Cascading effects of a highly specialized beech-aphid–fungus interaction on forest regeneration

Specialist herbivores are thought to often enhance or maintain plant diversity within ecosystems, because they prevent their host species from becoming competitively dominant. In contrast, specialist herbivores are not generally expected to have negative impacts on non-hosts. However, we describe a cascade of indirect interactions whereby a specialist sooty mold (Scorias spongiosa) colonizes the honeydew from a specialist beech aphid (Grylloprociphilus imbricator), ultimately decreasing the survival of seedlings beneath American beech trees (Fagus grandifolia). A common garden experiment indicated that this mortality resulted from moldy honeydew impairing leaf function rather than from chemical or microbial changes to the soil. In addition, aphids consistently and repeatedly colonized the same large beech trees, suggesting that seedling-depauperate islands may form beneath these trees. Thus this highly specialized three-way beech-aphid-fungus interaction has the potential to negatively impact local forest regeneration via a cascade of indirect effects.