近年来的研究表明, 与捕食、竞争等负相互作用相比, 物种间的正相互作用(facilitation)在生态系统中发挥着同等甚至更为重要的作用, 日益受到生态学家的重视(Bronstein, 1994a; Bruno et al., 2003; Agrawal et al., 2007)。常见的互利关系包括动物对植物的传粉、种子传播、根菌与植物的作用等(Bruno et al., 2003)。其中, 蚂蚁与植物的互利关系是互利关系研究中的一个热点问题(Rico-Gray & Oliveira, 2007)。在漫长的进化过程中, 许多植物都和蚂蚁建立了密切的联系, 其中既有互利作用, 如蚂蚁对植物种子的散布、传粉和对植物的保护, 也有对立的关系, 如切叶蚁对植物叶片的切割。二者间的相互作用很早就引起了人们的兴趣。但早期的研究多为描述性质, 缺乏严谨的实验证据(Rico-Gray & Oliveira, 2007)。自Janzen (1966)用实验手段首次在金合欢属(Acacia)植物和蚂蚁之间确定了互利关系之后, 涌现出了大量以蚂蚁和植物的互利关系为对象的研究(Rico-Gray & Oliveira, 2007)。这二者间的互利是自然界众多互利关系中的一种经典例子, 其中蚂蚁对植物的保护作用由于便于控制, 已成为种间关系的生态与进化研究的模式系统之一(Heil & McKey, 2003; Stadler & Dixon, 2005)。
在一些植物与蚂蚁的相互作用中, 植物通过给蚂蚁提供食物体(food body)、蚁菌穴(domatia)以及各种蜜露来吸引蚂蚁。作为回报, 蚂蚁对植物进行保护, 阻止或减少除蜜露昆虫以外的其他植食性动物对植物的取食和破坏, 二者之间形成互利关系(Rico-Gray & Oliveira, 2007), 这种关系称为保护性的蚂蚁-植物相互作用(protective ant-plant interaction) (Heil & McKey, 2003)。这种关系分布非常广泛, 在蝶形花科、大戟科、山茶科与野牡丹科植物研究中最为多见(Rosumek et al., 2009), 涉及的蚂蚁中, 以蚁亚科、切叶蚁亚科以及臭蚁亚科的蚂蚁最为常见, 包括约40个属的蚂蚁(Heil & McKey, 2003)。至少20个科的植物都具有食物体结构; 66个科的有花植物和一些蕨类植物都具有花外蜜腺, 但在裸子植物中并未发现这类结构; 超过100个属的热带被子植物具有供蚂蚁居住的蚁菌穴结构(Heil & McKey, 2003)。这种相互作用在地理上分布广泛, 在热带地区更为常见(Rico-Gray & Oliveira, 2007)。
早期的研究多偏重于对互利关系本身的探讨, 而近年来的研究发现, 这种互利关系在群落中也发挥着重要的生态效应(Wimp & Whitham, 2001; Kaplan & Eubanks, 2005; Mooney, 2007)。本文试图综述蚂蚁对其植物保护研究的相关进展及当前研究存在的问题与不足, 以期更深入地理解种间互利关系的作用与维持机制及其生态与进化意义。
1 保护性的蚂蚁-植物相互作用
1.1 植物对蚂蚁的吸引
许多植物以一些特化的结构吸引蚂蚁, 这些结构主要有食物体、蚁菌穴和花外蜜腺(extrafloral nectaries)。此外, 生活在植物上的蜜露昆虫(honeydew producing insects)也能起到相同的作用(Buckley, 1987)。其中与蚂蚁关系最为紧密的是具有食物体和蚁菌穴结构的植物, 称为喜蚁植物(myrmecophily), 而具花外蜜腺的植物与蚂蚁的关系具有偶发性, 其相互作用强度较弱(Rico-Gray & Oliveira, 2007)。在一些植物上, 食物体、蚁菌穴和花外蜜腺同时存在, 它们所能吸引的蚂蚁数量更多, 受到蚂蚁的保护更强(Heil & McKey, 2003; Rico-Gray & Oliveira, 2007)。
一些植物的枝上或叶尖会形成一种由表皮细胞构成的膨大结构, 这种结构富含养分, 可以被蚂蚁切除并运走, 被认为是植物为了吸引蚂蚁而进化出的一种特殊结构, 称为食物体。食物体中富含蛋白质、脂类以及碳水化合物, 对蚂蚁具有极强的吸引力。生长于非洲稀树草原上的金合欢属植物是这类植物的典型代表。此外, 在荨麻科、大戟科、木棉科、胡椒科等科的部分植物中也存在食物体(Rico-Gray & Oliveira, 2007)。
蚁菌穴是在植物的刺、茎或者叶柄等部位形成的中空结构, 可供蚂蚁居住, 它是植物吸引蚂蚁的一种特化结构(Rico-Gray & Oliveira, 2007)。一旦植物形成蚁菌穴, 很快就会被蚂蚁发现和占据。有的蚁后在婚飞结束后, 就会寻找一个新的未被占据的植物或蚁菌穴, 随后产卵育幼, 一个新的植物-蚂蚁互利单元就此形成。蚁菌穴中也有真菌与蚂蚁一起生活。最近的研究表明, 真菌只在与植物互利的蚂蚁所占据的蚁菌穴中存在, 在非互利蚂蚁所占据的蚁菌穴中则不存在。蚂蚁可能对这些真菌的繁殖、转移和维持有利, 但真菌在该系统中所扮演的角色目前尚不清楚(Defossez et al., 2009)。
超过300个属的植物在叶柄、枝条等处都具有一些腺体, 可以分泌富含碳水化合物的蜜露, 这也是植物吸引蚂蚁的一种方式(Gonzalez-Teuber & Heil, 2009)。生活于林冠上的其他蜜露昆虫, 如蚜虫、介壳虫、沐蝉等, 也会吸引大量的蚂蚁, 它们所分泌的蜜露是许多蚂蚁的重要食物来源(Way, 1963)。林冠上的蜜露昆虫往往被一些竞争上处于优势的蚂蚁所占据(Davidson et al., 2003), 这类蚂蚁的种群数量十分惊人(Oliver et al., 2008), 能够给植物提供较强的保护(Bluthgen et al., 2000; Mooney, 2007)。值得注意的是, 蚜虫的物种丰富度呈现温带高、热带低的特点(Dixon et al., 1987), 这暗示着北方森林中, 蚂蚁-蚜虫-植物三者之间的关系可能会更为密切。
1.2 蚂蚁对植物的保护作用
蚂蚁是大约10万种昆虫的捕食者(Thomas & Settele, 2004), 它们对整个地面以及林冠上的食物网络具有极重要的影响(Mooney, 2007; Moya- Larano & Wise, 2007)。蚂蚁对植物的保护作用很早就被人们认识并用于生产实践中(Way & Khoo, 1992), 如中国早在公元300年就开始用蚂蚁控制同翅目害虫(Buckley, 1987), 现在一些地区的农民仍然用蚂蚁控制果树上的害虫(van Mele & Cuc, 2001)。许多昆虫虽然能够突破植物自身的化学防御, 但对于蚂蚁对植物的外在生物防御却束手无策。近年来, Styrsky和Eubanks (2007)、Chamberlain和Holland (2009)以及Rosumek等(2009), 分别对32篇、81篇和76篇有关蚂蚁-蜜露昆虫-植物三者之间和蚂蚁-植物二者之间相互作用的文献进行了整合分析(meta analysis), 发现对于蚂蚁-蜜露昆虫-植物三者间的相互作用, 72%的研究认为蚂蚁对植物具显著的保护作用; 对于蚂蚁-植物二者的直接相互作用, 几乎所有的研究都支持蚂蚁对植物有显著的保护作用。这些分析结果揭示了蚂蚁对植物的保护作用具有普遍性。
蚂蚁的保护可以降低植物叶片遭取食程度, 提高植物种子的产量或质量, 降低周围植物对宿主植物的竞争等(Heil & McKey, 2003)。在一枝黄花属(Solidago)的一种植物中, 有蚂蚁保护的植物长得更高, 种子产量更多, 当虫害爆发时, 只有具蚂蚁保护的植株才可以开花结实(Messina, 1981)。非洲的豆科植物Leonardoxa africana在失去蚂蚁后, 叶片损失会增加1-12倍(Gaume et al., 1997); 野牡丹科植物Tococa spadaciflora在失去蚂蚁后叶片损失程度从27%上升至91% (Alvarez et al., 2001); 无蚂蚁时, 白桦(Betula pendula)的叶片损失程度会提高6倍, 枝条上叶片的数量也会减少(Mahdi & Whittaker, 1993)。蚕豆(Vicia faba)上如无蚂蚁存在时, 种子产量仅为有蚂蚁存在植株的1/7。Quercus dentate在有蚂蚁看护的情况下, 完好种子的比率从27.7%上升到48.8% (Ito & Higashi, 1991)。
蚂蚁不仅能对植物进行直接保护, 而且还会杀死与宿主植物进行竞争的植物(Frederickson et al., 2005), 或将其他植物接触到宿主植物的枝条咬断(Federle et al., 2002), 显著提高宿主植物的竞争优势。如在临近宿主植物Duroia hirsute的区域里, 蚂蚁Myrmelachista schumanni将其腺体所分泌的毒素注入非宿主植物的叶片之中, 24 h之后, 这些叶片就开始死亡, 5天后绝大多数叶片脱落, 造成这些植物死亡, 逐步形成由该宿主植物完全占据的区域, 形成亚马逊雨林中的所谓“恶魔花园”(devil garden)现象。这种植物与蚂蚁的共生体, 会在一个地方存在800年之久, 一个“恶魔花园”就会包含多达300株的宿主植物和数以百万计的蚂蚁个体(Frederickson et al., 2005)。有些情况下, 蚂蚁的种群数量会过于庞大, 仅宿主植物并不能满足其居住需求, 这时, 蚂蚁也会通过某种未知的机制诱使一些非宿主植物的茎病变中空, 形成膨大的结构供蚂蚁居住, 这类蚂蚁对于整个群落的生态效应仍有待于进一步研究(Edwards et al., 2009)。
植物在获得蚂蚁保护的同时, 也会付出一定的代价, 有时甚至得不偿失。一方面植物需要消耗能量来形成食物体、蚁菌穴等特化结构, 另一方面, 由于蚂蚁的看护, 植物上植食性蜜露昆虫数量急剧增多, 会对植物产生不利影响(Eubanks, 2001; Coppler et al., 2007)。一些蚂蚁还会对宿主植物的繁殖器官造成严重的破坏, 比如, 蚂蚁Allomerus cf. demerarae会破坏其宿主节果决明(Cassia nodosa)花器官的发育, 而遭到蚂蚁“阉割” (castration)的植物会长出更多的蚁菌穴供蚂蚁居住, 但其种子产量几乎为零。这种植物之所以能够在自然选择中得以保存, 是因为仍有少数植物能与另外3种蚂蚁实现真正的互利, 从而使得宿主植物没有在漫长的进化过程中被淘汰(Yu & Pierce, 1998)。虽然在与蚂蚁的相互作用中, 植物会付出一定的代价, 但总体上看, 植物仍然能够获得显著的收益。
2 蚂蚁对植物保护作用的调节机制及影响因素
2.1 植物吸引蚂蚁的调节机制
对于植物来说, 用最小的投入来获得蚂蚁最大的回报是一种最佳策略。植物通过多种机制来保证自己能够受到蚂蚁的有效保护, 同时避免欺骗者或寄生者蚂蚁的存在。
一些植物通过对资源的时空分配达到利益最大化。比如一种薯蓣Dioscorea praehensilis只有在从地面向林冠攀爬的阶段才会分泌蜜露, 因为这一时期该植物最为脆弱, 最需要蚂蚁保护(di Giusto et al., 2001)。血桐(Macaranga tanarius)在叶片遭到损伤后才会增加蜜露的分泌(Heil et al., 2001)。遭植食性昆虫取食压力较大的植物种群花外蜜腺的分泌量也较大(Rios et al., 2008), 这说明植物可以依据自己遭到破坏的程度来调节与蚂蚁的关系。此外, 有的植物还具有一些十分精巧的机制来保证蚂蚁对自己的保护。比如, 只有在有蚂蚁存在的情况下,胡椒属植物Piper cenocladum才会长出食物体, 将蚂蚁移除之后, 食物体的生长就停止, 如果再次将蚂蚁移到植物上, 食物体的生长又重新启动(Risch & Rickson, 1981), 即必须在有蚂蚁在植物上持续“巡逻”的情况下, 植物才会给蚂蚁以回报。植物对非互利蚂蚁的物理隔离也是一种重要的调节机制。在豆科的一些植物中, 虫蚁穴的顶部有一层由薄壁细胞形成的特化的“锁”式结构, 这种结构在每一种植物中都不相同, 只有形态上与之对应的特定种类的蚂蚁才能打开这把“锁”进入到虫蚁穴中(Brouat et al., 2001)。血桐属(Macaranga)植物M. myrmecophytes, 茎表皮上具有非常光滑的蜡质, 只有对其具有显著保护作用的蚂蚁才能顺利通过这层蜡质, 而其他非互利蚂蚁则无法通过(Federle et al., 1997)。与之相似, 最新的一项研究表明, 生活于圭亚那的西哥罗佩树(Cecropia obtusa)的叶片背面具有黏性, 可以牢牢地粘住与之互利的蚂蚁的足部, 因而这些蚂蚁可藏在叶片的背面对猎物发动伏击(Dejean et al., 2010)。
植物还可以通过改变蜜露中的化学成分来吸引特定的蚂蚁, 只有这些蚂蚁才能给植物提供有效的保护, 而这种蜜露对于盗猎者或寄生者蚂蚁则毫无吸引力。如在金合欢属植物与互利蚂蚁的相互作用中, 几种喜蚁植物蜜露中一种蔗糖裂解酶的活性都很高, 因而其蜜露中不含蔗糖, 而与之互利的蚂蚁Pseudomyrmex sp.的消化道内几乎不含这种酶, 所以这类蚂蚁就专性地以该植物的蜜露为食, 同时对其提供有效的保护。而那些与该植物没有互利关系的蚂蚁, 其消化道内蔗糖裂解酶的活性都很高, 它们需要摄入含蔗糖的蜜露来满足自己的需要, 所以对这种不含蔗糖的蜜露不感兴趣。这样, 植物就可以靠吸引特化的蚂蚁来保护自己(Heil et al., 2005)。
近年的研究表明, 蚂蚁在摄入蜜露之后, 对其他昆虫的攻击性会增强, 它们对植物的保护作用也随之加强(Ness et al., 2009)。在给蚂蚁提供糖溶液和蛋白质两种食物的情况下, 摄入糖溶液的蚂蚁对植食性昆虫的攻击性更强。由于蜜露中的C : N值较高, 蚂蚁在摄入蜜露之后需要摄入一定量的高N食物来平衡自己体内所需的C : N值, 所以它们会加大对体内N含量较高的昆虫的捕食。此结果揭示了植物可以通过改变蚂蚁食物的C : N值造成其食谱失衡, 从而促使蚂蚁加强对自己的保护(Ness et al., 2009)。
植物还可以通过多种机制避免蚂蚁带来的负面效应。大多数蚂蚁身体上都有一些腺体, 这些腺体的分泌物具有抗菌作用, 以维持蚂蚁体表和蚁巢的卫生(Fernandez-Marin et al., 2006), 但这些分泌物对于花粉的存活和繁育不利(Galen & Butchart, 2003)。许多植物的花中也含有大量的蜜露, 这会引起蚂蚁在植物花器官上聚集, 并对花器官进行破坏, 进而给植物带来不利的影响(Edwards & Yu, 2008)。此外, 蚂蚁还会对传粉昆虫进行干扰, 妨碍植物传粉过程的进行(Ness, 2006; Lach , 2008)。自然条件下, 植物如何避免花器官或者传粉过程遭到蚂蚁的破坏呢?Janzen (1977)提出的假说认为, 蚂蚁之所以不会破坏植物的花器官, 是因为花中可能存在一些化学成分令蚂蚁感到厌恶, 难以消化, 或者中毒; 在缺乏蚂蚁的生境中, 如在海拔2 200 m以上的高山上, 花上就没有必要存在这些物质。这一假说得到一些研究的证实(Beattie et al., 1984; Ghazoul, 2001; Raine et al., 2002; Agarwal & Rastogi, 2008; Willmer et al., 2009)。如Willmer和Stone (1997)在金合欢属植物Acacia zanzibarica中发现, 在一个新的花苞打开之前, 拜访花苞的蚂蚁较多, 可以防止昆虫对花苞的破坏。而在花苞开始打开时, 拜访花的蚂蚁却会减少, 这样传粉昆虫对花的拜访就不会受到干扰。花经过传粉, 种子开始发育之后, 蚂蚁的数量就又重新增多, 这时它们能够对种子进行保护, 使得金合欢的结实量增加。即蚂蚁对金合欢花的拜访存在着时间上的差异, 恰好能与传粉昆虫错开。迫使蚂蚁离开刚打开的花朵的因素可能是花粉本身所释放的挥发性化合物。植物的繁殖器官或部位上吸引蚂蚁的资源的减少、消失, 也是防止蚂蚁破坏的一种策略。如亚马逊地区金橡实科(Chrysobalanaceae)的喜蚁植物Hirtella myrmecophila将要结实的老枝上的蚁菌穴会脱落, 而嫩枝上则不存在这一现象。嫩枝上的嫩叶受到蚂蚁的强烈保护, 而果实却只在较老的枝条上才会出现。所以老枝上蚁菌穴的脱落可能是一种适应性机制, 可避免蚂蚁在老枝上营巢与活动, 破坏老枝的结实, 所以这是植物对蚂蚁既利用又排斥的一种精巧策略(Izzo & Vasconcelos, 2002)。
此外, 叶片的损伤或震荡, 植物汁液的释放, 都会引起蚂蚁的聚集, 植物的各种诱导效应, 如花外蜜腺分泌蜜露的量的变化, 蜜露中糖分的浓度, 氨基酸的浓度变化都会影响蚂蚁对植物的看护效果(Agrawal, 1998; Katayama & Suzuki, 2003; Palmer & Brody, 2007; Dejean et al., 2008; Grangier et al., 2008)。虽然这些植物依赖于蚂蚁的看护, 但在没有蚂蚁或蚂蚁较少的区域, 这些植物仍然可以通过加强叶片硬度、增加体表毛状体多度等自身物理防御, 在一定程度上弥补外在保护者的不足(Moraes & Vasconcelos, 2009)。需要指出的是, 虽然植物有多种策略来保证自己得到蚂蚁的保护, 但蚂蚁对植物的欺骗与寄生仍然存在, 缺乏对欺骗者和寄生者的惩罚机制可能是二者得以存在的重要原因(Edwards et al., 2010)。
2.2 影响蚂蚁保护作用的因素
影响蚂蚁对植物的保护作用的因素有很多, 具有很强的背景依赖性(context dependence)和变异性(Bronstein, 1994b, 1998; Rico-Gray & Oliveira, 2007)。总体来看, 蚂蚁的保护作用在热带强于温带, 并会随海拔的上升而降低, 单一种类蚂蚁的保护作用要强于多种蚂蚁, 与蚂蚁关系更紧密的植物(如能给蚂蚁提供食物体、蚁菌穴, 或者能够同时提供多种资源)受到的保护更强(Chamberlain & Holland, 2009; Rosumek et al., 2009)。嫩叶受到的保护强于成熟叶(Fonseca, 1994; Izzo & Vasconcelos, 2002; Edwards et al., 2007)。植物的基因型(Floate & Whitham, 1994; Wimp & Whitham, 2001; Johnson, 2008; Mooney & Agrawal, 2008)、施肥(Trager & Bruna, 2006)、光照条件(de La Fuente & Marquis, 1999)以及季节变化(Mooney & Tillberg, 2005)等多种因素都会影响到蚂蚁和植物的相互作用。不同种类的蚂蚁对植物的保护还可能存在时间上的错位, 例如在稀树草原中的一种棺木Didymopanax vinosum上存在21种蚂蚁, 这些蚂蚁对蚜虫及植物的看护存在着昼夜的交替, 这会有效地降低不同蚂蚁种类之间对资源的竞争(Del-Claro & Oliveira, 1999)。
植物遭到植食性动物的取食压力也是这种互利关系能否维持的重要因素。最近, Palmer等(2008)通过对金合欢属植物Acacia drepanolobium进行长达10年的与大型植食性动物(长颈鹿等)的隔离之后发现, 这种植物分泌的蜜露和提供给蚂蚁的蚁菌穴的数量显著减少, 对其最有利的蚂蚁所占比例显著下降, 但对其不利的蚂蚁所占比例显著上升, 且该种蚂蚁与一种甲虫相互作用, 加剧了植物受破坏的程度, 从而造成了金合欢与蚂蚁互利关系的崩溃。此研究说明, 一定程度的干扰可能也是互利关系得以维持的必要条件。
3 保护性蚂蚁-植物相互作用的进化历史与生态效应
3.1 保护性植物-蚂蚁相互作用的进化历史
当前, 对于植物的食物体、蚁菌穴的起源与进化历史的研究较少; 而对于花外蜜腺的起源以及植物与蚂蚁在系统发育上的相互关系则关注较多。
花外蜜腺的起源是当前争论较多的一个问题。一种观点认为, 花外蜜腺起源于其对蜜露昆虫的替代作用, 即植物分泌蜜露能够使蚂蚁放弃对蜜露昆虫的照顾, 从而降低植物遭到这类昆虫伤害的程度, 同时也能得到蚂蚁的保护(Pemberton, 1992)。化石证据表明, 在一种生活于距今3 500万年前现已灭绝的杨柳科杨属植物Populus crassa的叶片上就存在蜜腺。与该化石位于同一区域的昆虫化石中, 以蚂蚁最为丰富, 多达32种, 其中10种蚂蚁的后裔具有拜访花外蜜腺的行为(Pemberton, 1992)。但有反对者认为, 在该区域, 与这种植物处于同一时期的一些昆虫的后裔同样会拜访花外蜜腺, 所以并不能依此断定花外蜜腺的产生就是为了吸引蚂蚁。当前的实验结果表明, 除了蚂蚁, 许多昆虫同样是植物花外蜜腺的拜访者, 如蜘蛛、螨虫和寄生蜂等, 这些拜访者在花外蜜腺起源中所扮演的角色及其对植物的影响仍不清楚(Rico-Gray & Oliveira, 2007)。有的研究表明, 相对于植物的花外蜜腺, 蜜露昆虫所分泌的蜜露对于蚂蚁更具吸引力(Katayama & Suzuki, 2003)。一些蚂蚁即使在获得更优质食物资源的情况下仍然不会放弃对蜜露昆虫的看护(Rico-Gray & Oliveira, 2007), 所以靠花外蜜腺来减少蚂蚁对蜜露昆虫的看护这一假说, 目前仍然缺乏实验证据。
从系统发育的角度来看, 蚂蚁与植物之间的系统发育关系比较复杂。在系统发育树上, 喜蚁植物具有重复发生的特点。植物本身的进化、与之相互作用的蚂蚁的局部灭绝、不同谱系的蚂蚁对植物的占据都会影响到二者间系统发育的历史(Rico-Gray & Oliveira, 2007)。最近的研究(Heil et al., 2009)揭示, 从喜蚁植物的系统发育来看, 在漫长的进化过程中, 植物对蚂蚁具有高回报与低回报两种策略。低回报策略由高回报策略进化而来。而对于植物来说, 进化历史上有的蚂蚁为互利者, 有的蚂蚁则为盗猎者, 这两种类型的蚂蚁在进化上各自独立起源。该研究认为, 不同区域内植物的付出与收益之比的变异性是造成两种吸引蚂蚁策略能够长期共存的关键因素(Heil et al., 2009)。近年通过对蚂蚁系统发育过程的研究还发现, 与植物具有密切关系的蚂蚁, 其消化道内都具有能够分解吸收蜜露的共生细菌, 这些共生细菌在二者相互作用的长期维持与进化上发挥着重要作用, 那些与植物关系不密切的蚂蚁则不具备这些共生细菌(Russell et al., 2009)。
3.2 保护性植物-蚂蚁相互作用的生态效应
早期的研究多集中于对蚂蚁-植物相互作用机制和对双方影响的探讨, 但近来的研究揭示, 这种互利关系有着广泛的生态影响(Wimp & Whitham, 2001; Kaplan & Eubanks, 2005; Mooney, 2007)。当前研究关注的重点, 在于这种互利关系对食物链的影响以及由此所引发的连锁反应。
首先, 蚂蚁在植物上的聚集与活动对植食性昆虫具有强烈的抑制作用。Rosumek等(2009)通过对相关文献的整合分析发现, 在对蚂蚁进行隔离之后, 植物上植食性昆虫的多度增加了53.1%, 且这种抑制作用在热带地区更为显著。值得注意的是, 在现有的研究中, 仅发现几种比较特殊的蚂蚁以植物上的植食性昆虫为食(Heil & McKey, 2003)。所以与植物互利的蚂蚁对植食性昆虫的作用更多的是一种威慑而非捕食。如甲虫(Rhyparida wallacei)对蚂蚁留在叶片上的信息素非常敏感, 它们尽量避免在蚂蚁占领的植物上活动和进食(Offenberg et al., 2004)。一些毛虫会通过特殊的机制避免与蚂蚁直接接触(Rashbrook et al., 1992; Stiefel & Margolies, 1998; Oliveira & Freitas, 2004), 有的蛾类则会通过视觉观察, 避免在具有蚂蚁的叶片上产卵(Sendoya et al., 2009)。
其次, 蚂蚁对植物上的捕食者(如蜘蛛)也具有重要影响。Rosumek等(2009)研究发现, 在无蚂蚁的植物上的捕食者数量比对照多一倍。蚂蚁会对捕食者进行攻击, 一些蜘蛛与蚂蚁在拜访花外蜜腺上具有竞争关系, 但蚂蚁在数量与行为上都占有优势, 所以会引起捕食者数量的减少(Heil & McKey, 2003)。另一方面, 在没有蚂蚁保护的情况下, 蜜露昆虫更易于受到捕食者的攻击, 这也会引起捕食者数量的增加(Del-Claro & Oliveira, 2000)。并非所有的蜘蛛都会受到蚂蚁的干扰, 如最近的一项研究表明, 一种蜘蛛Bagheera kiplingi可巧妙地避开蚂蚁对金合欢的保护, 并以金合欢的食物体为食, 这也是人类首次发现的植食性蜘蛛(Meehan et al., 2009)。
总体上看, 蚂蚁的存在能大大地降低植物上其他节肢动物的物种多样性和多度(Wimp & Whitham, 2001; Kaplan & Eubanks, 2005)。也有研究表明, 如蚂蚁的数量过高, 则会影响种子传播者和传粉者对植物的拜访, 从而可能引发更多的连锁反应(Altshuler, 1999; Mooney, 2007; Davis et al., 2010)。
4 当前研究存在的问题与不足
虽然蚂蚁对植物的保护作用已成为探讨互利关系的进化与生态意义的模式系统, 对此已经做了大量的研究与探讨, 但仍对许多问题认识不足, 总结起来可以归纳为以下4个方面:
(1)对互利关系的起源与维持机制还不清楚。有研究表明, 生活在距今大约3 500万年前的现已灭绝的杨树Populus crassa就带有花外蜜腺, 但当时除了蚂蚁之外, 其他昆虫也十分繁盛, 所以并不能以此作为花外蜜腺是因蚂蚁而产生的直接证据(Pemberton, 1992)。在漫长的进化过程中, 蚂蚁与植物之间究竟从何时起通过何种方式建立了互利关系, 这种互利关系如何得以维持?互利是否起源于捕食、寄生等敌对的相互作用?或是盗取植物蜜露、寄生于植物之上的蚂蚁都由互利者转化而来?虽然已有少量研究对这些问题进行了探讨, 但上述问题仍然是未解之谜, 系统发育树的建立等分子手段可能是解决这些问题的有力工具。
(2)互利关系对蚂蚁的影响尚不清楚。虽然目前的绝大多数研究以互利作用为出发点, 但大多探讨的是对植物一方的影响(Styrsky & Eubanks, 2007; Chamberlain & Holland, 2009; Rosumek et al., 2009), 而对于蚂蚁一方的影响极少涉及, 尤其是互利关系对蚂蚁的适合度的影响, 仅见于Palmer等(2008)和 Ness等(2009)的研究中。这种研究的偏爱性可能是由于植物对蚂蚁的影响难以控制, 指标不易选取和测量造成的, 也可能是因为大多研究者想当然地认为蚂蚁只是从中获取了食物而已。探讨互利关系对双方的影响对于了解互利的产生和维持机制具有重要意义(Bronstein, 1994a), 所以将来急需加强互利对蚂蚁一方影响的研究。
(3)缺乏这种互利关系与生物入侵的联系的研究。与其他生物一样, 蚂蚁的入侵同样会引发巨大的生态后果(Holway et al., 2002), 但目前的研究大多偏重于蚂蚁对入侵地的生物群落的直接影响, 对于一些更深入的关键问题缺乏探讨。比如, 蚂蚁入侵某地后, 是否能够取代本土种蚂蚁而继续发挥其生态功能?入侵的蚂蚁大都体型较小, 攻击性强且数量惊人, 它们能否与当地一些本土植物重新建立互利关系? 一旦建立互利关系, 会具有什么样的生态影响?本土蚂蚁与植物相互作用的网络结构对于外来蚂蚁的入侵有何影响?蚂蚁与植物的相互作用对于其他植物或昆虫的入侵也可能会产生一定影响, 有时甚至形成入侵种之间的互利, 使得入侵更加剧烈和难以控制(Helms & Vinson, 2002)。对于上述问题的探讨, 将大大加深我们对蚂蚁、植物、昆虫入侵的机理与生态效应的认识, 有利于运用科学的方法对生物入侵进行控制。
(4)对互利双方的长期影响研究较少。当前绝大多数的研究都基于对互利关系的短期结果的探讨上, 一般不超过3年, 而长期的研究非常少(Palmer et al., 2008)。尤其是在当前全球变暖、生物多样性丧失加剧的背景下, 建立长期的站点对互利关系及其生态影响进行定点跟踪研究, 显得颇为必要。
蚂蚁是陆地生态系统中数量最为庞大的顶级捕食动物之一, 有理由相信, 它们在生态系统中发挥着重要的作用(Hölldobler & Wilson, 1990)。目前人们对蚂蚁在食物网络、养分循环、能量流动、生物多样性维持等生态过程中的作用还很不清楚。蚂蚁对植物的保护及其生态与进化意义, 是当前种间互利作用和协同进化研究中的热点问题和经典模式系统, 尤其是近年来的研究表明, 种间互利关系的引入, 将会极大地改变甚至颠覆以往建立在捕食、竞争等种间敌对关系之上的生态学经典范式(Bruno et al., 2003)。国内对于蚂蚁的生态意义的研究相对薄弱, 目前局限于蚂蚁的多样性调查及其在种子传播中的作用(徐正会, 1999; 张智英等, 2001; 陈帆等, 2004; Zhou et al., 2007; 张霜和陈进, 2008), 尚未开展有关蚂蚁对植物的保护作用的相关研究。本文通过综述当前蚂蚁对植物保护作用的研究进展及存在的问题和不足, 以期引起国内同行对此领域的关注和兴趣, 加强对该领域相关问题的研究与探讨。
责任编委: 安黎哲 责任编辑: 王 葳
致谢
国家自然科学基金(30900185)资助项目。北京名壹堂图书公司张花女士在论文写作过程中给予了大力帮助, 特此致谢。
参考文献
Role of floral repellents in the regulation of flower visits of extrafloral nectary-visiting ants in an Indian crop plant
Leaf damage and associated cues induce aggressive ant recruitment in a neotropical ant-plant
Filling key gaps in population and community ecology
Novel interactions of non-pollinating ants with pollinators and fruit consumers in a tropical forest
Ant-plant association in two Tococa species from a primary rain forest of Colombian Choco (Hymenoptera: Formicidae).
Ant inhibition of pollen function: a possible reason why ant pollination is rare
How plants shape the ant community in the Amazonian rainforest canopy: the key role of extrafloral nectaries and homopteran honeydew
a). Our current understanding of mutualism
b). Conditional outcomes in mutualistic interactions
The contribution of ant plant protection studies to our understanding of mutualism
Plant lock and ant key: pairwise coevolution of an exclusion filter in an ant-plant mutualism
Inclusion of facilitation into ecological theory
Interactions involving plants, homoptera, and ants
Quantitative synthesis of context dependency in ant-plant protection mutualisms
Context dependency, variation in the outcome of species interactions with biotic and abiotic conditions, is increasingly considered ubiquitous among mutualisms. Despite several qualitative reviews of many individual empirical studies, there has been little quantitative synthesis examining the generality of context dependency, or conditions that may promote it. We conducted a meta-analysis of ant-plant protection mutualisms to examine the generality of context-dependent effects of ants on herbivory and plant performance (growth, reproduction). Our results show that ant effects on plants are not generally context dependent, but instead are routinely positive and rarely neutral, as overall effect sizes of ants in reducing herbivory and increasing plant performance were positive and significantly greater than 0. The magnitude of these positive effects did vary, however. Variation in plant performance was not explained by the type of biotic or abiotic factor examined, including plant rewards (extrafloral nectar, food bodies, domatia), ant species richness, plant growth form, or latitude. With the exception of plant growth form, these factors did contribute to the effects of ants in reducing herbivory. Reductions in herbivory were greater for plants with than without domatia, and greatest for plants with both domatia and food bodies. Effect sizes of ants in reducing herbivory decreased, but remained positive, with latitude and ant species richness. Effect sizes in reducing herbivory were greater in tropical vs. temperate systems. Although ant-plant interactions have been pivotal in the study of context dependency of mutualisms, our results, along with other recent meta-analyses, indicate that context dependency may not be a general feature of mutualistic interactions. Rather, ant-plant protection mutualisms appear to be routinely positive for plants, and only occasionally neutral.
The role of ants in seed dispersal of Globba lancangensis and the spatial distribution of its seedlings
Red imported fire ants (Hymenoptera : Formicidae) increase the abundance of aphids in tomato
Explaining the abundance of ants in lowland tropical rainforest canopies
Invasive ants disrupt frugivory by endemic island birds
The role of ant-tended extrafloral nectaries in the protection and benefit of a neotropical rainforest tree
Ant-plants and fungi: a new threeway symbiosis
Nest site selection and induced response in a dominant arboreal ant species
Arboreal ants use the “Velcroh Principle” to capture very large prey
Ant-homoptera interactions in a neotropical savanna: the honeydew-producing treehopper, Guayaquila xiphias (Membracidae), and its associated ant fauna on Didymopanax vinosum (Araliaceae)
Conditional outcomes in a neotropical treehopper-ant association: temporal and species-specific variation in ant protection and homopteran fecundity
Variation in the effectiveness of biotic defence: the case of an opportunistic ant-plant protection mutualism
Why are there so few species of aphids, especially in the tropics
Can the failure to punish promote cheating in mutualism?
Protection in an ant-plant mutualism: an adaptation or a sensory trap?
A plant needs ants like a dog needs fleas: Myrmelachista schumanni ants gall many tree species to create housing.
Tolerating castration by hiding flowers in plain sight
Estimates of the direct and indirect effects of red imported fire ants on biological control in field crops
Slippery ant-plants and skilful climbers: selection and protection of specific ant partners by epicuticular wax blooms in Macaranga(Euphorbiaceae).
Pruning of host plant neighbours as defence against enemy ant invasions: Crematogaster ant partners of Macaranga protected by “wax barriers” prune less than their congeners.
Active use of the metapleural glands by ants in controlling fungal infection
Aphid-ant interaction reduces chrysomelid herbivory in a cottonwood hybrid zone
Herbivory and the long-lived leaves of an Amazonian ant-tree
‘Devil’s gardens’ bedevilled by ants
'Devil's gardens' are large stands of trees in the Amazonian rainforest that consist almost entirely of a single species, Duroia hirsuta, and, according to local legend, are cultivated by an evil forest spirit. Here we show that the ant Myrmelachista schumanni, which nests in D. hirsuta stems, creates devil's gardens by poisoning all plants except its host plants with formic acid. By killing these other plants, M. schumanni provides its colonies with abundant nest sites--a long-lasting benefit as colonies can live for 800 years.
Ants in your plants: effects of nectar-thieves on pollen fertility and seed-siring capacity in the alpine wildflower, Polemonium viscosum
Benefits conferred by “timid” ants: active anti-herbivore protection of the rainforest tree Leonardoxa africana by the minute ant Petalomyrmex phylax.
Can floral repellents pre-empt potential ant-plant conflicts?
The role of extrafloral nectar amino acids for the preferences of facultative and obligate ant mutualists
Indirect defense in a highly specific ant-plant mutualism
Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced, indirect, defensive response elicited by jasmonic acid.
Plant species in at least 66 families produce extrafloral nectar (EFN) on their leaves or shoots and therewith attract predators and parasitoids, such as ants and wasps, which in turn defend them against herbivores. We investigated whether EFN secretion is induced by herbivory and/or artificial damage, and thus can be regarded as an induced defensive response. In addition, we studied the underlying signaling pathway. EFN secretion by field-grown Macaranga tanarius increased after herbivory, artificial leaf damage, and exogenous jasmonic acid (JA) application. Artificial damage strongly enhanced endogenous JA concentrations. The response in EFN production to artificial damage was much less pronounced in those leaves that were treated with phenidone to inhibit endogenous JA synthesis. Quantitative dose-response relations were found between the increase in nectar production and both the intensity of leaf damage and the amounts of exogenously applied JA. The amount of endogenously produced JA was positively correlated with the intensity of leaf damage. Increased numbers of defending insects and decreased numbers of herbivores were observed on leaves after inducing EFN production by exogenous JA treatment. Over 6 weeks, repeatedly applied JA or artificial damage resulted in a ten-fold reduction in herbivory. These results demonstrate that EFN production represents an alternative mechanism for induced, indirect defensive plant responses that are mediated via the octadecanoid signal transduction cascade.
Protective ant-plant interactions as model systems in ecological and evolutionary research
Postsecretory hydrolysis of nectar sucrose and specialization in ant/plant mutualism
Obligate Acacia ant plants house mutualistic ants as a defense mechanism and provide them with extrafloral nectar (EFN). Ant/plant mutualisms are widespread, but little is known about the biochemical basis of their species specificity. Despite its importance in these and other plant/animal interactions, little attention has been paid to the control of the chemical composition of nectar. We found high invertase (sucrose-cleaving) activity in Acacia EFN, which thus contained no sucrose. Sucrose, a disaccharide common in other EFNs, usually attracts nonsymbiotic ants. The EFN of the ant acacias was therefore unattractive to such ants. The Pseudomyrmex ants that are specialized to live on Acacia had almost no invertase activity in their digestive tracts and preferred sucrose-free EFN. Our results demonstrate postsecretory regulation of the carbohydrate composition of nectar.
Divergent investment strategies of Acacia myrmecophytes and the coexistence of mutualists and exploiters.
Ant-plant interactions represent a diversity of strategies, from exploitative to mutualistic, and how these strategies evolve is poorly understood. Here, we link physiological, ecological, and phylogenetic approaches to study the evolution and coexistence of strategies in the Acacia-Pseudomyrmex system. Host plant species represented 2 different strategies. High-reward hosts produced significantly more extrafloral nectar (EFN), food bodies, and nesting space than low-reward hosts, even when being inhabited by the same species of ant mutualist. High-reward hosts were more effectively defended against herbivores and exploited to a lower extent by nondefending ants than low-reward hosts. At the phenotypic level, secretion of EFN and ant activity were positively correlated and a mutualistic ant species induced nectar secretion, whereas a nondefending exploiter did not. All of these mechanisms contribute to the stable association of high-reward hosts with defending ant species. However, exploiter ants are less dependent on the host-derived rewards and can colonize considerable proportions of the low-reward hosts. Mapping these strategies onto phylogenetic trees demonstrated that the low-reward hosts represent the derived clade within a monophyletic group of obligate ant plants and that the observed exploiter ant species evolved their strategy without having a mutualistic ancestor. We conclude that both types of host strategies coexist because of variable net outcomes of different investment-payoff regimes and that the effects of exploiters on the outcome of mutualisms can, thus, increase the diversity within the taxa involved.
Widespread association of the invasive ant Solenopsis invicta with an invasive mealybug.
The causes and consequences of ant invasions
An indirect mutualism between oaks and wood ants via aphids
Cheating the cheater: domatia loss minimizes the effects of ant castration in an Amazonian ant-plant
Coevolution of mutualism between ants and acacias in Central America
Bottom-up effects of plant genotype on aphids, ants, and predators
Aphids alter the community-wide impact of fire ants
Changes in the use of extrafloral nectaries of Vicia faba(Leguminosae) and honeydew of aphids by ants with increasing aphid density.
Argentine ants displace floral arthropods in a biodiversity hotspot
Do birch trees ( Betula pendula) grow better if foraged by wood ants?
Herbivory in a spider through exploitation of an ant-plant mutualism
Plant protection as a consequence of an ant-membracid mutualism: interactions on goldenrod (Solidago sp.).
Tritrophic effects of birds and ants on a canopy food web, tree growth, and phytochemistry
Plant genotype shapes ant-aphid interactions: implications for community structure and indirect plant defense
Many plant species have been introduced from their native ranges to new continents, but few have become naturalized or, ultimately, invasive. It has been predicted that species that do not require the presence of compatible mates and the services of pollinators for reproduction will be favored in establishment after long-distance dispersal. We tested whether this hypothesis, generally referred to as Baker's law, holds for South African species of Iridaceae (iris family) that have been introduced in other regions for horticultural purposes. Fruit and seed production of flowers from which pollinators had been experimentally excluded was assessed for 10 pairs of species from nine different genera or subgenera. Each species pair comprised one naturalized and one nonnaturalized species, all of which are used in international horticulture. On average, species of Iridaceae that have become naturalized outside their native ranges showed a higher capacity for autonomous fruit and seed production than congeneric species that have not become naturalized. This was especially true for the naturalized species that are considered to be invasive weeds. These results provide strong evidence for the role of autonomous seed production in increasing potential invasiveness in plants.
Temporal and spatial variation to ant omnivory in pine forests
Long-term persistence of a neotropical ant-plant population in the absence of obligate plant-ants
Direct and indirect effects of ants on a forest-floor food web
Interactions among predators that prey on each other and are potential competitors for shared prey (intraguild [IG] predators) are widespread in terrestrial ecosystems and have the potential to strongly influence the dynamics of terrestrial food webs. Ants and spiders are abundant and ubiquitous terrestrial IG predators, yet the strength and consequences of interactions between them are largely unknown. In the leaf-litter food web of a deciduous forest in Kentucky (USA), we tested the direct and indirect effects of ants on spiders and a category of shared prey (Collembola) by experimentally subsidizing ants in open plots in two field experiments. In the first experiment, ant activity was increased, and the density of ants in the litter was doubled, by placing carbohydrate and protein baits in the center of each plot. Gnaphosa spiders were almost twice as abundant and Schizocosa spiders were half as abundant in baited plots relative to controls. There were more tomocerid Collembola in baited plots, suggesting possible indirect effects on Collembola caused by ant-spider interactions. The second experiment, in which screening of two mesh sizes selectively excluded large and small worker ants from a sugar bait, revealed that the large ants, primarily Camponotus, could alone induce similar effects on spiders. Gnaphosa biomass density was almost twice as high in the plots where large ants were more active, whereas Schizocosa biomass density was reduced by half in these plots. Although tomocerid densities did not differ between treatments, tomocerid numbers were negatively correlated with the activity of Formica, another large ant species. Path analysis failed to support the hypothesis that the ant Camponotus indirectly affected tomocerid Collembola through effects on densities of spiders. However, path analysis also revealed other indirect effects of Camponotus affecting tomocerids. These results illustrate the complexity of interactions between and within two major IG predator groups with disparate predatory behaviors, complexities that will have consequences for functioning of the forest-floor food web.
A mutualism’s indirect costs: the most aggressive plant bodyguards also deter pollinators
For ant-protected plants, the best defense is a hungry offense
Animal foraging has been characterized as an attempt to maximize the intake of carbon and nitrogen at appropriate ratios. Plant species in over 90 families produce carbohydrate-rich extrafloral nectar (EFN), a resource attractive to ants and other omnivorous insects. This attraction can benefit the plant if those arthropods subsequently attack herbivores. This protective response has been attributed to the increased visitation and
Evidence that insect herbivores are deterred by ant pheromones
Ant-plant-herbivore interactions in the neotropical cerrado savanna
The Brazilian cerrado savanna covers nearly 2 million km2 and has a high incidence on foliage of various liquid food sources such as extrafloral nectar and insect exudates. These liquid rewards generate intense ant activity on cerrado foliage, making ant-plant-herbivore interactions especially prevalent in this biome. We present data on the distribution and abundance of extrafloral nectaries in the woody flora of cerrado communities and in the flora of other habitats worldwide, and stress the relevance of liquid food sources (including hemipteran honeydew) for the ant fauna. Consumption by ants of plant and insect exudates significantly affects the activity of the associated herbivores of cerrado plant species, with varying impacts on the reproductive output of the plants. Experiments with an ant-plant-butterfly system unequivocally demonstrate that the behavior of both immature and adult lepidopterans is closely related to the use of a risky host plant, where intensive visitation by ants can have a severe impact on caterpillar survival. We discuss recent evidence suggesting that the occurrence of liquid rewards on leaves plays a key role in mediating the foraging ecology of foliage-dwelling ants, and that facultative ant-plant mutualisms are important in structuring the community of canopy arthropods. Ant-mediated effects on cerrado herbivore communities can be revealed by experiments performed on wide spatial scales, including many environmental factors such as soil fertility and vegetation structure. We also present some research questions that could be rewarding to investigate in this major neotropical savanna.
Numerical abundance of invasive ants and monopolisation of exudate-producing resources―a chicken and egg situation
Mutualism as reciprocal exploitation: African plant-ants defend foliar but not reproductive structures
Breakdown of an ant-plant mutualism follows the loss of large herbivores from an African savanna
Mutualisms are key components of biodiversity and ecosystem function, yet the forces maintaining them are poorly understood. We investigated the effects of removing large mammals on an ant-Acacia mutualism in an African savanna. Ten years of large-herbivore exclusion reduced the nectar and housing provided by plants to ants, increasing antagonistic behavior by a mutualistic ant associate and shifting competitive dominance within the plant-ant community from this nectar-dependent mutualist to an antagonistic species that does not depend on plant rewards. Trees occupied by this antagonist suffered increased attack by stem-boring beetles, grew more slowly, and experienced doubled mortality relative to trees occupied by the mutualistic ant. These results show that large mammals maintain cooperation within a widespread symbiosis and suggest complex cascading effects of megafaunal extinction.
Fossil extrafloral nectaries, evidence for the ant-guard antiherbivore defense in an Oligocene Populus.
Spatial structuring and floral avoidance behavior prevent ant-pollinator conflict in a Mexican ant-acacia
Ant- herbivore interactions: reasons for the absence of benefits to a fern with foliar nectaries
Population variation in plant traits associated with ant attraction and herbivory in Chamaecrista fasciculata(Fabaceae).
The benefits of ant-plant-herbivore interactions for the plant depend on the abundance of ants and herbivores and the selective pressures these arthropods exert. In plants bearing extrafloral nectaries (EFN), different mean trait values may be selected for by different populations in response to local herbivore pressure, ultimately resulting in the evolution of differences in plant traits that attract ants as defensive agents against herbivory. To determine if variation in traits that mediate ant-plant interactions reflect herbivore selective pressures, we quantified intra- and inter-population variation in plant traits for eight populations of the EFN-bearing annual Chamaecrista fasciculata (Michx.) (Fabaceae). Censuses in rural and urban areas of Missouri and Illinois (USA) showed population differences in ant attendance and herbivore pressure. Seeds were collected from each population, and plants were grown in a common greenhouse environment to measure sugar production, nectar volume and composition, EFN size and time of emergence, leaf pubescence, and leaf quality throughout plant development. Populations varied mainly in terms of nectary size, sugar production, and nectar volume, but to a lesser degree in leaf pubescence. Populations of C. fasciculata within urban areas (low in insect abundance) had small nectaries and the lowest nectar production. There was a positive correlation across populations between herbivore density and leaf damage by those herbivores on the one hand and sugar production and nectar volume on the other. These results, in conjunction with lack of evidence for maternally based environmental effects, suggest that population differences in herbivore damage have promoted differential evolution of EFN-related traits among populations.
Mutualism in which ants must be present before plants produce food bodies
Ants on plants: a meta-analysis of the role of ants as plant biotic defenses
We reviewed the evidence on the role of ants as plant biotic defenses, by conducting meta-analyses for the effects of experimental removal of ants on plant herbivory and fitness with data pooled from 81 studies. Effects reviewed were plant herbivory, herbivore abundance, hemipteran abundance, predator abundance, plant biomass and reproduction in studies where ants were experimentally removed (n = 273 independent comparisons). Ant removal exhibited strong effects on herbivory rates, as plants without ants suffered almost twice as much damage and exhibited 50% more herbivores than plants with ants. Ants also influenced several parameters of plant fitness, as plants without ants suffered a reduction in biomass (-23.7%), leaf production (-51.8%), and reproduction (-24.3%). Effects were much stronger in tropical regions compared to temperate ones. Tropical plants suffered almost threefold higher herbivore damage than plants from temperate regions and exhibited three times more herbivores. Ant removal in tropical plants resulted in a decrease in plant fitness of about 59%, whereas in temperate plants this reduction was not statistically significant. Ant removal effects were also more important in obligate ant-plants (=myrmecophytes) compared to plants exhibiting facultative relationships with hemiptera or those plants with extrafloral nectaries and food bodies. When only tropical plants were considered and the strength of the association between ants and plants taken into account, plants with obligate association with ants exhibited almost four times higher herbivory compared to plants with facultative associations with ants, but similar reductions in plant reproduction. The removal of a single ant species increased plant herbivory by almost three times compared to the removal of several ant species. Altogether, these results suggest that ants do act as plant biotic defenses, but the effects of their presence are more pronounced in tropical systems, especially in myrmecophytic plants.
Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants
Egg-laying butterflies distinguish predaceous ants by sight
Ecology and evolution of aphid-ant interactions
Is host plant choice by a clytrine leaf beetle mediated through interactions with the ant Crematogaster lineolata?
In the grasslands of northeastern Kansas, adult populations of Anomoea flavokansiensis, an oligophagous leaf beetle (subfamily Clytrinae), specialize on Illinois bundleflower (Desmanthus illinoensis) even though other reported host species commonly occur and are simultaneously available. We performed choice feeding tests to examine whether A. flavokansiensis adults have a fixed feeding preference for bundleflower. In choice tests, beetles ate similar amounts of bundleflower and honey locust (Gleditsia triacanthos). In addition, we measured fecundity and longevity of adults in no-choice tests to determine if adults were adapted solely to bundleflower. In no-choice tests, fecundity and longevity were no different for adults feeding on bundleflower and honey locust. We next examined the influence of host plant on the attractiveness of beetle eggs to ants. In northeastern Kansas, Crematogaster lineolata ants are attracted to A. flavokansiensis eggs and carry them into their nests where the larvae hatch and apparently reside as inquilines. C. lineolata exhibited a strong preference for eggs from female A. flavokansiensis that fed exclusively on bundleflower compared to eggs from females that fed exclusively on honey locust. Local populations of A. flavokansiensis in northeastern Kansas may specialize on bundleflower to increase the chances of their eggs being transported by C. lineolata ants into their nests. C. lineolata nests may serve as a predator-free and sheltered environment in which A. flavokansiensis eggs undergo embryogenesis.
Ecological consequences of interactions between ants and honeydew-producing insects
Evolutionary biology: butterfly mimics of ants
Effects of plant age, experimental nutrient addition and ant occupancy on herbivory in a neotropical myrmecophyte
Farmers perceptions and practices in use of Dolichoderus thoracicus (Smith) (Hymenoptera: Formicidae) for biological control of pests of sapodilla
Mutualism between ants and honeydew- producing homoptera
Role of ants in pest management
Floral volatiles controlling ant behaviour
How aggressive ant-guards assist seed-set in Acacia flowers.
Biodiversity consequences of predation and host plant hybridization on an aphid-ant mutualism
An analysis on the ant fauna of the tropical rain forest in Xishuangbanna of China
A castration parasite of an ant-plant mutualism
Codariocalyx motorius seed removed by ants in Xishuangbanna
Secondary seed dispersal of Ficus benjamina: new evidence for ant-nonmyrmecochorous mutualism
Ant-mediated seed dispersal contributes to the local spatial pattern and genetic structure of Globba lanciangensis(Zingiberaceae).
