Pollinator-transmitted pathogens typically hinder sexual reproduction of their hosts and affect pollen flow among remaining healthy individuals in a population. The extent to which a pathogen also influences host’s population growth depends on the importance of sexual reproduction for the host’s life cycle. Such pathogen impact cannot be traced by measuring only the vital rates directly affected by the pathogen, and thus a study of the host’s entire life cycle is necessary. In this study, we aimed to quantify the effects of the pollinator-transmitted anther smut pathogen Microbotryum carthusianorum on population growth rate in three populations of the long-lived perennial Dianthus carthusianorum. We followed plant individuals over three years and measured their size, disease state, and reproduction. We then constructed an Integral Projection Model (IPM). To evaluate the pathogen impact, we performed a stochastic analysis of the IPM for real diseased populations as well as for simulated populations without the pathogen. As the populations also hosted predispersal seed predators, the same approach was used to evaluate their impact. Stochastic population growth rates indicated two of the real populations to be increasing, and one to be declining. Comparison with the simulated healthy populations showed that the pathogen impact on the growth rate was negative and relatively strong, because the growth rate was highly sensitive to changes in sexual reproduction. However, the pathogen did not appear to cause the decline in the one decreasing population, since the growth rate there was impaired more substantially by high rates of predispersal seed predation and low germination rates than by the castration of diseased flowers. Overall, our study suggests that D. carthusianorum is highly vulnerable to biotic interactions affecting sexual reproduction pathway. Additionally, our study illustrated several complexities in disease dynamics (e.g., occurrence of partially or fully asymptomatic plants) that need to be incorporated into the assessment of the impact of pollinator-transmitted pathogens on long-lived perennials.

传粉媒介传播的病原体通常会阻碍其宿主的有性繁殖，并影响种群中其余健康个体之间的花粉流动。病原体对宿主种群增长的影响程度取决于有性繁殖对宿主生命周期的重要性。这种病原体的影响不能通过仅测量直接受病原体影响的生命率来追踪，因此有必要研究宿主的整个生命周期。在这项研究中，我们旨在量化传粉者传播的花药黑穗病病原体Microbotryum carthusianorum对长寿多年生石竹 carthusianorum 三个种群种群增长率的影响。我们跟踪植物个体超过三年，并测量了它们的大小、疾病状态和繁殖情况。然后我们构建了一个整体投影模型 (IPM)。为了评估病原体的影响，我们对真实患病人群以及没有病原体的模拟人群进行了 IPM 随机分析。由于这些种群还拥有传播前的种子捕食者，因此使用相同的方法来评估它们的影响。随机人口增长率表明两个实际人口在增加，一个在下降。与模拟的健康种群比较表明，病原体对生长速度的影响是负的，且影响较大，因为生长速度对有性生殖的变化高度敏感。然而，病原体似乎并没有导致一个正在减少的种群的减少，因为与病花的阉割相比，传播前种子捕食率高和发芽率低对那里的生长速度的损害更大。总的来说，我们的研究表明D. carthusianorum极易受到影响有性繁殖途径的生物相互作用的影响。此外，我们的研究还说明了疾病动力学中的几种复杂性（例如，部分或完全无症状植物的发生），需要将这些复杂性纳入评估传粉者传播的病原体对长寿多年生植物的影响中。