Large differences in herbivore performance emerge from simple herbivore behaviors and fine-scale spatial heterogeneity in phytochemistry

Patterns of phytochemistry localization in plant tissues are diverse within and across leaves. These spatial heterogeneities are important to the fitness of herbivores, but their effects on herbivore foraging and dietary experience remain elusive. We manipulated the spatial variance and clusteredness of a plant toxin in a synthetic diet landscape on which individual caterpillars fed. We monitored caterpillars with cameras across most of their larval development. Caterpillars that fed on diets with a lower spatial variance and more clustered arrangement of toxins had overall worse performance, mostly because those caterpillars ate less, moved more, ingested more toxin, or failed to physiologically acclimate. Using empirically parameterized individual-based models, we found that differences in movement out of, not towards, less toxic food, drove a body size dependent effect of clusteredness. Hence, the spatial pattern of phytochemicals itself, beyond mean concentration, can have important consequences for herbivores through complex interactions with herbivore foraging.