Evaluating endophyte-rich leaves and leaf functional traits for protection of tropical trees against natural enemies

Plants use physical barriers and chemical compounds to defend themselves against natural enemies. For instance, tough leaves are considered to be better defended than soft leaves, part of a spectrum of defences defined by functional traits such as leaf chemistry, lifespan, toughness and leaf mass per area (LMA). Plants with longer lifespans, which invest more in leaf tissue and higher LMA, typically feature robust constitutive defences (e.g. toughness, thickness and dense cell walls). In contrast, plants with lower LMA and more leaf nutrients often invest more in induced defences. Leaf traits represent an environmental filter for foliar endophytic fungi (FEF), which may play an additional role in plant defence. Our overarching assumption is that FEF alter leaf fate by interacting directly or indirectly with leaf traits, thus shaping successive FEF colonization, development of leaf traits and response to plant enemies. To evaluate this hypothesis, we inoculated seedlings of seven tropical tree species, which varied in leaf traits, with natural and diverse endophyte communities. We characterized leaves by low FEF load (E-low) and high FEF load (E-high) based on culturing and culture-free amplicon sequencing. We measured leaf removal by leaf-cutter ants and leaf necrosis due to a generalist fungal pathogen. Across the experiment, we observed greater leaf removal from the E-low treatment compared to the E-high treatment, but no difference in pathogen damage. Dimensionality reduction of leaf functional traits (i.e. LMA, toughness, thickness and anthocyanin levels) revealed relationships among traits and distinct host species characteristics. All leaf functional traits had significant correlations with FEF community composition. In turn, indicator species analyses revealed functional traits and taxonomic identities of FEF associated with high and low leaf damage by natural enemies. Our findings highlight the complex dynamics of plant-herbivore-pathogen relationships and underscore the importance of endophytes as a potentially low-cost, preemptive defence strategy for plants, especially during early growth stages. These insights shed light on the nuanced role of endophytes in plant ecology. Further, they open avenues for future research, particularly in exploring strategic resource allocation in plants and the specific contributions of endophytes to plant resilience. Read the free Plain Language Summary for this article on the Journal blog.