青藏高原及周边高山地区的植物繁殖生态学研究进展

青藏高原及周边高山地区孕育了极为丰富的植物多样性资源, 研究该地区植物如何顺利完成繁殖过程有助于我们理解植物对典型高山环境的进化和适应机制。该文综述了青藏高原地区高山植物在资源分配、繁殖方式、花部特征演化等方面的研究进展, 包括全球气候变化对植物繁殖特征的影响, 以及一些新技术和新方法在本研究领域的应用。在高山地区限制性环境中, 随海拔升高, 繁殖分配通常表现出增大的趋势, 其中投入到雄性资源的比例上升, 但具体的资源分配模式还要取决于植株的交配系统、个体大小、生活史特征、遗传特性以及环境中的资源有效性等。面对资源和传粉的双重限制, 植物在不同繁殖方式之间存在权衡, 当传粉者稀少时, 克隆繁殖和自交有利于繁殖保障; 而有性繁殖和异交能够提高种子的质量和后代的遗传多样性, 从而在复杂多变的气候条件下有利于种群的维持。因此, 不同繁殖方式的结合以及泛化的传粉互作网络可能是应对高山限制性环境的最优选择。花部特征的演化主要受到当地传粉者的选择压力, 但是外来传粉者、植食者、盗蜜者以及非生物环境(如温度、雨水和紫外辐射等)对花部性状的影响越来越受到重视。近年来, 青藏高原因其脆弱性和对气候变化的高度敏感性而在全球气候变化研究中备受关注, 以全球变暖和氮沉降增加为显著特征的全球气候变化正在直接或间接地影响着该地区高山植物的繁殖特征。气候变化影响植物和传粉者的物候并引起物种的迁移, 最终将导致植物与传粉者的时空不匹配。植物通过改变花部特征(花展示、花冠结构、花报酬的数量和质量)来响应气候变化, 这可能会改变其传粉者的类型、数量和访花行为, 从而最终影响植物的繁殖成功。3D打印和高通量测序等新技术和新方法的应用有助于促进植物繁殖生态学研究的进一步发展。3D打印的花能够精确控制其形态构造, 可以用于研究精细的花部特征变化对于传粉者行为的影响, 在此基础上与人工饲养的传粉者结合使用, 有助于进一步研究传粉者介导的花部特征演化。随着高通量测序技术的发展, 植物繁殖生态学领域, 尤其是花部特征演化的许多重要问题的潜在机制得以深入研究。该文最后提出了目前研究中需要注意的问题以及值得深入研究的发展方向。     

高山物种栗色鼠尾草(Salvia castanea Diels)访花昆虫多样性与传粉行为变化

唇形科鼠尾草属是世界性分布、物种多样性丰富的大类群,具有独特的传粉模式和多样化的生态类型及繁殖策略,以往对鼠尾草属的花结构和雄蕊杠杆的生态功能、雄蕊杠杆机制对传粉者空间变异的进化响应和表型选择等方面已有较深入的研究,但至今对分布于不同区系代表性物种的传粉者组成、访花行为和繁育系统特征仍知之甚少。对分布于喜马拉雅东段至横断山高海拔地区栗色鼠尾草的传粉生态、交配系统和繁殖特性进行了研究,分析了2014年至2016年的年际间、2014年晴天和阴雨天的传粉者组成和传粉行为变化,探讨了这些变化对繁殖成功的影响。研究结果表明：3年共发现栗色鼠尾草有9种访花昆虫,传粉者组成及其行为变化较为明显。2014年有桔尾熊蜂Bombus friseanus、灰熊蜂B.grahami、圣熊蜂B.religiosus和中华蜜蜂Apis cerana 4种有效传昆虫,2015年仅有桔尾熊蜂是有效传粉者,而2016年的有效传粉昆虫改变为灰熊蜂和圣熊蜂。栗色鼠尾草的盗蜜现象较为普遍,主要盗蜜昆虫为灰熊蜂和桔尾熊蜂。桔尾熊蜂访花行为的年际变化较大,受天气条件的影响明显,同时其有效传粉行为可能显著影响了灰熊蜂的盗蜜行为。栗色鼠尾草的繁育系统为专性异交,主要依靠传粉者进行授粉,缺少传粉者时低程度的主动自花授粉可为其提供繁殖保障,且没有花粉限制和近交衰退。研究揭示了在高海拔地区,多变的天气条件可能显著影响着鼠尾草属植物的传粉者种类组成、访花行为和传粉效率,进而影响植物的繁殖成效和种群稳定。有效传粉频率是保证栗色鼠尾草较高自然结实率的主要因素,在一定程度上,盗蜜强度对繁殖成功具有中性的影响。本研究结果为阐明高山鼠尾草物种的繁殖如何受气候环境变化的影响,以及保证繁殖成功的可能策略奠定基础。     

云南草蔻花蜜分泌格局与访花动物行为及其对果实和种子产量的影响

依靠动物传粉的植物, 其繁殖成功 (胚珠受精与花粉散布 ) 很大程度上取决于访花动物的种类和拜访行为, 而访花动物的种类和行为又受植物提供给传粉者的回报, 主要是花蜜分泌格局的影响。通过对姜科山姜属植物云南草蔻 (Alpiniablepharocalyx) 花蜜分泌量及糖分含量的测定, 拜访动物种类、传粉昆虫拜访频率及停留时间的调查, 主要盗蜜者花松鼠 (Tamiopsswinhoei) 的盗蜜行为观察, 植物的结实率以及结籽量的分析等, 探讨花蜜分泌与传粉昆虫的关系以及盗蜜对果实及种子生产的影响。研究表明 :云南草蔻的两种花型花蜜的分泌量在一天的单花开花过程中呈现相反的格局, 花柱上举型花下午的花蜜分泌量高于上午, 而花柱下垂型花则上午略高于下午 ;两种花型花蜜的糖分浓度都随着开花时间而下降 ;共有 17种访花动物拜访云南草蔻的花, 其中 8种具有传粉作用 ;传粉昆虫的停留时间随拜访频率的不断增加而缩短 ;被盗蜜植株与未被盗蜜植株的结实率差异不显著而结籽量差异显著。     

盗蜜对角蒿传粉者行为和生殖成功的影响

一些研究显示盗蜜对自交植物的结实和结籽没有显著影响。然而, 对于既有传粉者为其传粉实现异交又能通过自交实现生殖保障的兼性自交植物来说, 盗蜜对其生殖的影响还知之甚少。由于兼性自交植物可以自交, 盗蜜对其总体结实可能不会有显著影响, 但可能会通过影响传粉者行为而影响传粉者介导的结实。为了验证这一假说, 本研究以兼性自交的一年生角蒿(Invarvillea sinensis var. sinensis)为研究材料, 通过野外调查和控制实验, 探讨了盗蜜对传粉者介导的结实(传粉者行为)和总体结实率的影响。结果表明: 角蒿的盗蜜者和主要传粉者相同, 均为密林熊蜂(Bombus patagiatus)。熊蜂盗蜜频率平均为20.24% (范围为0-51.43%)。盗蜜对角蒿总体结实率、每果结籽数和每果种子重量没有显著影响。然而, 被盗蜜花的柱头闭合比率显著高于未被盗蜜花, 说明盗蜜影响传粉者的访花行为和传粉者介导的结实率。另外, 被盗蜜花的高度显著高于未被盗蜜花, 说明盗蜜者倾向于从较大较高的花上盗蜜。这些结果为全面认识盗蜜对植物生殖的影响提供了新的信息。     

青藏高原及周边高山地区的植物繁殖生态学研究进展

青藏高原及周边高山地区孕育了极为丰富的植物多样性资源,研究该地区植物如何顺利完成繁殖过程有助于我们理解植物对典型高山环境的进化和适应机制。该文综述了青藏高原地区高山植物在资源分配、繁殖方式、花部特征演化等方面的研究进展,包括全球气候变化对植物繁殖特征的影响,以及一些新技术和新方法在本研究领域的应用。在高山地区限制性环境中,随海拔升高,繁殖分配通常表现出增大的趋势,其中投入到雄性资源的比例上升,但具体的资源分配模式还要取决于植株的交配系统、个体大小、生活史特征、遗传特性以及环境中的资源有效性等。面对资源和传粉的双重限制,植物在不同繁殖方式之间存在权衡,当传粉者稀少时,克隆繁殖和自交有利于繁殖保障;而有性繁殖和异交能够提高种子的质量和后代的遗传多样性,从而在复杂多变的气候条件下有利于种群的维持。因此,不同繁殖方式的结合以及泛化的传粉互作网络可能是应对高山限制性环境的最优选择。花部特征的演化主要受到当地传粉者的选择压力,但是外来传粉者、植食者、盗蜜者以及非生物环境(如温度、雨水和紫外辐射等)对花部性状的影响越来越受到重视。近年来,青藏高原因其脆弱性和对气候变化的高度敏感性而在全球气候变化研究中备受关注,以全球变暖和氮沉降增加为显著特征的全球气候变化正在直接或间接地影响着该地区高山植物的繁殖特征。气候变化影响植物和传粉者的物候并引起物种的迁移,最终将导致植物与传粉者的时空不匹配。植物通过改变花部特征(花展示、花冠结构、花报酬的数量和质量)来响应气候变化,这可能会改变其传粉者的类型、数量和访花行为,从而最终影响植物的繁殖成功。3D打印和高通量测序等新技术和新方法的应用有助于促进植物繁殖生态学研究的进一步发展。3D打印的花能够精确控制其形态构造,可以用于研究精细的花部特征变化对于传粉者行为的影响,在此基础上与人工饲养的传粉者结合使用,有助于进一步研究传粉者介导的花部特征演化。随着高通量测序技术的发展,植物繁殖生态学领域,尤其是花部特征演化的许多重要问题的潜在机制得以深入研究。该文最后提出了目前研究中需要注意的问题以及值得深入研究的发展方向。     

火把花的繁殖生物学研究

火把花（Colquhounia coccinea?）表现出典型的鸟媒综合征,因此具有作为引鸟景观植物的开发潜力。以自然、人工生境的火把花居群为研究对象,通过观察和试验对其开花物候、花部综合特征、访花动物及其行为、繁育系统、种子萌发特性进行研究,以明确火把花的繁殖特性及对不同访花动物的吸引潜力。结果显示,火把花的整体花期持续约3个月,单花花期为9.6±0.6 d;花蜜较丰富且稀薄,具有较短的花冠管和己糖为主的花蜜糖组成;访花动物主要是中华蜜蜂和多种食蜜鸟类,尤其是短喙的泛化鸟类,且在非自然生境中仍然能吸引鸟类访花;完全自交亲和但需要传粉者才能完成授粉,不存在花粉限制;不同授粉处理种子的发芽能力无显著差异;中华蜜蜂能有效传粉,鸟类的传粉作用需进一步验证。综上所述,火把花可供观赏的时间很长,具有明显的吸引鸟类访花的能力,容易通过有性繁殖途径快速获得大量幼苗。     

菊科12种外来植物的有性繁殖特征和入侵风险研究

菊科植物具有极强的有性繁殖能力,对外来菊科观赏植物的引进存在极高的入侵风险。本研究以武汉常见的菊科12种外来观赏植物为对象,通过有性繁殖特征调查,研究植株的花部特征、花粉活力、传粉系统、种子产量,分析各物种有性繁殖能力的差异,评估其入侵能力。结果显示,多数物种可在隔绝传粉者情况下结实;访花昆虫类型多样,共观察到26种访花昆虫,其中膜翅目蜂类是主要的传粉者;结实情况具有一定差异。综合考虑花粉活力、传粉情况和结实情况,认为黑心金光菊(Rudbeckia hirta L.)、松果菊(Echinacea purpurea(L.)Moench)、大花金鸡菊(Coreopsis grandiflora Hogg.)、蛇目菊(Sanvitalia procumbens Lam.)的有性繁殖竞争力较高,对本地传粉环境可能有较大影响。本研究对近缘物种有性繁殖特征的综合分析结果可为评估外来物种的入侵风险提供一定的参考。     

大叶铁线莲访花昆虫调查及盗蜜昆虫行为研究

大叶铁线莲Clematis heracleifolia DC. 的花朵大多下垂,需要传粉昆虫为其传粉,目前尚无关于其访花昆虫研究的报道。 通过2年的野外观察研究,共观察到27种昆虫访问大叶铁线莲。 发现有盗蜜行为的昆虫7种, 其中1种同时具有初级盗蜜和次级盗蜜行为,2种具有初级盗蜜行为,4种具有次级盗蜜行为;黄胸木蜂Xylocopa appendiculata Smith是主要的盗蜜昆虫,其盗蜜行为影响了其它昆虫的访花行为,对大叶铁线莲的传粉造成一定的影响。 在其余20种访花昆虫中,双带弄蝶Lobocla bifasciata (Bremer et Grey)、贡尺蛾Gonodontis aurata Prout、熊蜂Bombus sp.和姬蜂虻Systropus sp.是优势种; 而小青花金龟Oxycetonia jucunda Faldermann和日本条螽Ducetia japonica (Thunberg)访花频率最低,且访花目的只是取食花朵。 通过对大叶铁线莲访花昆虫的调查和盗蜜昆虫行为的研究,为大叶铁线莲的传粉生物学和保护提供参考依据。     

毛乌素沙地固沙植物披针叶黄华主要传粉昆虫及其访花行为

披针叶黄华(Thermopsis lanceolata)是我国西部地区早春重要野生蜜源植物,也是一种重要的固沙植物,然而对其繁殖特性的研究甚少.本文在系统调查披针叶黄华的访花昆虫基础上,确定其主要传粉昆虫种类、访花行为、传粉过程以及日活动规律,以期揭示主要访花者行为对其有性繁殖的影响.作者在内蒙古毛乌素沙地设置1个10m×10 m的样方,于2010和2011年在披针叶黄华盛花期,采用目测、拍照和摄像等方式对传粉昆虫进行观测,记录样方内主要访花昆虫种类、数量、访花行为及日活动规律.研究表明,大和切叶蜂(Megachile japonica)和戎拟孔蜂(Hoplitis princeps)是披针叶黄华的主要传粉者,但两种昆虫的访花频率存在显著差异;晴天时,大和切叶蜂在19:00-13:00和16:00-18:00出现两个活动高峰,而戎拟孔蜂只在11:30-16:30出现1个活动高峰,两种蜂的访花活动高峰期存在互补关系.大和切叶蜂访花同时具有盗蜜行为,但其盗蜜行为对披针叶黄华的结籽率没有显著影响.根据种群数量、访花频率综合判断,大和切叶蜂是披针叶黄华优势传粉蜂.     

大和切叶蜂对其蜜源植物披针叶黄华的盗蜜行为

【目的】调查和观测内蒙古毛乌素沙地大和切叶蜂Megachile (Xanthosaurus) japonica Alfken对其蜜源植物披针叶黄华Thermopsis lupinoides (L.)的盗蜜行为。【方法】在披针叶黄华花期内, 设置样方观测披针叶黄华的主要访花昆虫。采用目测, 拍照等方法对大和切叶蜂盗蜜行为进行观测, 记录和统计花被盗蜜后留下的盗蜜孔的数量和在花上的位置。【结果】大和切叶蜂在披针叶黄华传粉蜂中数量上占有绝对的优势。作为初级盗蜜者时, 用上颚在花基部切割出一个纵向裂口, 将口器伸入孔内吸取花蜜。作为次级盗蜜者时, 利用已有的孔洞来吸蜜。在盗蜜时没有表现出寻找已经存在的盗蜜孔来吸蜜的现象, 同时其个体在盗蜜时表现出“偏好”花基部一侧的行为。在13个样地, 已开放花朵被盗蜜率最低为95.4%, 最高达到100%, 而未开放花朵的被盗蜜率最高则达到64.7%。【结论】在毛乌素沙地大和切叶蜂既是披针叶黄华的主要传粉者, 也是其初级盗蜜者和次级盗蜜者。     

Effects of nectar-robbing on plant reproduction and evolution

The relationship between plant and pollinator is considered as the mutualism because plant benefits from the pollinator's transport of male gametes and pollinator benefits from plant's reward.Nectar robbers are frequently described as cheaters in the plant-pollinator mutualism,because it is assumed that they obtain a reward (nectar) without providing a service (pollination).Nectar robbers are birds,insects,or other flower visitors that remove nectar from flowers through a hole pierced or bitten in the corolla.Nectar robbing represents a complex relationship between animals and plants.Whether plants benefit from the relationship is always a controversial issue in earlier studies.This paper is a review of the recent literatures on nectar robbing and attempts to acquire an expanded understanding of the ecological and evolutionary roles that robbers play.Understanding the effects of nectar robbers on the plants that they visited and other flower visitors is especially important when one considers the high rates of robbing that a plant population may experience and the high percentage of all flower visitors that nectar robbers make to some species.There are two standpoints in explaining why animals forage on flowers and steal nectar in an illegitimate behavior.One is that animals can only get food in illegitimate way because of the mismatch of the morphologies of animals'mouthparts and floral structure.The other point of view argues that nectar robbing is a relatively more efficient,thus more energy-saving way for animals to get nectar from flowers.This is probably associated with the difficulty of changing attitudes that have been held for a long time.In the case of positive effect,the bodies of nectar robbers frequently touch the sex organs of plants during their visiting to the flowers and causing pollination.The neutral effect,nectar robbers' behavior may destruct the corollas of flowers,but they neither touch the sex organs nor destroy the ovules.Their behavior does not affect the fruit sets or seed sets of the hosting plant.Besides the direct impacts on plants,nectar robbers may also have an indirect effect on the behavior of the legitimate pollinators.Under some circumstances,the change in pollinator behavior could result in improved reproductive fitness of plants through increased pollen flow and out-crossing.     

Effects of nectar-robbing on plant reproduction and evolution

The relationship between plant and pollinator is considered as the mutualism because plant benefits from the pollinator’s transport of male gametes and pollinator benefits from plant’s reward. Nectar robbers are frequently described as cheaters in the plant-pollinator mutualism, because it is assumed that they obtain a reward (nectar) without providing a service (pollination). Nectar robbers are birds, insects, or other flower visitors that remove nectar from flowers through a hole pierced or bitten in the corolla. Nectar robbing represents a complex relationship between animals and plants. Whether plants benefit from the relationship is always a controversial issue in earlier studies. This paper is a review of the recent literatures on nectar robbing and attempts to acquire an expanded understanding of the ecological and evolutionary roles that robbers play. Understanding the effects of nectar robbers on the plants that they visited and other flower visitors is especially important when one considers the high rates of robbing that a plant population may experience and the high percentage of all flower visitors that nectar robbers make to some species. There are two standpoints in explaining why animals forage on flowers and steal nectar in an illegitimate behavior. One is that animals can only get food in illegitimate way because of the mismatch of the morphologies of animals’ mouthparts and floral structure. The other point of view argues that nectar robbing is a relatively more efficient, thus more energy-saving way for animals to get nectar from flowers. This is probably associated with the difficulty of changing attitudes that have been held for a long time. In the case of positive effect, the bodies of nectar robbers frequently touch the sex organs of plants during their visiting to the flowers and causing pollination. The neutral effect, nectar robbers’ behavior may destruct the corollas of flowers, but they neither touch the sex organs nor destroy the ovules. Their behavior does not affect the fruit sets or seed sets of the hosting plant. Besides the direct impacts on plants, nectar robbers may also have an indirect effect on the behavior of the legitimate pollinators. Under some circumstances, the change in pollinator behavior could result in improved reproductive fitness of plants through increased pollen flow and out-crossing. __________ Translated from Acta phytoecologiaca Sinica, 2006, 30(4): 695–702 [译自: 植物生态学报]     

Nectar robbers deter legitimate pollinators by mutilating flowers

Nectar robbing – harvesting nectar illegitimately – can have a variety of outcomes for plant sexual reproduction and for the pollinator community. Nectar robbers can damage flowers while robbing nectar, which could affect the behavior of subsequent flower visitors and, consequently, plant reproduction. However, only nectar manipulation by nectar robbers has so far received attention. We found a short-tongued bee, Hoplonomia sp. (Halictidae), mutilating the conspicuous lower petal of the zygomorphic flowers of Leucas aspera (Lamiaceae) while robbing nectar. We hypothesized that the mutilation of the conspicuous lower petal deters legitimate pollinators on L. aspera flowers, which, in turn, might affect plant reproduction. We first assessed the proportion of naturally-robbed flowers in plant populations for three years to confirm that it was not a purely local phenomenon due to a few individual bees. We then studied diversity, community and visitation characteristics of pollinators, nectar dynamics and fruit set in unrobbed and robbed open flowers in naturally-robbed populations. The proportion of robbed flowers varied significantly across sites and years. Robbing did not affect nectar dynamics in flowers, but it did alter flower morphology, so much so that it reduced pollinator visitation and altered the pollinator community on robbed flowers. However, the maternal function of plant reproduction was not affected by nectar robbing. This study for the first time shows that a nectar robber can have an ecologically significant impact on floral morphology.     

Pollination ecology of Anthyllis vulneraria subsp. vulgaris (Fabaceae): nectar robbers as pollinators

This paper examines the hypothesis that nectar robbing can affect plant reproductive success either positively or negatively. To this end, I investigated various aspects of the pollination ecology of a population of the herb Anthyllis vulneraria subsp. vulgaris in northwest Spain over 5 yr. By observing floral visitors, I found that the most important pollinator species was the long-tongued bee Anthophora acervorum, which accounted for ～45% of recorded insect visits. However, just over 45% of visits were by the nectar-robbing bumble bees Bombus terrestris and B. jonellus. Although the incidence of robbing differed considerably over 5 yr of study, the frequency in every season was very high (66.4-76.5% of robbing) except for 1997 (0% robbing). Despite this high frequency of robbing, robbed flowers had a higher probability of setting fruit than nonrobbed flowers in all years of the study (mean: 82.0 vs. 51.0%; excluding 1997). This increased fruit set in robbed flowers is directly related to bumble bee behavior because the robbers' bodies came into contact with both the anthers and stigmas while robbing. Thus, the robbers effect pollination. These results suggest that the effect of nectar robbers on plant reproductive success is dependent both on the robbers' behavior and on flower/inflorescence structure. The importance of nectar-robbing bumble bees on the reproductive success of A. vulneraria and its yearly high frequency suggest that the relationship between robbers and this plant is part of a successful long-term mutualism.     

Effects of nectar robbing on pollinator behavior and plant reproductive success of Pitcairnia angustifolia (Bromeliaceae)

Nectar robbers may have direct and indirect effects on plant reproductive success but the presence of nectar robbing is not proof of negative fitness effects. We combined census data and field experiments to disentangle the complex effects of nectar robbing on nectar production rates, pollinator behavior, pollen export, and female reproductive success of Pitcairnia angustifolia. Under natural conditions flowers were visited by four different animal species including a robber‐like pollinator and a secondary robber. Natural levels of nectar robbing ranged from 40 to 100%. Natural variation in nectar robbing was not associated with fruit set in any year whereas seed set was weakly positively associated for 1 year only. Artificial nectar robbing did not increase nectar production or concentration, did not affect the behavior of long‐billed hummingbirds, and when faced with artificially robbed flowers, these visitors behaved as secondary nectar robbers. The number of stigmas within a patch that received pollen dye analogs and the average distance traveled by these analogs were not significantly different between robbing treatments (robbed flowers versus unrobbed flowers), but the maximum distance traveled by these pollen analogs was higher when nectar robbing was not prevented. Overall, the proportion of robbed flowers on an inflorescence had a neutral effect to a weak positive effect on the reproduction of individual plants (i.e. positive association between nectar robbing and fruit set in 2002) even when it clearly changed the behavior of its most efficient pollinator potentially increasing the frequency of nectar robbing within a plant.     

Pollination Ecology and Effect of Nectar Removal in Macleania bullata (Ericaceae)1

The floral syndrome of Macleania bullataYeo (Ericaceae) reflects its adaptation to hummingbird pollination. Its flowers, however, are subject to high levels of nectar robbing. I examined the floral visitor assemblage of M. bullata in a tropical montane wet forest in southwestern Colombia, focusing on the behavior of the visitors. I also tested for the presence of nocturnal pollination and the effects of nectar removal on new nectar production. The principal floral visitors were the nectar robbing hummingbirds Ocreatus underwoodii (19.1% of visits) and Chlorostilbon mellisugus (18.9%). Only two species of long–billed hummingbirds visited the flowers of M. bullata as “legitimate” pollinators: Coeligena torquata (14.7% of visits) and Doryfera ludoviciae (14.3%). The remaining visits constituted nectar robbing by bees, butterflies, and other species of hummingbirds. Nocturnal pollination took place, although fruit set levels were 2.4 times higher when only diurnal pollination was allowed as opposed to exclusively nocturnal pollination. Nectar robbers removed floral nectar without pollinating the flower. Treatments of experimental nectar removal were carried out to examine if flowers synthesize more nectar after nectar removal. Nectar removal increased the total volume of nectar produced by each flower without affecting sugar concentration. Thus, nectar robbing can impose a high cost to the plants by forcing them to replace lost nectar.     

Novel nectar robbing negatively affects reproduction in Digitalis purpurea

With many plant–pollinator interactions undergoing change as species’ distributions shift, we require a better understanding of how the addition of new interacting partners can affect plant reproduction. One such group of floral visitors, nectar robbers, can deplete plants of nectar rewards without contributing to pollination. The addition of nectar robbing to the floral visitor assemblage could therefore have costs to the plant´s reproductive output. We focus on a recent plant colonist, Digitalis purpurea, a plant that in its native range is rarely robbed, but experiences intense nectar robbing in areas it has been introduced to. Here, we test the costs to reproduction following experimental nectar robbing. To identify any changes in the behavior of the principal pollinators in response to nectar robbing, we measured visitation rates, visit duration, proportion of flowers visited, and rate of rejection of inflorescences. To find the effects of robbing on fitness, we used proxies for female and male components of reproductive output, by measuring the seeds produced per fruit and the pollen export, respectively. Nectar robbing significantly reduced the rate of visitation and lengths of visits by bumblebees. Additionally, bumblebees visited a lower proportion of flowers on an inflorescence that had robbed flowers. We found that flowers in the robbed treatment produced significantly fewer seeds per fruit on average but did not export fewer pollen grains. Our finding that robbing leads to reduced seed production could be due to fewer and shorter visits to flowers leading to less effective pollination. We discuss the potential consequences of new pollinator environments, such as exposure to nectar robbing, for plant reproduction.     

Nectar robbing: a common phenomenon mainly determined by accessibility constraints,nectar volume and density of energy rewards

Nectar robbers use a hole made in the perianth to extract nectar. Since robbers may modify plant fitness, they play an important role by driving evolution on floral traits, shaping population structure and influencing community dynamics. Although nectar robbing is widespread in angiosperms, the causes and ecological implications of this behaviour on large ecological scales are still unexplored. Our aim is to study the frequency of nectar robbing in plants of temperate and tropical regions and examine its association with plant traits. We characterised the levels of nectar robbing in 88 species of Mediterranean, Alpine, Antillean and Andean plant communities and identified the most important nectar robbers. We analysed associations between the levels of robbing and floral morphology, production and density of energy rewards, mechanisms of protection against nectar robbers, plant life form and geographic origin. Nectar robbing was present at all sampling sites. Within communities two patterns of robbing levels related to the diversity and specialization of robbers were detected. In most communities one plant species presented very high levels of robbing while other species had intermediate to low robbing levels. There, nectar robbers are opportunists, robbing highly rewarding plants. In the Andean community the high specialization of several co‐existing flowerpiercers produced an even pattern of robbing levels in the plant community. Plants with long flowers, abundant nectar and a high energy density are more likely to be robbed by both insects and birds. A high aggregation of the flowers within the plants and the presence of long calyxes and bracts are associated to low robbing rates by insects and to a lesser extent by birds. Besides the morphological constraints that operate on a single flower basis, nectar robbing is a phenomenon dependent upon the density of energy rewards reflecting the presence of mechanisms on higher ecological scales.     

Dynamics of plant–pollinator–robber systems

Plant–pollinator–robber systems are considered, where the plants and pollinators are mutualists, the plants and nectar robbers are in a parasitic relation, and the pollinators and nectar robbers consume a common limiting resource without interfering competition. My aim is to show a mechanism by which pollination–mutualism could persist when there exist nectar robbers. Through the dynamics of a plant–pollinator–robber model, it is shown that (i) when the plants alone (i.e., without pollination–mutualism) cannot provide sufficient resources for the robbers’ survival but pollination–mutualism can persist in the plant–pollinator system, the pollination–mutualism may lead to invasion of the robbers, while the pollinators will not be driven into extinction by the robbers’ invasion. (ii) When the plants alone cannot support the robbers’ survival but persistence of pollination–mutualism in the plant–pollinator system is density-dependent, the pollinators and robbers could coexist if the robbers’ efficiency in translating the plant–robber interactions into fitness is intermediate and the initial densities of the three species are in an appropriate region. (iii) When the plants alone can support the robbers’ survival, the pollinators will not be driven into extinction by the robbers if their efficiency in translating the plant–pollinator interactions into fitness is relatively larger than that of the robbers. The analysis leads to an explanation for the persistence of pollination–mutualism in the presence of nectar robbers in real situations.