Complementary effects of two plant defence traits on behaviour and performance of monarch butterfly caterpillars

Abstract

Plants have evolved multiple defensive traits in response to herbivory; in turn, herbivore specialists evolved adaptive behaviours to avoid or tolerate such defences. Here, we employ milkweeds (Asclepias spp.) to test two defences, latex and trichomes, for their independent and interactive effects on behaviour and performance of monarch caterpillars (Danaus plexippus). Latex exuded upon damage and the density of leaf trichomes positively correlate across milkweed species, suggesting they may have evolved together as synergistic defences. Nonetheless, the complementary roles of these two traits have been little-studied. We focus on two behaviours: shaving, or the removal of trichomes, and chewing, which encompasses both deactivation of latex and leaf consumption. In an experiment with seven milkweed species, with and without manipulated latex flow, we found latex to be the primary determinant of reducing chewing, while both defences positively predicted shaving behaviour in the first instar. Next, we conducted a factorial experiment throughout the first three instars, manipulating latex and trichomes on a high-latex, high-trichome species, the woolly milkweed Asclepias vestita. On plants with latex and trichomes intact, caterpillars spent the most time shaving and least time chewing of all treatment groups, suggesting a possible synergism. These defence-driven behavioural effects decreased later in larval development. Latex and trichomes both impacted monarch performance, additively increasing mortality and reducing growth of survivors. Thus, latex and trichomes represent two important plant defences with effects on specialist herbivore behaviour and implications for insect fitness.