Urbanization Effects on Plant Parasitism: A Multi-Regional Comparison of Endemic Occurrence and Outbreak Intensity

Microbial and insect parasitism plays a crucial role in shaping plant communities. The urban stress hypothesis posits that urbanization increases parasitism owing to the physiological environment, whereas the habitat fragmentation hypothesis suggests that habitat fragmentation in urban areas suppresses disease transmission. In the epidemiological triangle (comprising pathogen occurrence, environment, and host susceptibility as determinants of outbreak intensity), the habitat fragmentation hypothesis primarily influences parasitism occurrence, whereas the urban stress hypothesis mainly affects outbreak intensity. In this study, we aimed to distinguish between these two hypotheses by formulating an epidemiological triangle using zero-inflated binomial regression based on surveys of herb layer plant communities along urban-rural gradients in Japan and China. In general, urbanization enhanced parasitism. Strong seasonal signatures found in natural ecosystems were generally the same as those in cultivated crops. When all types of parasitism (powdery mildew-like, rust-like, spot-forming diseases, leaf-eating, and other insects) were combined, urbanization enhanced outbreak intensity, supporting the urban stress hypothesis, and suppressed endemic occurrence, supporting the habitat fragmentation hypothesis. Notable exceptions included a significantly high endemic occurrence in powdery mildew-like diseases and in the combined analysis of all insect pests. This may be because ruderal host plant habitats are fragmented in forest-dominated landscapes. Additionally, rich nitrogen deposition in urban areas may explain the generally higher outbreak intensity, although reducing hyperparasites and carnivorous species can cause complicated effects. These findings provide the new ecological consequences of urbanization, offering a framework for understanding plant-parasite dynamics in cross-regional perspective and informing strategies for sustainable urban planning.