菌的鉴定、分离和培养手段, 宿主植物与丛枝菌根真菌的亲和力差异如何影响群落的物种多度差异还缺乏更具体的证据。

外生菌根真菌的宿主种类远少于丛枝菌根真菌。据统计, 外生菌根真菌仅可以和部分裸子植物, 以及壳斗科、桃金娘科、龙脑香科和木麻黄科等一些植物形成互利共生的关系。相比于丛枝菌根真菌, 外生菌根真菌不仅可以增强植物的养分吸收能力(Rousseau et al, 1994; Plassard & Dell, 2010), 还可以通过形成菌根鞘提供物理防护、释放抗菌化合物等方式帮助植物抵御根部病原微生物的侵害, 来保护植物细根(Marx, 1972), 从而显著地降低土壤病原菌引起的负反馈(Chen et al, 2019)。因为外生菌根真菌对宿主植物根系有较强的保护作用, 所以被认为可以促进单科或单种优势森林植被的形成, 对多样性的维持不利(Hart et al, 1989; Corrales et al, 2016)。近期, 邢华等(未发表数据)通过对浙江省庆元县百山祖国家公园中的极度濒危树种百山祖冷杉(Abies beshanzuensis)的根际微生物进行研究发现, 百山祖冷杉的细根与外生菌根真菌高度共生(外生菌根真菌相对丰度显著高于其他两种冷杉), 且其外生菌根真菌的物种组成不同于其他外生菌根真菌植物及其他两种非稀有冷杉。因此这种对专性菌根真菌的高度依赖可能反而限制了百山祖冷杉种群在母树以外的其他地方的增长。这一发现表明, 一些稀有种确实从土壤微生物中获得了优势, 但宿主与外生菌根真菌之间的专性共生可能又会限制种群增长, 即百山祖冷杉的外生菌根真菌在保证宿主稀有种优势的同时又限制了宿主的种群规模。以往对外生菌根真菌与植物群落多样性方面的认识多在其如何帮助植物形成单种优势并降低多样性方面(McGuire, 2007; Corrales et al, 2016), 但在群落水平上外生菌根真菌的扩散限制是否会影响外生菌根树种的分布, 并进而影响群落的多样性还有待研究。未来可以尝试通过分析其他外生菌根树种的菌根真菌与宿主的依赖性来探索外生菌根真菌专性对宿主种群分布的影响。

3.2 细根性状、养分与土壤反馈

植物细根是植物对养分、水分吸收的最末端结构(Pregitzer, 2002), 同时也与土壤中的微生物直接进行相互作用。许多研究发现植物细根性状的变异从资源进取型至资源保守型变化(Reich, 2014; Kramer-Walter et al, 2016), 这也被生态学家称作根经济谱(root economics spectrum)。植物的细根性状会随着其所在土壤养分含量的变化而快速周转(turnover)和变化(Ho et al, 2005)。例如, 植物在土壤养分低时可能会通过产生直径更小、比根长(specific root length, SRL)和比根面积(specific root area, SRA)更大的细根之类的方式来提高单位碳投入所能探索的土壤体积范围(Lynch & Ho, 2005), 而更大的比根长和比根面积也有利于养分吸收和菌根真菌的侵染(Guo et al, 2008; McCormack et al, 2015; Cortois et al, 2016)。因此, 由于土壤养分变化引起的细根性状响应变化可能也会影响细根对病原微生物或恶劣环境的抗性(Eissenstat, 1992; Newsham et al, 1995)。在西澳大利亚的研究发现, 极度缺乏磷元素的土地上往往具有极高的物种多样性, 如澳大利亚西部Kwongan的0.01 ha内有40个灌木树种, 并且各个种均存在成年个体(Laliberté et al, 2015)。这可能是因为土壤极端缺乏磷元素导致植物的细根更加倾向于在较低投入情况下探索更多的土壤, 从而导致细根更易感病, 植物更容易受到负密度制约(Laliberté et al, 2012, 2015)。在对澳大利亚西部的Jurien Bay自然形成的连续时间序列土壤进行研究后发现, 随着生态系统的发展, 土壤中的无机磷含量逐渐减少, 植物的养分吸收策略也逐渐多样化, 植物的多样性随着土壤有效磷的降低而增加(Zemunik et al, 2015), 这也进一步说明了土壤磷含量可以通过塑造细根养分获取策略进而影响植物群落多样性。

相对于在贫瘠土壤上较为一致的实验结论, 一些研究也对养分添加如何影响植物土壤反馈进行了探讨, 但是结论并不相同。一些研究发现, 养分添加会降低土壤负反馈(Gustafson & Casper, 2004; in’t Zandt et al, 2019), 主要原因是养分添加缓解了植物受到的养分胁迫, 从而可以对病原菌产生更强的耐受力; 而另一些研究则发现在养分充足的环境下, 植物会降低对菌根真菌的依赖(Balzergue et al, 2011; Kobae et al, 2016; Regus et al, 2017), 这是因为与菌根真菌的共生需要消耗植物合成的碳水化合物, 反而会成为植物的负担, 这会使其与真菌的共生关系逐渐丧失, 最后导致土壤病原菌对植物造成更大的威胁(Porter & Sachs, 2020)。基于分子水平的研究发现, 磷酸盐也是调节丛枝菌根真菌定植的信号分子。当根系磷酸盐浓度高时, 可以抑制植物的磷酸盐饥饿信号对丛枝菌根真菌定植的诱导(Branscheid et al, 2010)。可见, 土壤养分对植物-土壤反馈过程的影响非常复杂, 受到许多因素的调控。而随着氮沉降等因素对土壤养分含量的影响, 养分增加如何影响植物-土壤反馈并进一步影响群落组成也是一个值得关注的问题。

综上, 某些稀有种是否可能是因为占据特殊的生态位(例如具有特殊的养分获取策略从而占据特殊养分含量的土壤)而难以扩大种群, 但同时又不被常见种所淘汰? 或者是具有相对特殊的地下性状或养分响应机制? 这是在未来值得探讨的一个问题。

因此, 我们认为土壤养分、菌根真菌及细根性状可以共同调控土壤负反馈, 而宿主对丛枝菌根真菌的偏好性、对外生菌根真菌的专性等因素可能也会影响植物的分布, 从而对群落中的物种多度产生影响(图2)。未来对土壤负反馈的研究不仅要关注病原菌, 同时也需关注以上这些调控土壤负反馈的因素, 以及揭示它们在稀有种维持机制方面的作用。

图2

图2   植物-土壤反馈的调控因素及其对植物多度影响的框架

Fig. 2   The framework of factors formulating plant-soil feedback (PSF) and consequently determining abundance of plant species


4 其他稀有种维持的观点

除了从土壤反馈的角度, 还有一些研究尝试从其他角度, 如繁殖、食物网、生态位分化和竞争等方面来解释稀有种的产生与维持机制。

Vermeij和Grosberg (2018)认为长期的稀有性是对环境的高度适应, 他们认为稀有种对繁殖的成功率非常依赖, 因此从繁殖的角度探讨了能使稀有种长期维持低密度以及与繁殖相关的性状。结果发现, 自花授粉、与配偶选择有关的长距离信号传播能力、动物辅助繁殖以及雌雄同体是有利于稀有种维持长期稀有的性状。Bachelot等(2015)对哥斯达黎加热带森林中负密度制约效应10年的动态变化进行分析, 发现在不同年份, 稀有种还是常见种受到的负密度制约强度更强并不一致, 而且这种变化与气候有关——在湿热的年份常见种受到更强的负反馈。虽然他们并没有详细研究气候如何影响负密度制约, 但是这一发现对解释负密度制约的变异仍有一定参考价值。Xi等(2020)在青藏高原通过分析高山植物散布前的种子-捕食者网络的结构特征及其对植物种子损失率的影响发现, 不对称的拮抗网络可以使得常见种被更多的捕食者所干扰, 使得稀有种产生优势, 进而促进物种共存。Mi等(2021)从生态位分化的角度对森林群落中物种的生态位和功能生态位进行研究后发现, 稀有种倾向于占据边缘生态位而常见种则倾向于占据中心生态位, 这使得稀有种可以避免与常见种的生态位重叠而产生竞争; 而稀有种在功能性状上具有更大的变异, 暗示稀有种对不同时间和空间上的资源可能有更强的探索能力(Umaña et al, 2015)。Lloyd等(2002)对蔷薇科和禾本科的亲缘关系相近的常见种和稀有种进行竞争实验后发现, 植物的竞争能力与其是否稀有并没有直接的关系。

以上这些研究结论提示我们, 除了土壤反馈之外的其他因素也会影响到稀有种的产生与维持, 由于生态系统的高度复杂性, 植物-土壤反馈并非是解释稀有种与常见种共存机制的唯一途径。例如气候变化已被广泛认为会对生物多样性产生影响(Bellard et al, 2012), 但这种影响对维持稀有种和常见种的共存有何作用? 通过什么途径来产生作用? 这都是未来值得思考的问题。而繁殖失败对种群多度的影响, 无论是对动物(Harnik et al, 2012; Vermeij & Grosberg, 2018)还是植物( 哀建国 (2005) 百山祖冷杉濒危机制与保护对策研究. 硕士学位论文, 浙江大学, 杭州.)都非常显著, 因此对于极度稀有物种在繁殖、定植等方面的优势或劣势的研究也可以解释稀有种长期稀有的机制。除此之外, 植物的系统发育信号、功能性状、种子扩散能力以及土壤微生物等对于稀有种共存机制的解释也有待探索。与此同时, 还应尽可能地区分稀有种的类型, 例如是长期稀有种还是短期稀有种? 这对于提高研究结果的可靠性有重要作用。

5 结论

物种共存是生态学中最核心的问题之一, 而稀有种和常见种在群落中如何共存? 稀有种的种群受到何种限制? 它们又存在何种优势确保其不被排除? 这些都是解释热带、亚热带森林群落高物种多样性亟待回答的问题。其中, 促进稀有种存续的“稀有种优势”以及限制稀有种扩大种群使其保持稀有性的因素同样重要, 这种优势与限制如何维持其稀有性将是未来需要重点关注的问题。

近10余年来, 随着生态学理论的发展, 新技术与新方法不断涌现, 大量新的研究结果也带来了许多争论, 如稀有种的“理论优势”与“实证劣势”的对立, 这对稀有种研究而言既是挑战也是机遇。我们希望通过对稀有种维持机制与土壤反馈理论以及近年来的一些研究结果与争议的介绍, 提出潜在研究方向, 以期能够吸引更多研究人员关注这一问题, 为探索稀有种的维持机制带来更多的研究动力, 进而更好地理解植物群落的生物多样性维持机制。

致谢

感谢百山祖国家公园管理处给予的大力支持;感谢华东师范大学的于文波博士、陈佳乐博士以及审稿人对本文提出的大量宝贵意见。

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群落内的多物种如何共存是群落生态学的核心研究内容之一。经典的物种共存理论强调物种之间的生态位分化, 注重具体共存机制的研究。这种以具体共存机制为研究对象的方法一定程度上促进了当代物种共存理论框架的形成。在当代物种共存理论框架下, 物种间的差异被划分为两类综合性的抽象差异——生态位差异和平均适合度差异, 前者促进物种共存, 对应稳定化机制; 后者导致竞争排除, 对应均等化机制。本文在简要回顾经典物种共存理论的基础上, 介绍了当代物种共存理论的框架(包括理论的形成和定义)、基于该理论的部分实验验证工作及其在一些重要生态学问题中的应用。当代物种共存理论不仅揭示了群落内物种是如何共存的这一基本理论问题, 更重要的是在全球变化的背景下该理论对生物多样性的保护和管理具有重要的应用价值。期望本文的介绍有助于国内生态学和生物多样性工作者了解当代物种共存理论, 并将其应用于群落构建和生物多样性维持机制等方面的研究。

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The factors determining species commonness and rarity are poorly understood, particularly in highly diverse communities. Theory predicts that interactions with neighbors of the same (conspecific) and other (heterospecific) species can influence a species' relative abundance, but empirical tests are lacking. By using a hierarchical model of survival for more than 30,000 seedlings of 180 tropical tree species on Barro Colorado Island, Panama, we tested whether species' sensitivity to neighboring individuals relates to their relative abundance in the community. We found wide variation among species in the effect of conspecific, but not heterospecific, neighbors on survival, and we found a significant relationship between the strength of conspecific neighbor effects and species abundance. Specifically, rare species suffered more from the presence of conspecific neighbors than common species did, suggesting that conspecific density dependence shapes species abundances in diverse communities.

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Tropical forests are renowned for their high diversity, yet in many sites a single tree species accounts for the majority of the individuals in a stand. An explanation for these monodominant forests remains elusive, but may be linked to mycorrhizal symbioses. We tested three hypotheses by which ectomycorrhizas might facilitate the dominance of the tree, Oreomunnea mexicana, in montane tropical forest in Panama. We tested whether access to ectomycorrhizal networks improved growth and survival of seedlings, evaluated whether ectomycorrhizal fungi promote seedling growth via positive plant-soil feedback, and measured whether Oreomunnea reduced inorganic nitrogen availability. We found no evidence that Oreomunnea benefits from ectomycorrhizal networks or plant-soil feedback. However, we found three-fold higher soil nitrate and ammonium concentrations outside than inside Oreomunnea-dominated forest and a correlation between soil nitrate and Oreomunnea abundance in plots. Ectomycorrhizal effects on nitrogen cycling might therefore provide an explanation for the monodominance of ectomycorrhizal tree species worldwide. © 2016 John Wiley & Sons Ltd/CNRS.

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Plant traits associated with alien invasiveness may also distinguish rare from common native species. To test this, we grew 23 native (9 common, 14 rare) and 18 alien (8 common, 10 rare) herbaceous species in Switzerland from six plant families under nutrient-addition and competition treatments. Alien and common species achieved greater biomass than native and rare species did overall respectively. Across alien and native origins, common species increased total biomass more strongly in response to nutrient addition than rare species did and this difference was not confounded by habitat dissimilarities. There was a weak tendency for common species to survive competition better than rare species, which was also independent of origin. Overall, our study suggests that common alien and native plant species are not fundamentally different in their responses to nutrient addition and competition.© 2012 Blackwell Publishing Ltd/CNRS.

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Ecological theory predicts that the high local diversity observed in tropical forests is maintained by negative density-dependent interactions within and between closely related plant species. By using long-term data on tree growth and survival for coexisting (Fabaceae, Mimosoideae) congeners, we tested two mechanisms thought to underlie negative density dependence (NDD): competition for resources and attack by herbivores. We quantified the similarity of neighbors in terms of key ecological traits that mediate these interactions, as well as the similarity of herbivore communities. We show that phytochemical similarity and shared herbivore communities are associated with decreased growth and survival at the sapling stage, a key bottleneck in the life cycle of tropical trees. None of the traits associated with resource acquisition affect plant performance, indicating that competition between neighbors may not shape local tree diversity. These results suggest that herbivore pressure is the primary mechanism driving NDD at the sapling stage.Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.

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Background and aimsThe concept of plant-soil feedback is increasingly used to explain plant community assembly processes. Soil nutrient availability can be expected to play a critical role on these processes. However, little is known about the effects of nutrient availability on feedback direction and strength.MethodsA plant-soil feedback experiment was performed with the grasses Anthoxanthum odoratum and Festuca rubra, and the forbs Leontodon hispidus and Plantago lanceolata, on soil with either low or high nutrient availability. Additionally, we tested if plant-soil feedback of the two forbs under these conditions changed by inoculation of the soil with spores of an arbuscular mycorrhizal fungus.ResultsIncreased nutrient availability neutralised plant-soil feedback based on shoot biomass independent of its negative or positive direction, whereas the effects on root biomass were either not altered or turned negative. Mycorrhizal fungi spore addition decreased negative feedback and increased positive feedback.ConclusionsOur results suggest that negative plant-soil feedback on low nutrient soil can be overcome with nutrient addition, and that positive soil biota associations on low nutrient soil may become superfluous with nutrient increase. We hypothesize that species-specific, microbial mediated plant community assembly processes occur in low rather than high nutrient environments.

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Conspecific negative density-dependent establishment, in which local abundance negatively affects establishment of conspecific seedlings through host-specific enemies, can influence species diversity of plant communities, but the generality of this process is not well understood. We tested the strength of density dependence using the United States Forest Service's Forest Inventory and Analysis database containing 151 species from more than 200,000 forest plots spanning 4,000,000 square kilometers. We found that most species experienced conspecific negative density dependence (CNDD), but there was little effect of heterospecific density. Additionally, abundant species exhibited weaker CNDD than rarer species, and species-rich regions exhibited stronger CNDD than species-poor regions. Collectively, our results provide evidence that CNDD is a pervasive mechanism driving diversity across a gradient from boreal to subtropical forests.

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Understanding why some species are rare while others are common remains a central and fascinating question in ecology. Recently, interactions with soil organisms have been shown to affect local abundances of plant species within communities, however, it is not known whether they might also drive patterns of rarity at large scales. Further, little is known about the specificity of soil-feedback effects, and whether closely related plants share more soil pathogens than more distantly related plants. In a multi-species soil-feedback experiment (using 19 species) we tested whether regionally and locally rare species differed in their response to soil biota. Regional rarity was measured using range size or IUCN status and local rarity by typical abundance within an area. All species were grown on soils trained by a variety of regionally and locally rare and common species, which also varied in their degree of relatedness to the target. We found that, in general, regionally rare species suffered more than twice as much from soil biota than regionally common species. Soil cultured by regionally rare species also had a more negative effect on subsequent plant growth, suggesting they may have also accumulated more pathogens. Local rarity did not predict feedback strength. Further, soil trained by closely related plants had a more negative effect on growth than soil trained by distant relatives, which indicates a phylogenetic signal in the host range of soil biota. We conclude that soil biota may well contribute to plant rarity at large spatial scales, which offers a novel explanation for plant rarity and commonness. Moreover, our results show that phylogenetic relatedness between plants was a good predictor of the likelihood that two plant species interacted negatively via soil biota, which might mean that soil pathogens could prevent the coexistence of closely related plants and could drive patterns of phylogenetic overdispersion. Our results suggest that soil pathogens could restrict the ability of rare species to shift their ranges and might need to be considered by conservation biologists seeking to protect populations of rare plants.© 2018 by the Ecological Society of America.

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Hyperdiverse forests occur in the lowland tropics, whereas the most species-rich shrublands are found in regions such as south-western Australia (kwongan) and South Africa (fynbos). Despite large differences, these ecosystems share an important characteristic: their soils are strongly weathered and phosphorus (P) is a key growth-limiting nutrient. Soil-borne pathogens are increasingly being recognized as drivers of plant diversity in lowland tropical rainforests, but have received little attention in species-rich shrublands. We suggest a trade-off in which the species most proficient at acquiring P have ephemeral roots that are particularly susceptible to soil-borne pathogens. This could equalize out the differences in competitive ability among co-occurring species in these ecosystems, thus contributing to coexistence. Moreover, effective protection against soil-borne pathogens by ectomycorrhizal (ECM) fungi might explain the occurrence of monodominant stands of ECM trees and shrubs amongst otherwise species-rich communities. We identify gaps in our knowledge which need to be filled in order to evaluate a possible link between P limitation, fine root traits, soil-borne pathogens and local plant species diversity. Such a link may help to explain how numerous plant species can coexist in hyperdiverse rainforests and shrublands, and, conversely, how monodominant stands can develop in these ecosystems.© 2014 The Authors. New Phytologist © 2014 New Phytologist Trust.

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1. The enemy-induced Janzen-Connell ( JC) effect, a classic model invoking conspecific negative density dependence (CNDD) and distance dependence, is a primary biodiversity maintenance hypothesis. Yet, conflicting evidence for the JC effect leads to disagreement about its role in maintaining forest diversity. 2. We focus this review on soil-borne pathogens, which are the primary agent inducing the JC effect in many forest ecosystems. Although the test of the pathogeninduced JC effect in ecology critically rests on the seedling mortality caused by soil pathogens, what has not been explicitly explored in the early literature but has increasingly received attention is the long-recognized fact that the environment can alter virulence of pathogens and host susceptibility (thus pathogen-host interactions), as predicted by the classic disease triangle framework enlightened by pathology research in agricultural systems. 3. Here, following the disease triangle framework we review evidence on how the pathogen-induced JC effect may be contingent on context (e.g. environmental conditions, pathogen inoculum load and genetic divergence in host and pathogen populations). The reviewed evidence reveals and clarifies the conditions where pathogens may or may not cause disease to hosts, thus contributing to reconciling the inconsistent results about the pathogen-induced JC effect in the literature. The context dependence of the disease triangle predicts that the pathogen-induced JC effect would change under global change. 4. Gaining insights from evidence that the pathogen-induced JC effect is context-dependent, we suggest that future tests on the JC hypothesis be conducted under the framework of disease triangle, and we stress the necessity by controlling the effect of context factors on plant-pathogen interactions when testing for the JC effect. We conclude the review by proposing three lines of future research for testing the importance of the JC effect in maintaining global forest tree species diversity, with a particular emphasis on testing the effect of global warming on the strength of pathogen-host interactions for better predicting changes of forest biodiversity under climate change.

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In tropical forests, rarer species show increased sensitivity to species-specific soil pathogens and more negative effects of conspecific density on seedling survival (NDD). These patterns suggest a connection between ecology and immunity, perhaps because small population size disproportionately reduces genetic diversity of hyperdiverse loci such as immunity genes. In an experiment examining seedling roots from six species in one tropical tree community, we found that smaller populations have reduced amino acid diversity in pathogen resistance (R) genes but not the transcriptome in general. Normalized R gene amino acid diversity varied with local abundance and prior measures of differences in sensitivity to conspecific soil and NDD. After exposure to live soil, species with lower R gene diversity had reduced defence gene induction, more cosusceptibility of maternal cohorts to colonization by potentially pathogenic fungi, reduced root growth arrest (an R gene-mediated response) and their root-associated fungi showed lower induction of self-defence (antioxidants). Local abundance was not related to the ability to induce immune responses when pathogen recognition was bypassed by application of salicylic acid, a phytohormone that activates defence responses downstream of R gene signalling. These initial results support the hypothesis that smaller local tree populations have reduced R gene diversity and recognition-dependent immune responses, along with greater cosusceptibility to species-specific pathogens that may facilitate disease transmission and NDD. Locally rare species may be less able to increase their equilibrium abundance without genetic boosts to defence via immigration of novel R gene alleles from a larger and more diverse regional population.© 2017 John Wiley & Sons Ltd.

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Plant-soil feedbacks and interspecific competition are ubiquitous interactions that strongly influence the performance of plants. Yet few studies have examined whether the strength of these interactions corresponds with the abundance of plant species in the field, or whether feedbacks and competition interact in ways that either ameliorate or exacerbate their effects in isolation. We sampled soil from two intermountain grassland communities where we also measured the relative abundance of plant species. In greenhouse experiments, we quantified the direction and magnitude of plant-soil feedbacks for 10 target species that spanned a range of abundances in the field. In soil from both sites, plant-soil feedbacks were mostly negative, with more abundant species suffering greater negative feedbacks than rare species. In contrast, the average response to competition for each species was unrelated with its abundance in the field. We also determined how competitive response varied among our target species when plants competed in live vs. sterile soil. Interspecific competition reduced plant size, but the strength of this negative effect was unchanged by plant-soil feedbacks. Finally, when plants competed interspecifically, we asked how conspecific-trained, heterospecific-trained, and sterile soil influenced the competitive responses of our target species and how this varied depending on whether target species were abundant or rare in the field. Here, we found that both abundant and rare species were not as harmed by competition when they grew in heterospecific-trained soil compared to when they grew in conspecific-cultured soil. Abundant species were also not as harmed by competition when growing in sterile vs. conspecific-trained soil, but this was not the case for rare species. Our results suggest that abundant plants accrue species-specific soil pathogens to a greater extent than rare species. Thus, negative feedbacks may be critical for preventing abundant species from becoming even more abundant than rare species.© 2016 by the Ecological Society of America.

Marx DH (1972)

Ectomycorrhizae as biological deterrents to pathogenic root infections

Annual Review of Phytopathology, 10, 429-454.

PMID:18479192      [本文引用: 3]

McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo DL, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB, Leppälammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M (2015)

Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes

New Phytologist, 207, 505-518.

DOI:10.1111/nph.13363      PMID:25756288      [本文引用: 1]

Fine roots acquire essential soil resources and mediate biogeochemical cycling in terrestrial ecosystems. Estimates of carbon and nutrient allocation to build and maintain these structures remain uncertain because of the challenges of consistently measuring and interpreting fine-root systems. Traditionally, fine roots have been defined as all roots ≤ 2 mm in diameter, yet it is now recognized that this approach fails to capture the diversity of form and function observed among fine-root orders. Here, we demonstrate how order-based and functional classification frameworks improve our understanding of dynamic root processes in ecosystems dominated by perennial plants. In these frameworks, fine roots are either separated into individual root orders or functionally defined into a shorter-lived absorptive pool and a longer-lived transport fine-root pool. Using these frameworks, we estimate that fine-root production and turnover represent 22% of terrestrial net primary production globally - a c. 30% reduction from previous estimates assuming a single fine-root pool. Future work developing tools to rapidly differentiate functional fine-root classes, explicit incorporation of mycorrhizal fungi into fine-root studies, and wider adoption of a two-pool approach to model fine roots provide opportunities to better understand below-ground processes in the terrestrial biosphere.© 2015 The Authors. New Phytologist © 2015 New Phytologist Trust.

McGuire KL (2007)

Common ectomycorrhizal networks may maintain monodominance in a tropical rain forest

Ecology, 88, 567-574.

PMID:17503583      [本文引用: 1]

Most tropical rain forests contain diverse arrays of tree species that form arbuscular mycorrhizae. In contrast, the less common monodominant rain forests, in which one tree species comprises more than 50% of the canopy, frequently contain ectomycorrhizal (ECM) associates. In this study, I explored the potential for common ECM networks, created by aggregations of ECM trees, to enhance seedling survivorship near parent trees. I determined the benefit conferred by the common ECM network on seedling growth and survivorship of an ECM monodominant species in Guyana. Seedlings with access to an ECM network had greater growth (73% greater), leaf number (55% more), and survivorship (47% greater) than seedlings without such access, suggesting that the ECM network provides a survivorship advantage. A survey of wild seedlings showed positive distance-dependent distribution and survival with respect to conspecific adults. These experimental and survey results suggest that the negative distance-dependent mechanisms at the seedling stage thought to maintain tropical rain forest diversity are reversed for ECM seedlings, which experience positive feedbacks from the ECM network. These results may in part explain the local monodominance of an ECM tree species within the matrix of high-diversity, tropical rain forest.

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Functional Ecology, 35, 511-520.

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The American Naturalist, 180, E17-E30.

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Journal of Ecology, 83, 991-1000.

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Nature, 404, 278-281.

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Nature, 520, 542-544.

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Janzen-Connell effects are widespread and strong enough to maintain diversity in grasslands

Ecology, 89, 2399-2406.

PMID:18831160      [本文引用: 2]

Crop rotation schemes are believed to work by preventing specialist soil-borne pests from depressing the future yields of similar crops. In ecology, such negative plant-soil feedbacks may be viewed as a type of Janzen-Connell effect, which promotes species coexistence and diversity by preventing the same species from repeatedly occupying a particular site. In a controlled greenhouse experiment with 24 plant species and using soils from established field monocultures, we reveal community-wide soil-based Janzen-Connell effects between the three major functional groups of plants in temperate European grasslands. The effects are much stronger and more prevalent if plants are grown in interspecific competition. Using several soil treatments (gamma irradiation, activated carbon, fungicide, fertilizer) we show that the mechanism of the negative feedback is the buildup of soil pathogens which reduce the competitive ability of nearly all species when grown on soils they have formerly occupied. We further show that the magnitude of the change in competitive outcome is sufficient to stabilize observed fitness differences between functional groups in reasonably large communities. The generality and strength of this negative feedback suggests that Janzen-Connell effects have been underestimated as drivers of plant diversity in temperate ecosystems.

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Science, 269, 347-350.

PMID:17841251      [本文引用: 1]

Recent extinction rates are 100 to 1000 times their pre-human levels in well-known, but taxonomically diverse groups from widely different environments. If all species currently deemed "threatened" become extinct in the next century, then future extinction rates will be 10 times recent rates. Some threatened species will survive the century, but many species not now threatened will succumb. Regions rich in species found only within them (endemics) dominate the global patterns of extinction. Although new technology provides details of habitat losses, estimates of future extinctions are hampered by our limited knowledge of which areas are rich in endemics.

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Globally, phosphorus (P) limits productivity of trees in many forests and plantations especially in highly weathered, acidic or calcareous profiles. Most trees form mycorrhizal associations which are prevalent in the organic and mineral soil horizons. This review critically examines mechanisms that enhance the acquisition of P by tree roots. Mycorrhizal roots have a greater capacity to take up phosphate (Pi) from the soil solution than non-mycorrhizal root tips. Factors that contribute to this include the extent of extraradical hyphal penetration of soil and the physiology and biochemistry of the fungal/soil and fungal/plant interfaces. Ectomycorrhizal (ECM) trees are likely to benefit from association with basidiomycetes that possess several high-affinity Pi transporters that are expressed in extraradical hyphae and whose expression is enhanced by P deficiency. To understand fully the role of these putative transporters in the symbiosis, data regarding their localization, Pi transport capacities and regulation are required. Some ECM fungi are able to effect release of Pi from insoluble mineral P through excretion of low-molecular-weight organic anions such as oxalate, but the relative contribution of insoluble P dissolution in situ remains to be quantified. How the production of oxalate is regulated by nitrogen remains a key question to be answered. Lastly, phosphatase release from mycorrhizas is likely to play a significant role in the acquisition of Pi from labile organic forms of P (Po). As labile forms of Po can constitute the major fraction of the total P in some tropical and temperate soils, a greater understanding of the forms of Po available to the phosphatases is warranted.

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New Phytologist, 154, 267-270.

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Empirical studies show that plant-soil feedbacks (PSF) can generate negative density dependent (NDD) recruitment capable of maintaining plant community diversity at landscape scales. However, the observation that common plants often exhibit relatively weaker NDD than rare plants at local scales is difficult to reconcile with the maintenance of overall plant diversity. We develop a spatially explicit simulation model that tracks the community dynamics of microbial mutualists, pathogens, and their plant hosts. We find that net PSF effects vary as a function of both host abundance and key microbial traits (e.g., host affinity) in ways that are compatible with both common plants exhibiting relatively weaker local NDD, while promoting overall species diversity. The model generates a series of testable predictions linking key microbial traits and the relative abundance of host species, to the strength and scale of PSF and overall plant community diversity.

Schroeder JW, Martin JT, Angulo DF, Barbosa JM, Perea R, Arias-Del Razo I, Sebastián-González E, Dirzo R (2018)

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A major challenge in ecology is to understand how the millions of species on Earth are organized into biological communities. Mechanisms promoting coexistence are one such class of organizing processes, which allow multiple species to persist in the same trophic level of a given web of species interactions. If some mechanism promotes the coexistence of two or more species, each species must be able to increase when it is rare and the others are at their typical abundances; this invasibility criterion is fundamental evidence for species coexistence regardless of the mechanism. In an attempt to evaluate the level of empirical support for coexistence mechanisms in nature, we surveyed the literature for empirical studies of coexistence at a local scale (i.e., species found living together in one place) to determine whether these studies satisfied the invasibility criterion. In our survey, only seven of 323 studies that drew conclusions about species coexistence evaluated invasibility in some way in either observational or experimental studies. In addition, only three other studies evaluated necessary but not sufficient conditions for invasibility (i.e., negative density dependence and a trade-off in performance that influences population regulation). These results indicate that, while species coexistence is a prevalent assumption for why species are able to live together in one place, critical empirical tests of this fundamental assumption of community structure are rarely performed. These tests are central to developing a more robust understanding of the relative contributions of both deterministic and stochastic processes structuring biological communities.

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Ecology Letters, 6, 509-517.

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Rarity is a population characteristic that is usually associated with a high risk of extinction. We argue here, however, that chronically rare species (those with low population densities over many generations across their entire ranges) may have individual-level traits that make populations more resistant to extinction. The major obstacle to persistence at low density is successful fertilisation (union between egg and sperm), and chronically rare species are more likely to survive when (1) fertilisation occurs inside or close to an adult, (2) mate choice involves long-distance signals, (3) adults or their surrogate gamete dispersers are highly mobile, or (4) the two sexes are combined in a single individual. In contrast, external fertilisation and wind- or water-driven passive dispersal of gametes, or sluggish or sedentary adult life habits in the absence of gamete vectors, appear to be incompatible with sustained rarity. We suggest that the documented increase in frequency of these traits among marine genera over geological time could explain observed secular decreases in rates of background extinction. Unanswered questions remain about how common chronic rarity actually is, which traits are consistently associated with chronic rarity, and how chronically rare species are distributed among taxa, and among the world's ecosystems and regions.© 2017 John Wiley & Sons Ltd/CNRS.

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[ 祝燕, 米湘成, 马克平 (2009)

植物群落物种共存机制: 负密度制约假说

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负密度制约假说主要描述由于资源竞争、有害生物侵害(比如病原微生物、食草动物捕食)等, 同种个体之间发生的相互损害行为; 它主要强调同种个体之间的相互作用, 解释自然群落物种共存的机理; 负密度制约机制主要在小尺度上降低群落内同种个体生长率, 同时提高个体死亡率, 从而为其他物种的生存提供空间和资源, 促进物种共存。目前负密度制约假说的检验研究主要侧重密度制约、距离制约、群落补偿效应等三个方面。最近, 研究者又探讨了近缘物种之间由于对相似资源的竞争所产生的负效应, 扩展了负密度制约假说, 进而提出异群保护假说和谱系多样性制约假说。负密度制约假说引起生态学家长久的探讨和关注, 世界范围内大尺度森林动态样地的建立, 又为探索不同尺度上密度制约效应的研究提供了条件。然而目前的研究仍然存在不足, 比如负密度制约假说的检验受到其他因素的干扰、区域研究不平衡等。因此, 生态学家们仍然怀疑负密度制约效应调节群落物种共存的重要性, 但是目前的研究还没有发现否定负密度制约假说的充分证据。

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