Tri-trophic interactions in a plant-arthropod-parasitoid system drive spatial patterns of herbivory in a temperate forest

Background/Question/Methods

: Historically, analysis of the Janzen-Connell hypothesis and negative conspecific density dependence have focused solely on the interactions between plants and their natural enemies. While many enemies of plants, such as fungi or viruses, rarely have enemies of their own, others, such as insects, do. Larval lepidoptera, the caterpillars of moths and butterflies, are simultaneously responsible for controlling the populations of plants, while also being controlled by birds, parasitoids, ants, and disease. This aspect of negative conspecific density dependence – the tri-trophic interactions among multiple levels of natural enemies – has remained largely uninvestigated. Potentially, as plant density increases, so will herbivore density, leading to an increase in predation rates, and ultimately a lower rate of herbivory on densely-clustered plants. Here, I present a study investigating how the spatial structure of a common New England forest tree (witch hazel, Hamamelis virginiana) affects not only the distribution and density of two H. viginiana specialist caterpillars (mustard sallow, Pyreferra hesperidago and three-spotted nola, Nola triquetrana), but also the rate at which those caterpillars are killed by parasitoid wasps and flies (Brachonidae, Ichneumonidae, and Tachinidae). I sampled 415 H. virginiana trees and reared 861 caterpillars to death or pupation, with 292 of those caterpillars ultimately succumbing to parasitoidism. Additionally, I mapped over 3500 H. virginiana trees with <1m precision to directly address how the spatial structure of these trees affected the observed patterns.

Results/Conclusions

: As H. virginiana density increases, the densities of P. hesperidago and N. triquetrana do not change, but the incidence of parasitoidism on the two species dramatically increases. Ultimately, when caterpillars that succumb to parasitoidism are removed, H. virginiana in dense clusters face much lower herbivory pressure than those in sparser stands. As herbivorous insects are systematically sought and killed on plants in dense patches, H. virginiana may actually experience positive conspecific density dependence. This study may shed light on why the effects of negative conspecific density dependence are widely accepted in tropical systems, but less so in temperate systems. Furthermore, this study opens the door to future experiments investigating the role of herbivorous insects and parasitoid predators in systems with novel, invasive host plants.