Avoidance of High-Endophyte Space by Gall-Forming Insects

Abstract

Endophytic fungi and phytophagous insects derive energy from shared host plants, and so are likely to interact with one another. Several authors have proposed that fungal endophytes of woody perennials, like endophytes of grasses, have a mutualistic association with their host and provide enhanced protection from herbivory. However, there have been few tests of this hypothesis, and most studies have focused on correlating the presence of endophytes and herbivores. We investigated a system where an endophyte was known to cause significant mortality on one species of gall-forming insect (Besbicus mirabilis), but not another (Bassettia ligni) that occupies the same plant host. We predicted that gall insects should avoid high-endophyte space and that mortality would be lowest in low-endophyte space if endophytes protect plants from herbivory. We used the spatial location, temporal infection patterns, and within-leaf growth activity of the endophyte as elements of endophyte space. Besbicus mirabilis avoided high-endophyte space at the within-leaf scale by occupying part of the leaf where endophyte infection and endophyte-caused mortality were predictably low. However, the within-leaf position was under opposing selection pressure from mortality caused by grazing herbivores and developmental constraints, so the gall did not occupy the region of the leaf where both infection and endophyte-caused mortality were the lowest. B. ligni was spatially correlated within leaves with the presence of the endophyte but suffered almost no endophyte-caused mortality. However, B. ligni occupies the leaf lamina, where the endophyte has no growth activity, in contrast to the leaf midrib, where B. mirabilis galls are found. Further, B. ligni emerges from the gall just as endophyte infection levels reach a peak, so this species temporally avoids prolonged contact with highly infected tissue. However, the between-leaf distributions of both insects were independent of endophyte infection. Fungal endophytes influence the spatial patterns of insect distributions, but at different scales. Growth activity of the endophyte may also play a role, and simply examining presence/absence correlations of insects may be misleading.