Fungal Endophytes in Oak Trees: Long-Term Patterns of Abundance and Associations with Leafminers

Abstract

Endophytic fungi inhabiting foliage of woody plants are diverse and abundant, yet little is known of their temporal and spatial variation or their interactions with more commonly studied invertebrate and vertebrate macroherbivores. We studied seasonal and yearly variation in endophyte infections in five Emory oak trees over a 4-yr period from 1989 to 1993. In the 1992–1993 growing season, we documented seasonal patterns of abundance of the three most common fungal endophyte species, an ascomycete, Ophiognomonia cryptica, and two coelomycete species, Plectophomella sp. and Asteromella sp. To determine the association of fungal endophytes with macroherbivores, we compared infection frequencies of endophytes in unmined leaves and leaves harboring living and dead larval leafminers of Cameraria sp. nov., the dominant macroherbivore on Emory oak, over the 4-yr period. In the 1992–1993 growing season, we monitored survival and mortality of leafmining larvae on the five study trees. We then determined the association of total infections and infections by individual endophyte species with seasonal survival and sources of mortality of leafminers. Infection levels of endophytes varied over the 4-yr period, but seasonal patterns within years were consistent. The three dominant species of endophytes varied differently in frequencies over the growing season. Leafminers were positively associated with endophytic infections in all years. In two of the four years, leaves with living leafmining larvae had greater total infection frequencies than unmined leaves. In one of these years, infection frequencies were greater in leaves with dead larvae than in those with living larvae, suggesting that endophytes may increase mortality of leafminers. However, when infection levels of individual species were compared among leaf types, only levels of Asteromella were greater in mined leaves relative to unmined ones. This difference was explained largely by higher infection levels in leaves with living larvae than in leaves with dead larvae. Furthermore, seasonal changes in endophyte levels varied independently from seasonal changes in leafminer mortality from unexplained causes or natural enemies. We conclude that leafmining activity is associated with higher endophyte infections, but increased infections are not associated with increased leafminer mortality. Higher infections on mined leaves are likely caused by leafmining damage that enhances fungal colonization and penetration into oak leaves. Although endophytes of Emory oak are diverse and abundant and their presence is associated with leafmining activity, we do not find strong correlative evidence that endophytes interact mutualistically with Emory oak by increasing resistance to a dominant herbivore, the leafminer Cameraria. A companion paper (Faeth and Hammon 1997) corroborates experimentally the lack of antagonistic interaction between endophytes and the leafminer.