Food plant–associated predation risk and its impact on larval development and adult morphology in a specialist butterfly

Abstract Predation influences herbivore behaviour, physiology and reproductive success through both direct consumption and non‐lethal effects arising from predation risk alone. Plant traits, including defensive traits and architecture, can also influence herbivores both directly and indirectly, either by affecting feeding efficiency or by affecting herbivores' risk of predation. However, it remains unclear how predators and plant traits interact to shape the developmental outcomes of larval herbivores, particularly under field conditions. To understand larval performance within a tritrophic framework, we investigated how predation risk and food‐plant identity influence caterpillar development and subsequent adult morphology using the monarch butterfly ( Danaus plexippus ) as a focal species. We compared responses to predation risk in monarch caterpillars feeding on two common species of western milkweed, Asclepias speciosa and Asclepias fascicularis , which differ in various traits, including defensive traits and architectural complexity. Using an outdoor common garden experiment in two growing seasons, caterpillars were assigned to plants of each of the two species with or without a predator‐exclusion cage. Interestingly, we observed trends of slower weight gain in caterpillars feeding on A . speciosa than in those feeding on A . fascicularis , but only when caterpillars were exposed to predators. Additionally, in the first year of our study, predator exposure increased caterpillar development time on A. speciosa , but not on A. fascicularis . Predator exposure on A . speciosa was associated with reduced larval weight gain in the second year of our study, and because larval weight gain strongly predicted adult wing area, this pattern suggests a potential indirect effect of predators on wing size. In contrast, predator exposure had no detectable effect on the wing morphometrics of adults that had developed on A . fascicularis . Our findings highlight that larval food‐plant species can modulate the magnitude of predator effects at multiple life stages of an insect herbivore. This demonstrates that developmental changes associated with predator exposure can depend on the identity of the larval food‐plant and can carry forward to affect adult morphology, with potential implications for the fitness of migratory insects.