The interplay between defaunation and phylogenetic diversity affects leaf damage by natural enemies in tropical plants

Abstract

Natural enemies play an important role in controlling plant population growth and vegetation dynamics. Tropical rainforests host the greatest diversity of herbivores, from large mammalian ungulates to microscopic pathogens, generating and maintaining plant diversity. By feeding on the same resources, large mammalian herbivores may interfere with plant consumption and leaf damage by important enemy guilds such as invertebrate herbivores and pathogens, triggering indirect trophic cascades. However, the impact of local extinctions of large herbivores on plant–enemy interactions is relatively unknown. We experimentally tested the effects of defaunation of large mammalian herbivores (e.g. peccaries, tapirs and brocket deer; hereafter, large herbivores) on the leaf damage of 3350 understorey plants in tropical rainforests of Brazil. We examined leaf damage in 10,050 leaves from 333 morphospecies by assigning the area consumed or damaged by five guilds of insect herbivores and leaf pathogens within 86 paired open-closed plots and investigating the joint effects of defaunation and plant phylogenetic diversity. Plants released from large herbivores had 9% less leaf damage; this difference was due to the lower leaf pathogens incidence (29%) rather than insect herbivory. Evolutionary distinctness was positively correlated with leaf damage in a similar way in all treatments, suggesting additive effects of defaunation and phylogenetic diversity. Total and pathogenic leaf damage (but not insect damage) decreased with plant richness across treatments, and large herbivores exclusion resulted in increased plant species richness. This suggests that large herbivores exclusion leads to a dilution of total and pathogens' leaf damage by increasing plant species richness. Our results suggest that indirect effects of large herbivores decrease the dilution potential of plant communities against pathogens and rather reinforce their top-down impact on vegetation, demonstrating a previously overlooked cascading effect of large herbivore extinction on forest ecosystems. Synthesis: The extinction of large mammalian herbivores can lead to a decrease in pathogen-driven leaf damage, a previously unknown indirect effect in forest ecosystems, which might have consequences for plant fitness and ultimately for plant diversity. Large herbivores and plant pathogens might have synergistic effects in regulating the diversity of plant communities in some of the most diverse ecosystems on Earth.