Does Plant Origin Influence the Fitness Impact of Flower Damage? A Meta-Analysis

Herbivory has been long considered an important component of plant-animal interactions that influences the success of invasive species in novel habitats. One of the most important hypotheses linking herbivory and invasion processes is the enemy-release hypothesis, in which exotic plants are hypothesized to suffer less herbivory and fitness-costs in their novel ranges as they leave behind their enemies in the original range. Most evidence, however, comes from studies on leaf herbivory, and the importance of flower herbivory for the invasion process remains largely unknown. Here we present the results of a meta-analysis of the impact of flower herbivory on plant reproductive success, using as moderators the type of damage caused by floral herbivores and the residence status of the plant species. We found 51 papers that fulfilled our criteria. We also included 60 records from unpublished data of the laboratory, gathering a total of 143 case studies. The effects of florivory and nectar robbing were both negative on plant fitness. The methodology employed in studies of flower herbivory influenced substantially the outcome of flower damage. Experiments using natural herbivory imposed a higher fitness cost than simulated herbivory, such as clipping and petal removal, indicating that studies using artificial herbivory as surrogates of natural herbivory underestimate the real fitness impact of flower herbivory. Although the fitness cost of floral herbivory was high both in native and exotic plant species, floral herbivores had a three-fold stronger fitness impact on exotic than native plants, contravening a critical element of the enemy-release hypothesis. Our results suggest a critical but largely unrecognized role of floral herbivores in preventing the spread of introduced species into newly colonized areas.

植食作用长期以来被视作动植物互作的关键组分，可影响入侵物种在新生境中的定殖成功概率。联结植食作用与生物入侵过程的核心假说之一为天敌释放假说（Enemy Release Hypothesis），该假说提出，外来植物因在原生分布区脱离了专性天敌，故而在入侵范围内遭受的植食危害与对应的适合度代价均更低。然而，现有绝大多数实证证据均来自叶片植食作用相关研究，花部植食作用对生物入侵过程的重要性仍未得到充分探明。本研究针对花部植食作用对植物繁殖成功的影响开展元分析（meta-analysis），以花植食性动物造成的损伤类型与植物物种的定居状态作为调节变量。我们共筛选出符合纳入标准的论文51篇，同时纳入本实验室未公开数据中的60条记录，总计得到143个案例研究样本。研究结果显示，花植食作用与盗蜜行为均会对植物适合度产生显著负面影响。花部植食作用相关研究采用的实验方法，会对花损伤的实验结果造成显著影响：使用自然植食处理的实验，其测得的植物适合度代价高于修剪、去除花瓣等模拟植食操作的实验，这表明以人工植食作为自然植食替代物的研究，会低估花部植食作用对植物适合度的真实影响强度。尽管花部植食作用带来的适合度代价在本土植物与外来植物中均处于较高水平，但花植食性动物对外来植物的适合度影响强度是本土植物的三倍，这与天敌释放假说的核心论断相矛盾。本研究结果表明，花植食性动物在阻止外来物种扩散至新定殖区域方面，发挥着关键却长期未被学界充分认知的重要作用。