Anther smut pathogens as important drivers of population dynamics of long-lived perennial plants: A case study of Dianthus carthusianorum

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.