Grazers affect selection on inflorescence height both directly and indirectly and effects change over time

Selection mediated by one biotic agent will often be modified by the presence of other biotic interactions, and the importance of such indirect effects might change over time. We conducted an 11-year field experiment to test the prediction that large grazers affect selection on floral display of the dimorphic herb Primula farinosa not only directly through differential grazing damage, but also indirectly by affecting vegetation height and thereby selection mediated by pollinators and seed predators. Exclusion of large grazers increased vegetation height and the strength of pollinator-mediated selection for tall inflorescences and seed predator-mediated selection for short inflorescences. The direct effect of grazers on selection resulting from differential grazing damage to the two scape morphs showed no temporal trend. By contrast, the increase in vegetation height in exclosures over time was associated with an increase in selection mediated by pollinators and seed predators. In the early years of the experiment, the indirect effects of grazers on selection mediated by pollinators and seed predators were weak, whereas at the end of the experiment, the indirect effects were of similar magnitude as the direct effect due to differential grazing damage. The results demonstrate that the indirect effects of a selective agent can be as strong as its direct effects, and that the relative importance of direct vs. indirect effects on selection can change over time. A full understanding of the ecological processes governing variation in selection thus requires that both direct and indirect effects of biotic interactions are assessed.

单一生物作用因子所介导的选择作用，往往会因其他生物交互作用的存在而发生修饰，且这类间接效应的重要性可能随时间推移发生变化。我们开展了一项为期11年的野外实验，以验证如下预测：大型植食动物对二型性草本植物粉报春（Primula farinosa）的花展示选择作用，不仅可通过差异化取食伤害直接产生影响，还可通过改变植被高度，进而经由传粉者和种子捕食者介导的选择过程产生间接效应。排除大型植食动物后，样地植被高度升高，且针对高花序的传粉者介导选择强度、针对矮花序的种子捕食者介导选择强度均有所增强。植食动物因对两种花葶形态型造成差异化取食伤害而对选择产生的直接效应，未表现出时间趋势。与之相反，围栏排除样地中随时间推移出现的植被高度升高，与传粉者和种子捕食者介导的选择强度增加显著相关。实验早期，植食动物经由传粉者和种子捕食者介导的间接选择效应较为微弱；而在实验末期，这类间接效应的强度已与差异化取食伤害带来的直接效应相当。研究结果表明，选择因子的间接效应可与直接效应强度相当，且直接与间接效应对选择作用的相对重要性可随时间发生变化。因此，要全面解析调控选择作用变异的生态过程，必须同时评估生物交互作用的直接与间接效应。