Tri-trophic effects of plant defenses: chickadees consume caterpillars based on host leaf chemistry

Few studies have addressed how plant chemical defenses that directly affect herbivores in turn affect consumption patterns of vertebrates at higher trophic levels. We studied how variable foliar chemistry of trembling aspen (Populus tremuloides Michx.) affects the diet preferences of an avian insectivore feeding on an introduced herbivore, the gypsy moth (Lymantria dispar L.). Black-capped chickadees (Poecile atricapilla ) were offered paired choices of gypsy moth caterpillars feeding on one of three genotypes of aspen that differed in chemical composition. Chickadees chose to eat caterpillars fed aspen foliage with low levels of both condensed tannins and phenolic glycosides, or caterpillars fed foliage with high levels of tannins and low levels of phenolic glycosides, over caterpillars fed foliage with low levels of condensed tannins and high levels of phenolic glycosides. In addition, diet choices of the birds were affected by their previous experience. These findings are consistent with the ‘‘extended phenotype’’ concept, in that genetically-based chemical traits in an ecologically dominant plant influence the feeding behavior of third trophic level organisms, whose efficacy as regulators of herbivore populations may in turn be modified.